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close this bookFood and Nutrition Bulletin Volume 17, Number 4, 1996 (UNU, 1996, 163 p.)
View the documentForeword
View the documentSolemn Papal Audience
View the documentAddress to the Holy Father
Open this folder and view contentsEstablishing lactation
Open this folder and view contentsImpact on fertility
Open this folder and view contentsInfection and disease
Open this folder and view contentsSocial and demographic aspects
View the documentBooks received
View the documentNote for contributors
View the documentNote à l'intention des auteurs
View the documentNota para posibles autores
View the documentTitle of interest

Foreword

Recognizing the nutritional and immunologic benefits of breastfeeding to infants and the health benefits of lactation to mothers, the Pontifical Academy of Sciences and The Royal Society co-sponsored a Working Group that met in Vatican City 11-13 May 1995. The meeting brought together a multidisciplinary group of scientists engaged in social and biological research and in the clinical study of lactation. The purpose of the meeting was to create a forum for the presentation of accumulated research and to conduct a high-level scientific discussion of its implications. The Food and Nutrition Bulletin has provided the opportunity to publish the papers and the discussions, thereby making them available to a wider audience. We are profoundly grateful to the publishers for their cooperation, assistance, and patience in preparing the manuscripts.

We are grateful to the participants for their studies and their work in preparing their presentations. The papers and discussions address available scientific data in a competent and objective fashion. They do not represent the official teaching of the Roman Catholic Church or the moral and pastoral application of that teaching. Nor do they represent the official positions of The Royal Society or the policies of the United Kingdom. The workshop's aim was a comprehensive overview that met the highest scientific standards. We are confident it will be of great value to scholars, clinicians, and all others who work daily to enrich the lives of mothers and infants.

Dr. Ann McLaren
The Royal Society

Msgr. Renato Dardozzi
Pontifical Academy of Sciences

PONTIFICIA ACADEMIA SCIENTIARUM
THE ROYAL SOCIETY

Solemn Papal Audience

On the morning of 12 May 1995, His Holiness John Paul 11 granted a Solemn Audience in the Apostolic Palace of the Vatican to the participants the Working Group on "Breastfeeding: Science and Society."

The group, introduced by His Excellency Msgr. James T. McHugh, Bishop of Camden, New Jersey, USA, was paternally received by the Holy Father, who at the end of the Audience greeted all the participants.

The Holy Father pronounced the following discourse:

Your Eminences,
Your Excellencies,
Ladies and Gentlemen,

  1. As always, it is a great pleasure to meet the distinguished participants in the study sessions organized by the Pontifical Academy of Sciences, and I thank Bishop James McHugh for his kind words of introduction. Today I am especially happy to extend my appreciation to The Royal Society, which has cosponsored this significant meeting.

True to its purpose and statutes, the Pontifical Academy of Sciences addresses itself to a wide range of scientific, social, and ethical issues which have a bearing on the Church's service to the human family, a service which springs from the fundamental Gospel commandment of love. The Academy plays a resourceful role in helping the Church, in particular the Holy See, to fulfil this task of service with the benefit of the most expert scientific knowledge and insights. Your studies and enquiries contribute to the Church's supreme effort to journey hand in hand with humanity on its path through temporal realities towards man's great and inexorable transcendent destiny.

  1. On this occasion you have been invited to share your expertise on the specific subject of "Breastfeeding: Science and Society," as a part of the overall study which the Academy has been pursuing since 1990 on Population and Resources. As scientists you direct your enquiry towards a better understanding of the advantages of breastfeeding for the infant and for the mother. As your Working Group can confirm, in normal circumstances these include two major benefits to the child: protection against disease and proper nourishment. Moreover, in addition to these immunological and nutritional effects, this natural way of feeding can create a bond of love and security between mother and child, and enable the child to assert its presence as a person through interaction with the mother.

All of this is obviously a matter of immediate concern to countless women and children, and something which clearly has general importance for every society, rich or poor. One hopes that your studies will serve to heighten public awareness of how much this natural activity benefits the child and helps to create the closeness and maternal bonding so necessary for healthy child development. So human and natural is this bond that the Psalms use the image of the infant at its mother's breast as a picture of God's care for man [1]. So vital is this interaction between mother and child that my predecessor Pope Pius XII urged Catholic mothers, if at all possible, to nourish their children themselves [2]. From various perspectives, therefore, the theme is of interest to the Church, called as she is to concern herself with the sanctity of life and of the family.

  1. Worldwide surveys indicate that two-thirds of mothers still breastfeed, at least to some extent. But statistics also show that there has been a fall in the number of women who nourish their infants in this way, not only in developed countries where the practice almost has to be reinstituted, but also increasingly in developing countries. This decline is traced to a combination of social factors such as urbanization and the increasing demands placed on women, to health-care policies and practices, and to marketing strategies for alternative forms of nourishment.

Yet the overwhelming body of research is in favour of natural feeding rather than its substitutes.

Responsible international agencies are calling on governments to ensure that women are enabled to breastfeed their children for four to six months from birth and to continue this practice, supplemented by other appropriate foods, up to the second year of life or beyond [3]. Your meeting therefore intends to illustrate the scientific bases for encouraging social policies and employment conditions which allow mothers to do this.

In practical terms, what we are saying is that mothers need time, information, and support. So much is expected of women in many societies that time to devote to breastfeeding and early care is not always available. Unlike other modes of feeding, no one can substitute for the mother in this natural activity. Likewise, women have a right to be informed truthfully about the advantages of this practice, as also about the difficulties involved in some eases. Health-care professionals too should be encouraged and properly trained to help women in these matters.

  1. In the recent Encyclical Evangelium vitae I wrote that "A family policy must be the basis and driving force of all social policies ... It is also necessary to rethink labour, urban, residential, and social service policies so as to harmonize working schedules with time available for the family, so that it becomes effectively possible to take care of children and the elderly" [4].

Is this a vague utopia, or is it the obligatory path to the genuine well-being of society? Even this brief reflection on the very individual and private act of a mother feeding her infant can lead us to a deep and far-ranging critical rethinking of certain social and economic presuppositions, the negative human and moral consequences of which are becoming more and more difficult to ignore. Certainly, a radical reexamination of many aspects of prevailing socio-economic patterns of work, economic competitiveness, and lack of attention to the needs of the family is urgently necessary.

  1. I am therefore very grateful to all of you for offering your time and co-operation to this meeting co-sponsored by the Pontifical Academy of Sciences and The Royal Society. I look forward to the synthesis and report of your findings so that this information may be widely circulated to our Church agencies and interested institutions throughout the world. I pray for the success of your research and for your own personal well-being. May God's blessings of strength, joy, and peace be with each one of you and the members of your families.

References

1. Psalms 22:9. The Jerusalem Bible. New York: Doubleday, 1966.

2. Pius XII. Allocution to mothers, October 6, 1941. In: Monks of Solesmes, ed. The woman in the modern world. Boston, Mass, USA: The Daughters of St. Paul, 1959.

3. UNICEF. Children and development in the 1990s. A UNICEF sourcebook. New York: UNICEF, 1990.

4. John Paul II. Evangelium vitae. In: Origins 24(42), 6 April 1995. Washington, DC: Catholic News Service, 1995.

Address to the Holy Father

At the Solemn Audience granted to the Working Group participants on 12 May 1995, His Excellency Msgr. James T. McHugh, Bishop of Camden, NJ, USA, delivered the following address:

Most Holy Father,

I am pleased to present to you the participants in the Working Group on "Breastfeeding: Science and Society." The meeting of this Working Group is co-sponsored by the Pontifical Academy of Sciences and The Royal Society of London. The persons taking part in this meeting are physicians and scientists who are engaged in scientific research and who have accumulated much important data on the advantages of breastfeeding for both mother and child.

There is considerable evidence that breastfeeding provides proper nutrition for children and also protects the child against life-threatening infections in the earliest years of life. The mother also benefits by knowing that she is providing good nourishment and research shows that breastfeeding is associated with a reduction in the risk of breast cancer. The return of ovulation is inhibited in the fully breastfeeding woman, at least during the first six months after birth, thereby providing important health benefits to the family because of improved birth spacing.

We are now coming to a better understanding of the nutritional components of human milk and of the receptivity and response on the part of the child. The efforts of our participants are directed towards enabling women to initiate and sustain breastfeeding and enabling infants to benefit fully. The research papers and the discussions within our Working Group are a valuable contribution.

Unfortunately there are many factors that discourage or inhibit women from this important practice. In developed countries the rapid pace of life and time demands on women are obstacles. Absence of stable family life and familial support affects many women. Employment patterns, the work environment, and the absence of sufficient maternal leave time create difficulties.

In developing countries where breastfeeding has been a more common practice, urbanization, work outside the home, and other aspects of modernization tend to diminish the practice of breastfeeding. It is important to protect and strengthen the cultural support for breastfeeding practices within the family.

Our Working Group has also recognized that although breastfeeding primarily involves mother and child, there is also an important role for fathers. Every element of child care is a mutual responsibility and commitment of both parents. The father should be particularly sensitive to the physical demands placed on the mother and assist her in obtaining proper nutrition and rest. The father should give approval and encouragement to help the mother sustain the practice. Every woman should be supported in every aspect of her motherhood, by her family and by society.

Our Working Group is pleased with this opportunity to present and review the important research data. We are grateful to be able to meet with you, Holy Father, and we ask your blessing and your prayers.

Breast development and control of milk synthesis

Peter E. Hartmann, Robyn A. Owens, David B. Cox, and Jacqueline C. Kent

Abstract

We have developed a computerized breast measurement system that can quantitate both long-term (lactation cycle) and short-term (between breastfeedings) changes in breast volume. The increase in breast volume during pregnancy was not related to milk production at one month of lactation, whereas milk production from one to six months of lactation remained constant and was not controlled directly by the suckling-evoked secretion of prolactin. From the measurement of circadian changes in breast volume, it was concluded that infants rarely emptied the breasts at a single breastfeeding and that short-term variation in the rate of synthesis during the day and between the left and right breasts was closely related to the degree of breast fullness. Furthermore, differences between women in the storage capacity of the breasts dictated their flexibility in frequency of breastfeeding. These observations are consistent with the autocrine (local) control of milk synthesis during established lactation in women.

Introduction

Breastfeeding and breastmilk must be considered in the context of maternal physiology and infant development rather than just the narrow role of optimizing infant nutrition (table 1). The lactating breast has a high metabolic activity. Indeed, the energy output in milk represents approximately 25% of the total energy intake in the maternal diet for women exclusively breastfeeding single infants, and up to 50% for those breastfeeding twins [1]. In addition, milk is a very complex secretion, consisting of cells (leucocytes, macrophages, and epithelial cells), lipids (triacylglycerols, free fatty acids, phospholipids, sterols, hydrocarbons, and fat-soluble vitamins), carbohydrates (lactose, oligosaccharides, galactose, glucose, and glycoproteins), proteins (caseins, a-lactalbumin, lactoferrin, secretory IgA and other immunoglobulins, Iysozyme, enzymes, hormones, and growth factors), non-protein nitrogenous compounds (urea, creatine, creatinine, uric acid, amino acids including glutamine, nucleic acids, nucleotides, and polyamines), water-soluble vitamins, macronutrient elements, and trace elements [2,3]. Furthermore, it is now clear that the proportions of these constituents in breastmilk are uniquely appropriate for the human neonate at a time when growth and development are occurring at near-maximal rates, yet many of the infant's systems (such as the digestive, hepatic, immune, neural, renal, and skeletal systems) are functionally immature. In addition, breastfeeding is an integral component of the complex psychological and metabolic dependencies of the infant on its mother, with single physical functions, such as nursing, providing the stimuli of touch, balance, smell, hearing, and vision, and each having specific effects on the infant [4]. Nevertheless, the magnitude of these benefits of human lactation, by and large, has not been afforded appropriate prominence in either health-professional education or the specialist's medical literature (for example, ref. 5).

Successful lactation requires the development of fully functional mammary glands. Whereas other major organs are morphologically and functionally relatively mature at birth, the mammary gland undergoes very limited structural development in utero, with the most dramatic changes in women occurring during puberty, pregnancy, lactation, and weaning [6]. The latter three stages (pregnancy, lactation, and involution during and after weaning) form the phases of the lactation cycle (fig. 1). This cycle can vary greatly in length from a little over nine months to many years, and it may be repeated many times, depending on female fecundity.

TABLE 1. Functions attributed to breastfeeding and breastmilk

Breastfeeding and the infant
  • a unique food
  • augments the infant's digestive enzymes
  • stimulates growth and development
  • may modulate behaviour optimizes infant intelligence
  • protects against illness

Breastfeeding and the mother

  • reduces risk of breast cancer
  • may reduce body weight
  • suppresses maternal fertility

Foetal development

A comprehensive investigation of the foetal development of the human mammary gland was carried out by Dawson in 1934[7]. It was observed that a mammary band (milk streak) appeared as a raised portion of ectoderm on either side of the midline, extending from the axilla to the groin of the human embryo by about the fourth week of intrauterine life. This band contains a narrow ribbon of raised epithelial cells known as the milk line (mammary ridge). Whereas the mammary band generally disappears, the milk line diminishes in length from its caudal end, and the cranial extremity thickens into a small nodule of ectodermal cells in the thoracic region at about 6 to 7 weeks of age. The nodule composed of epidermal cells then sinks into the underlying mesenchymal tissue to form a mammary bud. By 12 to 16 weeks, the overlying skin no longer protrudes, allowing the formation of an indentation that ultimately forms the areola and nipple. From this time to birth, the mammary gland anlage buds to form a number of solid cords, which traverse the underlying mesenchymal and subcutaneous tissue. These cords branch and become canalized to become ducts at 20 to 24 weeks after conception. At the end of gestation, Russo and Russo [6] observed the development of very primitive lobular structures composed of ducts ending in short ductules, lined by one layer of epithelial cells and one layer of myoepithelial cells. The epithelial cells had fine cytoplasmic vacuolization containing lipid droplets and apocrine secretion, which was not confined to the primitive alveolar structures.

Although the endocrine control of foetal mammary gland development is poorly understood, the higher levels of androgen in male than in female foetal rats have been associated with the suppression of mammary development in the male foetus, and the administration of steroid hormones to pregnant mice and rats can induce abnormal mammary development in their offspring (see ref. 8). These findings strongly suggest that more attention should be given to the foetal environment as a potential cause of subsequent lactation failure.



FIG. 1. Breast development and the lactation cycle

Pre-pubertal development

"Witches' milk" is one of the very few pre-scientific terms still in current use and refers to colostrum-like fluid [9,10] that is secreted from the nipples of newborn infants. It was thought that infants secreting this "milk" were possessed by witches, and these infants were not favoured. It is now clear, however, that this is a normal transient event, as secretion can be expressed from the nipples of most infants by seven days after birth, and involution of the neonatal mammary gland is complete by eight weeks postpartum [10]. Throughout childhood, only isometric growth of the breast occurs, with limited elongation and branching of the ducts [7].

Pubertal development

In humans, unlike other mammals, extensive positive allometric growth of the breast occurs at puberty. From 10 to 12 years of age, girls enter puberty and, over time, develop to sexual maturity. Three phases of puberty have been identified: thelarche (commencement of breast development), pubarche (growth of pubic hair), and menarche (start of menstruation).

At thelarche, the ovaries of the immature female start to secrete oestrogen, which initiates positive allometric growth of the primitive mammary structures. The mammary ducts elongate and extend their epithelial lining, branching dichotomously, resulting in the formation of a branched, treelike structure that extends from the nipple into the mammary connective tissue. In addition, terminal buds form on the ducts in preparation for the development of alveolar and lobular tissue structures.

During thelarche, mammary elasticity, vascularization, connective tissue volume, and fat deposition increase [6], leading to the development of the characteristic shape of the mature human breast [11]. Compared with other mammals, mammary growth in pubescent girls is far in excess of the development required for subsequent successful lactation, and therefore it has been suggested that this growth is not related to lactation but rather provides an indicator of sexual maturity.

During puberty there is accelerated growth of the nipple and development of subareolar tissue leading to the elevation of the areola and nipple. About 15 to 25 lactiferous ducts lead to each nipple from discrete lobes within the mammary parenchymatous tissue. These lactiferous ducts may merge within the nipple so that the number of ductal openings is less than the number of lactiferous ducts. The lactiferous ducts dilate at the base of the nipple to form milk sinuses, which, during lactation, accumulate milk drained from the lobes. Unlike other mammals, the lobes of the human mammary gland are separated by deposits of adipose tissue, and the proportion of adipose to secretory tissue varies between individuals. Each lobe is subdivided into lobules that, in turn, are composed of 10 to 100 alveoli. The alveoli are lined with a single layer of lactocytes (mammary secretory epithelial cells) surrounded by starlike myoepithelial cells, a basement membrane, and a network of blood capillaries [9,12].

Under the cyclic influence of ovarian oestrogen and corpus luteal progesterone, as well as the presence of other metabolic and growth-promoting hormones [8, 12], the mammary glands are stimulated to grow. From three to four days before the onset of menstruation, women may experience swelling, tension, fullness, tightness, heaviness, and pain in their breasts [9]. Fluid retention in the connective tissue and enhanced ductular and lobulo-alveolar tissue growth increase breast volume by 30 ml [6, 9] to 100 ml [13]. Increases up to a doubling of breast size have been observed in some women. After menstruation the mammary gland is characterized by some apoptosis, with minimum breast volume occurring five to seven days post-menstrum [6]. Mammary involution following menstruation never completely returns the mammary gland back to the previous premenstrual morphology and, hence, allows the mammary parenchyma to develop, albeit gradually, during successive menstrual cycles [6] until women reach about 30 years of age. In spite of the functional responsiveness of the breast to stimulation [12], little information is available on breast development in relation to the commencement of sexual activity.

Lactation cycle

The lactation cycle begins at conception (fig. 1). During the lactation cycle, there is further growth of the breast (mammogenesis), the initiation of milk synthesis and secretion (lactogenesis 1 and lactogenesis 2), lactation (galactopoiesis), regression of the breast during and after weaning (involution), and relative quiescence during subsequent menstrual cycles.

Mammogenesis

The mammary gland develops the histologic and biochemical capacity to synthesize and secrete milk during pregnancy. Histologic studies have separated mammary development during pregnancy into two distinct phases: mammogenesis and lactogenesis 1. Mammogenesis occurs from early pregnancy and is characterized by proliferation of the distal elements of the ductal tree, creating multiple alveoli (acini) of variable size and shape [14]. Lactogenesis 1 occurs in the later stages of pregnancy and is characterized by the differentiation of resting mammary cells into lactocytes, with the potential to secrete the unique fats, carbohydrates, and proteins characteristic of milk [15].

Initially, mammary development during pregnancy appears to be an acceleration of the parenchymal hypertrophy associated with the menstrual cycle. Indeed, an increase in the sensitivity and tenderness of the breast, and nipple sensitivity in particular, is often one of the first indications of pregnancy, and this can occur within a few days of conception and before the due date of the next menstrual period. Thus, the factors initiating mammogenesis at this time must be closely related to those responsible for the mother's recognition of her pregnancy. Subsequently, the subcutaneous veins become enlarged and visible through the skin, and the areola usually enlarges and becomes more darkly pigmented [14]. Extensive lobulo-alveolar growth occurs during the first half of pregnancy, and in the third trimester there is a further increase in lobular size associated with hypertrophy of the lactocytes and the accumulation of secretion in the lumina of the alveoli [6].

Although there is little precise information on the hormonal control of mammary development in women during pregnancy, the changes in the patterns of circulating hormones are now well established. The implantation of the blastocyst in the uterine wall is associated with the secretion of human chorionic gonadotrophin (hCG), which maintains and increases the steroidogenic activity of the corpus luteum, until hCG secretion decreases at about 8 to 10 weeks of gestation. In the later stages of pregnancy, the maternal serum concentrations of progesterone and oestrogens are increased by de novo synthesis in the placenta [16].

In classical studies on ovariectomized-hypophysectomized-adrenalectomized rats and mice, Lyons [17] and others have shown that ductal mammogenesis is promoted by oestrogens, growth hormone, and corticosteroids. In addition, lobulo-alveolar development occurred at maximal rates in the presence of oestrogen, progesterone, prolactin, growth hormone, corticosteroids, and placental lactogen. Studies on isolated human mammary tissue in culture suggest that insulin, cortisol, growth hormone, prolactin, oestrogens, progesterone, and epidermal growth factor (EGF) are involved in the proliferation and differentiation of human mammary cells in tissue culture [18-22]. Relaxin has been implicated in the proliferation of porcine mammary parenchyma [23]. The action of oestrogen and progesterone on mammary parenchyma leads to the secretion of EGF and transforming growth factor-a (TGF-a), both of which are potent mammary mitogens [22]. In contrast, TGF-b1 inhibits mammary growth [22, 24, 25]. These studies imply that the development of the human mammary gland during pregnancy is controlled by a complex sequence of stimuli and inhibition similar to the hormonal mechanisms that control the growth and development of the mammary glands of common laboratory animals.

Hytten [26] used a water-displacement technique to measure the volume of the left breast of 11 women at three months of gestation and seven days postpartum. In 10 women breast volume increased by 60 to 480 ml, and in one woman the volume decreased by 20 ml. The relationship, however, between breast volume at the end of pregnancy and the volume of the "empty" breast on the seventh postpartum day is unknown. We [27] have developed a computerized breast measurement (CBM) system that uses video images of structured light stripes projected onto the breast to quantitate both long-term (throughout the lactation cycle) and short-term (during the day) changes in breast volume (figs. 1 and 2). Preliminary findings for breast development (fig. 3) from preconception until just before delivery [28] have demonstrated that significant growth can occur during the first trimester and that this growth can either continue throughout pregnancy or reach a plateau during the second trimester. The six mothers studied to date have had a successful lactation outcome irrespective of their pattern of breast growth during pregnancy.

Lactogenesis 1

The timing of lactogenesis 1 (development of potentially functional lactocytes) in women has not been precisely defined. In mid-pregnancy the true lobulo-alveolar system develops, the proliferative changes are reduced, and there is increasing cellular differentiation with the accumulation of cellular organelles and secretory products [6, 15, 29]. Lactose is the most osmotically active component of the colostrum, and hence excess lactose synthesis during pregnancy could lead to breast distension. Nevertheless, the tight junctions between the lactocytes are open during pregnancy, and thus lactose can escape across the mammary epithelium into the bloodstream and then be excreted in the urine. The concentration of lactose in the blood of pregnant women increases during mid-pregnancy [30], and this coincides with an increase in the excretion of lactose in the urine [28, 31]. These findings suggest that in women lactogenesis 1 occurs approximately halfway through pregnancy. Studies using an increase in the concentration of lactose in the blood or mammary secretion as an indicator of the occurrence of lactogenesis 1 have suggested that lactogenesis 1 occurs at different stages of pregnancy in different species. Whereas lactogenesis 1 occurs in late pregnancy in rats [32], ewes [33], and sows [34, 35], it occurs earlier in pregnancy in cows [36], goats [37], and women [30]. These species differences in the timing of lactogenesis 1 during pregnancy make it difficult to speculate on the control of the development of the functional lactocyte. A greater knowledge of the control of mammogenesis and lactogenesis 1 in women is important not only for the understanding of normal lactation, but also because early pregnancy [13] and lactation [38] have been associated with a reduced risk of breast cancer.

Lactogenesis 2

Whereas the umbilical cord couples the developing foetus to continuous life support from its mother's placenta, nursing after birth provides the growing infant with comparable but intermittent life support from its mother's breasts. Thus, it is essential for the breast to develop its unique synthetic capacity during pregnancy, so that the initiation of an adequate supply of milk accompanies the birth of the infant. The occurrence of lactogenesis 1 halfway through pregnancy in women permits lactogenesis 2 to occur, even if the infant is delivered prematurely, although the milk composition is different from that of full term mothers, possibly because of incomplete hypertrophy of the mammary gland or incomplete exposure to prolactin and other hormones [39].



FIG. 2. Computerized breast measurement system assessment of function for right and left breasts of two mothers (A and B) over 24 hour periods. The degree of fullness is the volume of the breast at the end of a breastfeeding minus the minimum volume of the breast during the 24-hour period, divided by the storage capacity of the breast, expressed as a percentage. The rate of milk synthesis is calculated from the difference between the breast volume at the end of a breastfeeding and the breast volume just before the beginning of the next breastfeeding, divided by the time between the measurements [60]

In women the control of lactogenesis 2 (the initiation of copious milk secretion) appears to be under endocrine regulation similar to that in other mammals. The pioneering work of Kuhn [40] established that progesterone withdrawal was the trigger for lactogenesis 2 in the rat, and subsequently Nicholas and Hartmann [32] established the temporal relationship between the withdrawal of progesterone approximately 24 hours before parturition and the increased rate of lactose synthesis (a measure of lactogenesis 2) coinciding with birth. This pattern appears to be consistent for most mammals studied to date.

In women, however, progesterone withdrawal is delayed until after the delivery of the placenta; thus, there is a frame shift to the post-partum period in the dose temporal relationship between the fall in progesterone and the increase in the concentration of lactose in the colostrum [41].

Lactogenesis 2 is delayed by more than a day to between 30 and 40 hours post-partum (fig. 4). Although this delay may seem inconsistent with the perceived energy requirements of the human infant, it is consistent with the acquisition of mucous membrane protection from maternal colostrum, as well as the remarkable resilience of the human neonate to nutritional abuse and the unusual weight loss m human infants after birth.



FIG. 3. The development of the left breast of one mother depicted by models generated using the computerized breast measurement system

Lactogenesis 2 also occurs 30 to 40 hours after delivery in mothers who have had a Caesarean section [42], since the timing of placenta removal in relation to birth is the same as in those who delivered normally. This is fortunate for human lactation, as Caesarean section delivery in other species, such as ewes, results in a delay in lactogenesis 2 of more than a day when compared with normal delivery [33].

The involvement of the placenta in the initiation of lactation has been further substantiated by the finding that if a fragment of placenta is retained after delivery, lactogenesis 2 occurs only after its removal [43]. These observations also are consistent with progesterone withdrawal acting as the trigger for lactogenesis 2 in women, as it does in other mammals.

Although lactogenesis 2 in women does not require either the suckling stimulus or milk removal [44], it does require the presence of adequate concentrations of lactogenic hormones. The concentration of prolactin in a woman's blood is high at parturition, and suppression of prolactin secretion by the administration of bromocriptine results in the inhibition of lactogenesis 2 [44]. Nevertheless, undesirable side-effects and the potential role of prolactin in facilitating maternal behaviour have cautioned against the use of this drug for the suppression of lactation in women who choose not to breastfeed.

Close assessment of the initiation of lactation in mothers with type I diabetes shows that the increase in the concentration of lactose in the colostrum is delayed by about 24 hours compared with normal mothers [45-47]. Since this delay coincides with the reduction in insulin therapy after birth and the reestablishment of control of glucose homeostasis, permissive amounts of insulin also may be required for lactogenesis 2. Notwithstanding this delay, diabetic women with perseverance can establish successful lactation.

Milk "coming in," which is sensed by mothers as a sudden enlargement of their breasts with milk, is a post-lactogenesis 2 event occurring two to three days after delivery [42]. The physiological significance of the sensation of milk coming in is not clear, but it may represent the time when the mother's capacity to synthesize milk first exceeds the infant's appetite. That is, it may represent the transition from an endocrine-promoted lactogenesis 2 to another form of control during established lactation. Despite these considerations, severe engorgement can be associated with milk coming in, and this is a very painful event of short duration but long remembered by mothers. The risk of severe engorgement is reduced if mothers avoid timed schedules for breasfeeding and fully breastfeed their babies to appetite, day and night, from birth. The implications for lactogenesis 2 and milk coming in are important when considering the design of programmes for the early discharge of mothers from maternity hospitals [48].



FIG. 4. Peripartum milk lactose expressed as a percentage of the maximum lactose concentration for the cow, rat, and woman

Galactopoiesis

The maintenance of galactopoiesis appears to be under a combination of endocrine, autocrine (local), and metabolic control, which varies according to the species and the stage of lactation. The relative importance of these mechanisms, however, depends on whether the species has been selected for dairy production. Nevertheless, the removal of milk from the mammary gland is of the utmost importance for the maintenance of milk secretion in all mammals. In women, frequent suckling not only stimulates the release of oxytocin and thereby elicits milk ejection, but also stimulates the release of prolactin [49] and results in the removal, inactivation, or both of local inhibitory factors [50].

The finding in the early 1970s that the sucking stimulus evoked the release of prolactin [49] provided a potential explanation for the regulation of milk synthesis. We have not, however, found any relation between the suckling-evoked release of prolactin and milk yield. Although the prolactin response decreases in later stages of lactation, there is no decrease in milk yield [28]. Therefore, the concept that demand feeding regulates the rate of milk synthesis by evoking the release of prolactin must be seriously questioned.

About 20 years ago, it was generally accepted that the nutrition of the mother was the most important determinant of milk synthesis. This assumption was based on numerous studies demonstrating the dependence of milk production on the level of nutrition in dairy cows and goats. As a result, it was concluded that feeding the malnourished mother would thereby feed the child [51]. Nevertheless, subsequent studies by Prentice et al. [52] have shown that improving the nutritional status of malnourished mothers does not increase milk production. This, together with extensive studies on milk production in women from both developing and developed countries, has led to the conclusion that maternal nutrition is not an important determinant of milk production in women (see ref. 53).

The demand-fed infant consumes irregular quantities of milk at irregular intervals during the day [53]. These feeding patterns also are consistent with mothers' awareness [54] and with recent studies that indicate that it is the baby's appetite that determines milk yield [53]. Indeed, a comprehensive consideration of the literature leads to the conclusion that ensuring that the infant has sufficient access to the breast to satisfy its appetite for milk optimizes milk production. The basic question, however, remains: How does the breast regulate milk synthesis to meet this unpredictable external demand for milk by the infant?

In 1984 Neil Matterson [55] provided a practical answer to this question: "The more he cries the less milk he drinks, so less milk is produced, so there's less for him to drink, so he cries because he didn't get a drink. Do you understand that?" Perhaps this confusing explanation of the control of milk synthesis underlies epidemiologic results showing that many mothers give up breastfeeding in the belief that they cannot produce enough milk for their babies [56].

A prerequisite for investigating the control of milk synthesis during galactopoiesis in any suckling mammal is to measure the rate of milk synthesis accurately. The classical means of determining the daily rate of milk synthesis in women has been the "weigh-suckle-weigh" or "test-weighing" method [57], which conventionally records the combined milk output from both breasts and sums the milk consumed during all breastfeedings over a period of 24 hours. If correction is made for evaporative water loss during each breastfeeding, test weighing is a very accurate method of determining milk transfer between the mother and her infant [58]. But neither test weighing nor alternative methods of measuring milk production [59] measure the short-term (between breastfeedings) rates of milk synthesis in individual breasts.

Our CBM system measures the short-term rates of milk synthesis in women by determining the rate of increase in breast volume between breastfeedings [27]. We installed the CBM system in the homes of seven mothers so that we could measure their milk production and changes in breast volume while they breastfed on demand in their normal environment. In addition to the short-term rate of milk synthesis, we were able to calculate two new parameters for the assessment of breast function from the progressive changes in breast volume over the 24-hour period. First, the storage capacity of the breast was calculated, that is, the demonstrated capacity of the breast to store milk that was available to the infant. This was calculated as maximum breast volume minus minimum breast volume observed over the 24-hour period [60]. Second, the degree of fullness of the breast was calculated as the volume of the breast at the end of a breastfeeding minus the minimum volume of the breast during the 24-hour period, divided by the storage capacity of the breast. Thus, the degree of fullness varied from one when the breast was full to zero when the breast was empty.

To illustrate our findings using the CBM system, the results for two of the seven mothers who participated in this study [60] are presented (table 2 and fig. 2). Mothers A and B were fully breastfeeding their babies and had similar levels of milk production: 912 and 950 g/24 hours, respectively. Nevertheless, as with most other women we have studied, this production was not divided equally between the mother's breasts, emphasizing the importance of investigating the regulation of milk synthesis in individual breasts rather than in individual women.

TABLE 2. Computerized breast measurement system assessment of breast function for two mothers

Measurement Mother A Mother B
Stage of lactation (mo) 4 5
Milk yield (g/24 h) 912 950
Storage capacity (ml) 780 190
Relative breast size (%)
minimum 69 92
maximum 71 96
Individual breasts
Measurement Left Right Left Right
Milk yield (g/24 h) 108 804 338 612
Storage capacity (ml) 180 600 80 110
Feedings/24 h 3 4 7 7
Rate of synthesis (ml/h)
minimum 3 17 6 23
maximum 15 49 18 31

Source: ref. 60.

A detailed review of the results of our investigations of human lactation over the 24-hour period using the CBM system is given by Daly and Hartmann [61], and a summary of our observations and conclusions is given in table 3. These studies clearly demonstrated that the infant's appetite determined the milk intake at a particular breastfeeding. The breast storage capacity varied greatly between women (table 2), and this factor significantly influenced the breastfeeding frequency required to maintain an adequate milk supply. In addition to these observations, we were unable to show a relation between the increase in blood prolactin at a breastfeeding and the subsequent rate of milk synthesis between breastfeedings [62]. Furthermore, the short-term rates of milk synthesis of a woman's right and left breasts often responded independently from breastfeeding to breastfeeding. For example, after the first feeding, the milk synthesis rate of the right breast could be higher than that of the left breast, but after the next feeding, the reverse could be true, with the left breast now showing the higher rate of milk synthesis.

The negative relationship between the degree of breast fullness and the short-term rate of milk synthesis (fig. 2) was of particular interest. In this respect, the right breasts of mothers A and B represent two extremes. Mother A, with a large storage capacity, had high rates of milk synthesis when her breast contained the least milk (fullness approximately zero) and low rates of milk synthesis when her breast was nearly full (fullness approximately one). In contrast, mother B. with a small breast storage capacity, achieved a high level of milk production by more frequent breastfeedings with relatively consistent short-term rates of milk synthesis, as her degree of fullness was low after each breastfeeding.

TABLE 3. Observations and conclusions from computerized breast measurements of the circadian changes in breast volume in lactating women

Observation Conclusion
The infant did not consume all available milk at a breastfeeding The infant's appetite determines milk intake at a breastfeeding
Mothers with small breast storage capacity breastfed more frequently The storage capacity of the mother's breasts dictates the flexibility in frequency of breast feeding
Rates of milk synthesis varied greatly within and between breast-feedings The short-term rate of milk synthesis is under autocrine (local) control
Rate of milk synthesis was highest when the breast contained the least milk Autocrine control responds to the fullness of the breast
Right and left breasts differed in both milk production and size Autocrine mechanisms may affect the number of lactocytes in the breast

Our results for women are consistent with the autocrine theory of milk synthesis control during established lactation, which has been recently proposed for dairy goats by Peaker and Wilde [50]. These workers have isolated a protein called feedback inhibitor of lactation (FIL) that appears to suppress milk synthesis as milk accumulates in the mammary gland between breastfeedings by reversibly inhibiting the transfer of newly synthesized protein from the endoplasmic reticulum to the Golgi vesicles.

We also have shown that the difference in the fat content of breastmilk between the beginning and the end of a breastfeeding is related to the degree of fullness of the breast, rather than to whether it is either fore or hind milk [63]. Furthermore, Heesom et al. [64] have demonstrated that medium-chain-length fatty acids inhibit glucose metabolism and lipid synthesis in isolated mammary acini of rats. The presence of lipases in breastmilk and the nature of the accumulation of triacylglycerol in the alveolus suggest that autocrine control of milk fat synthesis by free fatty acids also is mechanistically plausible in lactating women [65]. In vitro studies have shown that free fatty acids may act as messenger and modulator molecules, mediating responses of the cell to extracellular signals [66].

A further interesting development arises from studies by Molenaar et al. [67]. They used 35S-labelled cRNA probes to localize the sites of a-lactalbumin, a-S1-casein, and lactoferrin mRNA synthesis in sheep. Early in lactation, mammary gland expression of a-lactalbumin and a-S1-casein was high in some alveoli but not in others. Those alveoli with high expression of a-lactalbumin and a-S1-casein contained few fat globules in their cells and lumina, whereas those in which expression of these proteins was absent contained abundant fat globules. These latter alveoli also almost exclusively expressed lactoferrin. These findings suggest that milk secretion either is heterogeneous across lobules or occurs sequentially with time in the alveolus as newly secreted milk accumulates. The latter concept seems more plausible.

It is tempting to speculate that the FIL and free fatty acids may act locally to sequentially regulate the short-term rates of milk constituent synthesis, either within a mammary gland or, more likely, within lobules according to the degree of emptying of the lobules in each breast.

Involution

Studies of lactation in village women and the few remaining hunter-gatherer societies suggest that the normal duration of lactation in women is three to four years. In these societies, and more recently in a number of developed countries, weaning is prolonged and gradual (that is, child-led weaning). The cessation of sucking results in distension of the gland with milk and atrophy of the epithelial structures. Finally, milk secretion is greatly suppressed, and the lactocytes disintegrate and desquamate. Phagocytosis of the degenerated alveoli reduces the lobulo-alveolar structures, and ductal systems become predominant. It seems that the involution of the human breast occurs much more gradually than that of the mammary glands of other mammals [68], and this may explain the relative ease of relactation in women.

Acknowledgements

We would like to thank the mothers who kindly volunteered for our studies and the Nursing Mothers' Association of Australia. The work from our laboratory was supported by the National Health and Medical Research Council of Australia.

Continue

Discussion of paper by Hartmann et al.

Dr. McLaren

The two women you showed us both produced more milk from the right breast than the left. Is this usual, and is it related to which breast the baby is put to first at a feeding?

Dr. Hartmann

I think that perhaps two-thirds of women are uneven in the milk production between their left and right breasts, but it doesn't necessarily mean they are consistently higher in the right breast. We found that some women changed from one lactation to the next, so most milk production in one lactation is in the right breast, and in the next it's in the left breast, so there is a fairly random distribution between breasts. Some people think it has to do with the handedness of mothers. We haven't looked at that, but certainly it can change during subsequent lactations. It seems to me to relate to a behavioural characteristic in animals, which is teat order. There is evidence from Sweden, I believe, that indicates that when babies are put on their mother's abdomen, they make their way up to the breast. They also tend to associate with the breast that they attach to first. This observation would be consistent with observations of the establishment of teat order in other mammals.

Dr. McLaren

I was particularly interested in your observation that fat content increases as the breast is emptied. Does that mean it is better for a woman to empty one breast before transferring the baby to the other?

Dr. Hartmann

This is an interesting situation, and one has to be very careful in responding, because how it is applied in practice can be quite misleading. The breast has regular mechanisms that can cope with most patterns of feeding. So far, our results indicate that it doesn't much matter how the breast is emptied; the baby will get the same amount of energy over a 24-hour period. One-sided feeding has only been recommended for women with oversupply problems. For normal feeding it is reasonable to finish one breast before offering the other.

Dr. McNeilly

Back to milk production. Presumably, in the case of twins, both breasts can operate to full capacity if they are emptied at the same rate?

Dr. Hartmann

That is correct. Our studies suggest there is additional capacity. I think mothers in Western societies have to down-regulate their physiological capacity to produce milk to their babies' requirements. We can look at the endocrine system as setting the upper limits of the mother's milk production capacity and the autocrine mechanism as then cutting it down to the actual needs of the baby. With twins the mother sustains a higher level of production that perhaps approximates the breasts' maximum capacity. We studied a woman who fully breastfed triplets for two and a half months, so the breast has enormous capacity.

Dr. McNeilly

You didn't mention the relationship of oxytocin to storage capacity. It seems that much of the milk won't come out without oxytocin release. Is that true? There is very little information on that.

Dr. Hartmann

Residual milk, in my opinion, has done more to confuse our understanding of lactation than just about any other concept. This is because it is based on the very unnatural situation of the dairy cow. The suckling situation is totally different. Oxytocin is obviously required for milk ejection, but the amount of milk that is taken depends on the baby's appetite, not what the mother has available. So in mothers with high storage capacity, there is enormous variation between the storage capacity and the amount of milk that the baby might take at any one time.

Dr. McNeilly

But if the mother didn't release oxytocin at all, would that dramatically reduce the amount of milk the baby could get?

Dr. Hartmann

Yes, it certainly can be a problem. We don't notice it particularly in women who are breastfeeding. It is often a problem for mothers who are expressing milk. If they don't get a let-down, they can have a great decrease in milk production.

It is very important to look at milk production from individual breasts, which relates to Dr. McLaren's first question. We did an initial study in Oxford on six mothers to determine if the interval between feedings was correlated with the amount of milk the baby took. If you combine the production of both breasts, there's no relationship. If you split the intake from the left and the right breasts, there is a very tight coupling. That is, the gap between feeds determines how much the baby takes from a breast. For the other breast, there is no such relationship. It was clear women showed "breastedness" in the same way they show handedness, but it wasn't linked to handedness, because we had five "left breasted" mothers and one "right-breasted" mother, but they were all right-handed.

So it's not clear what the relationship is. It was almost as if the control mechanisms were located in one side, as in true handedness. When we moved to Bristol, we studied 20 more mothers and found no such relationship. We found the relationship was with the first breast to be offered, which confused us somewhat. Therefore, we didn't publish the results.

Constituents of human milk

Ann Prentice

Abstract

Breastmilk contains all the nutrients required by the newborn baby. It also contains non-nutritional components that may promote infant health, growth, and development, such as antimicrobial factors, digestive enzymes, hormones, trophic factors, and growth modulators. In some situations, breastmilk may also contain harmful components, such as pollutants, drugs, allergens, and viruses. Human milk has a unique composition, which differs from that of other mammals in its ingredients and their concentrations.

Breastmilk composition is not constant and varies with stage of lactation, breastfeeding pattern, season, and parity. It also differs among individuals and among communities, for reasons that are not well understood. Maternal nutrition is an obvious candidate, but the situation is complex. Supplementation studies and cross-cultural comparisons have demonstrated that the total concentrations of fat, protein, and lactose are relatively insensitive to current dietary intake and nutritional status, whereas the fatty acid profile and the concentrations of several micronutrients, particularly water-soluble vitamins, are responsive to maternal diet.

For many infants, nutrient intake from breastmilk becomes insufficient after four to six months, and other foods should be added to the diet. Nevertheless, breastmilk can continue to be a valuable nutrient source and to provide non-nutritional factors even for older children. Consequently, breastfeeding for one to two years as part of a mixed diet has many advantages, particularly for children living in impoverished circumstances.

Introduction

Breastmilk is a complex fluid, rich in nutrients and in non-nutritional bioactive components. Knowledge of the composition of human milk and the factors that influence it has increased considerably over the past two decades. This paper briefly summarizes current understanding, drawing largely on our cross-cultural studies in the Gambia and Britain as examples. More comprehensive reviews have recently been published [1-4].

Nutritional and non-nutritional components

Breastmilk contains all of the nutrients needed by the newborn baby during the first weeks of life. These include the metabolic fuels (fat, protein, carbohydrate), water, and the raw materials for tissue growth and development, such as fatty acids, amino acids, minerals, vitamins, and trace elements.

More than 98% of the fat in breastmilk is in the form of triglycerides, constructed within the mammary epithelial cell from medium- and long-chain fatty acids derived either from the maternal circulation (carbon chain lengths 16) or manufactured locally (carbon chain lengths 16) [5]. Short-chain fatty acids (carbon chain length 8) are only present in trace amounts. Oleic acid (18:1) and palmitic acid (16:0) are the most abundant fatty acids in breastmilk triglycerides, with comparatively high proportions of the essential fatty acids, linoleic acid (18: 2w 6) and linolenic acid (18: 3w 3). Comparatively high proportions of other long-chain polyunsaturated fatty acids, such as arachidonic acid (20: 4w 6) and docosahexaenoic acid (22: 6w 3), are also present [5]. These long-chain fatty acids are constituents of brain and neural tissue and are needed in early life for mental and visual development [6]. At least half of the triglyceride molecules in breastmilk contain palmitic acid attached to the central carbon of the glycerol component, a property that increases digestibility, absorption, and mineral balance [5, 7]. The lipid component of breastmilk is the transport vehicle for fat-soluble micronutrients such as prostaglandins and vitamins A, D, E, and K.

Proteins account for approximately 75 % of the nitrogen-containing compounds in breastmilk. Non-protein nitrogen substances include urea, nucleotides, peptides, free amino acids, and DNA. The proteins of breastmilk can be divided into two categories: micellar caseins and aqueous whey proteins, present in the ratio of about 40:60 [8]. The predominant casein of human milk is b-casein, which forms micelles of relatively small volume and produces a soft, flocculent curd in the infant's stomach. The major whey proteins are a-lactalbumin, lactoferrin, secretory IgA, and serum albumin [8], with a large number of other proteins present in smaller amounts. Secretory IgA is the principal immunoglobulin of breastmilk. It is synthesized in the mammary epithelial cell by the coupling of two IgA molecules, produced locally by lymphocytes resident in the breast tissue, with two proteins, J-chain and secretory component [8]. The specificity of breastmilk secretory IgA antibodies reflects the mother's exposure to mucosal infection and is independent of the specificity profile of blood-borne IgA [9]. Many of the proteins in breastmilk have a multitude of potential functions. Lactoferrin, for example, transports and promotes the absorption of iron, is bacteriostatic to a range of organisms, and acts as a nutritional protein, producing amino acids for absorption on digestion [8, 10].

The principal carbohydrate of human milk is lactose, a b-disaccharide manufactured in the mammary epithelial cell from glucose by a reaction involving a-lactalbumin [11]. In addition, breastmilk contains significant quantities of oligosaccharides, predominantly lactose-N-tetraose and its monofucosylated derivatives, representing about 10% of total milk carbohydrate. The oligosaccharide composition reflects the Lewis blood group and secretor status of the mother [12].

In addition to the nutritional components, breastmilk contains a wealth of bioactive components that may have beneficial non-nutritional functions [8, 9, 13, 14]. These include a wide range of specific and non-specific antimicrobial factors; cytokines and anti-inflammatory substances; and hormones, growth modulators, and digestive enzymes (table 1), many of which have multiple activities. These components may be of particular importance for young infants because of the immaturity of the host defence and digestive systems early in life. The physiological significance of many of these substances has yet to be determined, and some may be present merely as "spillover" or excretory products from metabolic processes occurring within the mammary epithelial cell. For those with established significance, the site of action may be within the mother's breast, within the infant's alimentary canal, or, after absorption, within the infant's body. Some antimicrobial components, for example, are active both within the breast, minimizing the risk of breast infection and mastitis [15], and within the baby's gastrointestinal and respiratory tracts, protecting the mucosal surfaces from infection by bacteria, viruses, and parasites [9]. By contrast, the site of action of the peptide feedback inhibitor of lacation (FIL) is within the breast, its function being the autocrine regulation of milk production [16]. On the other hand, casomorphins, opioid-like substances that may affect infant behaviour and mood in addition to a range of other functions, are produced in the baby's intestines by the degradation of breastmilk casein [17]. Many bioactive substances are also valuable nutrient sources and ultimately are digested and absorbed in the normal way. Protease inhibitors in breastmilk may afford a degree of protection from digestion for some breastmilk components [8]. A sufficient proportion of antimicrobial proteins, for example, escape digestion and emerge in the faeces, suggesting that antimicrobial activity continues throughout the length of the infant's gastrointestinal tract [10].

Breastmilk has also been shown to be an excretory route for a range of substances that might be harmful to the baby (table 1). These include viruses, such as human immunodeficiency virus (HIV) [18]; environmental and occupational pollutants, such as DDT, PCBs, and dioxins [19]; components of the mother's diet that might be toxic or allergenic, such as trans-fatty acids, aflatoxins, and cow's milk protein [2022]; commonly used stimulants, such as nicotine, caffeine, and theobromine [23, 24]; and various drugs and radioactive compounds [25-27]. Where exposure to xenobiotics jeopardizes infant health, difficult and often controversial decisions have to be made about whether the risks outweigh the benefits of breastfeeding [26, 28].

Comparison with animal milks

Breastmilk contains a unique combination of ingredients, differing from the milks of other mammals in both the concentration and the nature of its many components. In common with the milk of other primates, human milk has low energy and nutrient density compared with the milks of most other mammals, except for a high density of carbohydrates [4]. In addition, the daily output of the major nutrients in milk relative to the size of the mother is lower in humans than in other mammals, especially dairy and laboratory species [29].

The composition of cow's milk, the basis of most breastmilk substitutes over the centuries, is compared with that of human milk in table 2. In addition to the obvious concentration differences, the milks differ considerably in the structure of many of the milk fractions [30]. For example, in cow's milk the major proteins are a-casein and , b-lactoglobulin; the ratio of casein to whey protein is 80:20; the casein micellar volume is double that of human milk, and the curd formed is hard; the principal milk immunoglobulin is IgG; and lactoferrin and Iysozyme are present only in small amounts [30]. Cow's milk triglycerides contain a higher proportion of short chain fatty acids and a lower proportion of long chain and polyunsaturated fatty acids; furthermore, the positional distribution of fatty acids on the glycerol molecule is different [30]. In addition, many of the non-nutritional factors found in human milk are absent from cow's milk or are present only in trace amounts. For the human baby, these differences affect the digestibility and absorption of nutrients, the bioavailability of micronutrients, and the potential benefits from non-nutritional factors.

TABLE 1. Examples of the non-nutritional components of breastmilk

Antimicrobial factors Growth factors
secretory IgA, IgM, IgG
lactoferrin
lysozyme
complement C3
leucocytes
bifidus factor
lipids and fatty acids
antiviral mucins, GAGs
oligosaccharides
epidermal (EGF)
nerve (NGF)
insulin-like (IGF)
transforming (TGF)
taurine
polyamines
Cytokines and anti-inflammatory factors Digestive enzymes
tumour necrosis factor
interleukins
interferon-g
prostaglandins
a1-antichymotrypsin
a1-antitrypsin
platelet-activating factor: acetyl hydrolase
amylase
bile acid-stimulating esterase
bile acid-stimulating lipases
lipoprotein lipase
Hormones Transporters
feedback inhibitor of lactation (FIL)
insulin
prolactin
thyroid hormones
corticosteroids, ACTH
oxytocin
calcitonin
parathyroid hormone
erythropoietin
lactoferrin (Fe)
folate binder
cobalamin binder
IgF binder
thyroxine binder
corticosteroid binder
Potentially harmful substances Others
viruses (e.g., HIV)
aflatoxins
trans-fatty acids
nicotine, caffeine
food allergens
PCBs, DDT, dioxins
radioisotopes
drugs
casomorphins
d -sleep peptides
nucleotides
DNA, RNA

Data compiled from references given in the text.

Variations in breastmilk composition

The composition of breastmilk is not uniform, and the concentrations of many of its constituents change during the lactation period and differ between individual mothers. As variations in concentration are not necessarily inversely related to breastmilk volume, differences in breastmilk composition affect the daily intakes of milk components by the breastfed child. There are several factors that are known to influence the concentration of breastmilk constituents in predictable ways [31]. These include stage of lactation; breastfeeding routine; parity, age, and other maternal characteristics; regional differences; and, in some situations, season of the year and maternal diet. These are discussed in detail below.

Stage of lactation

Human lactation can be divided into four phases that differ in the composition and volume of milk produced: colostral, transitional, mature, and involutional. Colostrum is secreted for the first three to five days after delivery, transitional milk until the end of the second week, mature milk during full lactation, and involutional milk at the end of lactation. These definitions are arbitrary; the timing varies from one mother to another, and composition does not change abruptly. Typical concentrations of selected milk constituents are shown in table 3 [29, 32-35]. Notably, colostrum is rich in secretory IgA, lactoferrin, vitamin A, and sodium compared with mature milk but has relatively low concentrations of fat, lactose, and vitamin B1. Involutional milk is characterized by low lactose content and high concentrations of protein, fat, and sodium [11, 36]. Because milk volume is low during the colostral phase, rising slowly during the first week to the higher levels of established lactation [37-39], the daily intake of most milk components by breastfed babies increases after birth, reaching a peak after several weeks (table 4). The exception is secretory IgA and, hence, total protein intake, which is maximal in the first week (table 4).

Mature breastmilk composition also changes during the course of lactation, although not as markedly as in the early weeks [31, 36, 40]. Many nutrients show a gradual decrease in concentration of around 10% to 30% during the first year of lactation, often reaching a low plateau thereafter. A greater decrease occurs for some components, such as zinc [41]. Some components show little change, especially those involved in osmoregulation, including lactose and sodium, whereas a few, notably Iysozyme, increase.

Breastfeeding routine

Breastmilk composition can vary during the day and from the beginning to the end of a feeding. This is most pronounced for fat and fat-soluble components such as vitamin A and zinc [5, 42]. The fat content of breastmilk can change by as much as fivefold during the course of a feeding [42]. The fat concentration is influenced by the breastfeeding routine of the mother, and short-term variations are related to the volume of milk produced per feeding and the time interval between feedings [42]. Differences in breastfeeding routine can affect the diurnal variation in fat concentration. In the Gambia, for example, where mothers feed on demand and sleep with their infants who suckle during the night, the highest breastmilk fat concentration tends to occur in the early morning, whereas in Western societies, with different feeding schedules, the early morning is associated with the lowest fat concentration of the day [42]. Other constituents, such as protein, may show small but consistent changes from the beginning to the end of a feeding and during the day [36, 43], whereas others, such as calcium, are unaffected [44].

TABLE 2. Typical contents of human and cow's milk

Contents Human milk Cow's milk
Fat
total (g/100 ml) 4.2 3.8
fatty acids 8C (% ) trace 6
polyunsaturated fatty acids (%) 14 3
Protein (g/100 ml)
total 1.1 3.3
casein 0.4 0.3 2.5
a-lactalbumin 0.3 0.1
lactoferrin 0.2 trace
IgA 0.1 0.003
IgG 0.001 0.06
lysozyme 0.05 trace
serum albumin 0.05 0.03
lactoglobulin - 0.3
Carbohydrate (g/100 ml)
lactose 7.0 4.8
oligosaccharides 0.5 0.005
Minerals (g/100 ml)
calcium 0.030 0.125
phosphorus 0.014 0.093
sodium 0.015 0.047
potassium 0.055 0.155
chlorine 0.043 0.103

Data compiled from references given in the text.

TABLE 3. Typical contents of 100 ml breastmilk produced on days 1-5 (colostrum) and more than 15 days (mature milk) post-partum

Contents Colostrum Mature milk C: M%a
Metabolizable
energy (kcal) 55 67 82
Fat (g) 2.9 4.2 69
Lactose (g) 5.3 7.0 76
Protein (g)
total 2.0 1.1 182b
secretory IgA 0.5b 0.1 500b
lactoferrin 0.5 0.2 250
casein 0.5 0.4 125
Calcium (mg) 28 30 93
Sodium (mg) 48 15 320
Vitamin A
(g retinol equivalents) 151 75 201
Vitamin B1 (g) 2 14 14
Vitamin B2 (g) 30 40 75
Vitamin C (g) 6 5 120

Data compiled from references given in the text.

a. Percentage ratio of concentrations in colostrum and mature milk.
b. Considerably higher on days 1-3.

Maternal parity and age

Breastmilk composition may be influenced by the parity and age of the mother. In the Gambia young, primiparous mothers have higher concentrations of several constituents, especially fat, total protein, and immunoproteins, whereas older mothers of very high parity (nine or more children) tend to produce milk with reduced quality [45-48]. Other components, such as calcium, do not change with parity [44]. Similar observations have been made in some studies elsewhere [36], but not in others, and the mechanisms involved remain elusive.

Season

The season can influence breastmilk composition. In subSahelian Africa, where food availability, infection rates, farm work, and child-care patterns vary between seasons, variations in the concentrations of some constituents, such as fat, immunoproteins, and watersoluble vitamins, have been observed [45, 49, 50]. The changes may be related, in pan, to alterations in the mother's diet or breastfeeding behaviour. Milk ascorbate level, for example, closely parallels maternal plasma ascorbate concentration and vitamin C intake, and is high during the season when mangoes are plentiful but low for the rest of the year [50].

Region

Differences in breastmilk composition have been reported between urban and rural populations, and between different socio-economic, geographic, and ethnic groups. Failure to consider differences in duration of lactation, breastfeeding practices, maternal parity and age, sampling protocols, and assay techniques may have contributed to the impression of marked regional differences. A recent evaluation of the available data suggests that the similarities between regions are more striking than the differences, particularly with respect to the major nutrients [31]. Nevertheless, some distinct regional differences are evident, particularly in the concentrations of certain protein components, minerals, vitamins, and trace elements [31, 44, 51]. The reasons are largely unknown but may be related, in part, to the maternal diet and the local environment.

Maternal diet and nutritional status

In the past it was commonly believed that poorly nourished mothers had reduced lactational performance, in both the amount and the quality of breastmilk produced. This view has now been shown to be largely incorrect [4]. A recent examination of the world literature could not demonstrate any convincing relationships between maternal nutritional status, as indicated by body mass index (BMI), defined as weight/height2, and either breastmilk output or energy content [52], even in very thin mothers (BMI < 18.5 kg/m2).

TABLE 4. Typical daily intakes (g) of selected breastmilk constituents

Age Protein Fat Lactose Calcium
Total Secretory IgA Other
Day 1 5.0 4.8 0.2 <1 1 0.01
Day 3 12.0 5.0 7.0 5 12 0.06
Day 8 9.0 1.8 7.2 22 40 0.19
3 mo 7.5 0.7 6.8 29 52 0.22

Calculated intakes assume the following daily milk volumes: day 1 (0-24 h), 40 ml; day 3 (48-72 h), 200 ml; day 8, 600 ml; 3 months, 750 ml [1, 38, 52]. concentration data from table 3 and other references in the text.

Direct dietary supplementation studies mostly support this view. In a Gambian study, where poorly nourished lactating mothers were given a high-energy, nutritionally balanced supplement that provided a net energy gain of 3 MJ/day, there was no impact on breastmilk volume [4, 37]. Breastmilk fat and protein concentrations were increased slightly by the supplement, but lactose levels fell, resulting in only a marginal effect on total breastmilk energy. A review of other intervention studies concluded that there was no persuasive evidence for the positive effects of diet on breastmilk energy output [53]. Although breastmilk fat concentration has been correlated with various aspects of maternal fatness in a number of studies [4, 36], including those in the Gambia [45], this observation is not universal; in some populations negative relationships have been reported [4].

Lactation, therefore, appears to be relatively robust in the face of poor nutrition. Maternal diet can, however, affect the breastmilk concentrations of many minor constituents, particularly long-chain polyunsaturated fatty acids, some vitamins, zinc, selenium, iodine, and fluorine [51]. The profile of fatty acids in the mother's diet and adipose tissue stores is reflected in the fatty acids of breastmilk [5, 47]. The concentrations of two water-soluble vitamins, riboflavin (vitamin B2) and ascorbic acid (vitamin C), show rapid, dose-related responses to maternal supplementation [4, 50]. The fat-soluble vitamins A, D, E, and K are less responsive to diet because of the buffering action of maternal stores and carrier proteins, but large supplements can result in increased breastmilk concentrations, occasionally to potentially toxic levels [51]. Maternal zinc supplementation may slow the decline in breastmilk zinc concentration during lactation, although the magnitude of this effect and its significance for the breastfed child are still uncertain [41, 54].

Worldwide variations in breastmilk composition have suggested that poor maternal calcium intake may be a factor in determining breastmilk calcium concentration [55]. Mothers in the Gambia, for example, where the diet contains little calcium, have an average breastmilk calcium concentration more than 20% lower than that of British women [44, 56]. A recent supplementation study, however, which tripled the calcium intake of Gambian women for the first year of lactation, had no impact on breastmilk calcium concentration [56]. Intriguingly, a possible link with calcium intake during the preceding pregnancy emerged during this study, an observation that deserves further investigation [57].

Differences between mothers

Even when these various influences are taken into consideration, breastmilk composition varies considerably from one mother to another in the same population. Typically, major constituents such as fat, protein, and calcium can differ by two- to threefold between mothers at the same stage of lactation [44], and the concentrations and activities of some of the minor constituents can be highly variable [48]. At the same stage of lactation, breastmilk volume also varies between mothers [37]. In general, between-mother differences in composition and volume are maintained throughout lactation and are not necessarily related to each other [36, 37, 45, 48, 53, 58]. As a consequence, the intakes of breastmilk components are also highly variable, and some infants consistently receive substantially more or less from breastmilk than others of the same age. It is, therefore, important, when assessing the adequacy of breastfeeding for individual children, that measurements be made of both breastmilk intake and breastmilk composition.

Contribution of breastmilk to infant nutrition

Breastfeeding will normally provide all the nutrient requirements of a baby for the first four to six months of life [59]. After this time some nutrients may become limiting, including not only dietary energy, but also essential minerals such as zinc and iron. Current recommendations are that solid foods are unlikely to be necessary before four months, but a mixed diet should be offered by six months [59].

Moreover, breastmilk can continue to make substantial contributions to infant nutrition for many months after the introduction of weaning foods [40, 60]. This is especially true in communities where weaning and adult foods are of poor quality. In the Gambia, for example, older, partially breastfed children obtain more than two-thirds of their vitamin A and fat from breastmilk [60]. When breastfeeding stops, the intake of these nutrients drops dramatically. A similar effect is seen in Dutch children weaned onto macrobiotic diets [61]. The contribution of breastmilk to vitamin A nutrition may be the reason why prolonged breastfeeding protects against xerophthalmia and eye disorders in regions where vitamin A deficiency is common [60]. In addition, significant quantities of many of the non-nutritional factors continue to be ingested by the partially breastfed older child, which may be especially important for children living in impoverished and unsanitary environments [60]. In affluent societies, where high-quality weaning foods and health care are read fly available, the benefits of partial breastfeeding beyond six months are less apparent [60]. For children in poorer societies, however, the many beneficial effects of prolonged breastfeeding on nutrition, health, birth spacing, and the family economy [61)] strongly suggest that breastfeeding for one to two years should be encouraged as part of a mixed diet.

Continue

Discussion of paper by Prentice

Dr. Garza

Dr. Prentice, I also am intrigued by the calcium data. If you look at casein levels, are they comparable between the Gambia and Britain, or is the casein just not saturated? (I know that is not an appropriate term.)

Dr. Prentice

Clemens Kunz of the University of Dortmund in Germany measured the casein levels for us not long ago, and they seem to be very similar in American and Gambian mothers. In human milk, however, the main vehicle for calcium is citrate, not casein, and we are concentrating on the citrate levels first before going for the casein, as we are not expecting to see any major differences there.

Dr. McNeilly

Dr. Prentice, I have learned a lot. Could you tell me if nutrition might affect the rate of milk synthesis, or is that not shiftable?

Dr. Prentice

Dr. Hartmann could probably answer that question better than I. The only information we have is from our Gambian supplementation study, in which both unsupplemented and supplemented women produced the same amount of milk per day, but the supplemented women fed fewer times per day. So we think that it quite possibly has something to do with the mother's nutritional state, not necessarily with substrate supply affecting the storage capacity, as Dr. Hartmann said. Perhaps the unsupplemented women had smaller storage capacity and had to feed much more frequently during the day to produce the same volume. This is speculation, because we have not done any work on it. Have you any comment, Dr. Hartmann?

Dr. Hartmann

Yes, I think that when substrate supply is limited, the babies have to feed very frequently, regardless of the storage capacity, to keep the rate of synthesis at the maximum. Providing the mothers with more energy from the diet somewhat increases their ability to produce milk. Then the baby might not suckle as frequently to get the volume of milk that it requires, so I don't think it is inconsistent.

Dr. Rasmussen

I would like to contribute the results from a supplementation trial in Guatemala that have been presented at meetings but haven't yet been published. We selected women at the end of pregnancy and the beginning of lactation based on mid-calf circumference, not on body-mass index (BMI), because BMI has the properties that you mentioned. In that supplementation trial, we gave mothers either a low-energy or a high-energy supplement; we didn't have a no-treatment group, because we didn't consider it ethical, given the state of the population. The women in the high-energy group produced more milk, and-of particular importance to this meeting-they exclusively breastfed their babies for a longer period. We were not in the field long enough to ask if there was an effect on fertility in these women (in other words, on the length of their amenorrhoea), but I think there were clearly changes in the way the women breastfed as a result of changes in their milk volume. So I think there may be important effects of supplementation that we may not have seen in the trials that we have had today.

Dr. Prentice

I don't want to detract from that at all, but I still feel that we may be talking about two different things: the biological limits on lactation and the whole area of the mother's well-being-the social factors that affect the way she and the baby interact to increase milk volume. It seems from the work we have been doing that most women can produce reasonable volumes of milk, and if they don't, there are other factors that are probably affecting it other than the capacity of the breast in most instances. I wanted to ask you if you had any macronutrient content data from the breastmilk-that was my brief this morning. Does it affect the composition of the milk?

Dr. Rasmussen

The only component we have looked at is energy. There are compensatory changes in energy, such that women who produce more milk have less energy-dense milk The effects on infant growth are expected to be minimal. But our statistical power was not calculated on measuring infant growth.

Dr. Prentice

I think I would have predicted that. In our supplementation studies we found that if we gave women essentially a higherfat diet, there was more fat in the breastmilk, but lactose was reduced. This has been seen in quite a lot of other studies as well. Thus, the mother's breastmilk fat concentrations may well be responsive either to her own diet or to her adipose tissue stores. We have seen it, other people have seen it, but some other studies have not, and so it is still relatively controversial. But whatever happens, total milk energy seems to stay remarkably similar.

Dr. Hartmann

Could I add that we looked at some immunologic factors in the same material, and lactoferrin remained the same in both groups.

Dr. Garza

What was the content of fat in the Gambian diet?

Dr. Prentice

It's about 20% to 25%.

Dr. Garza

In studies done with Salvador Villalpando and Nancy Butte in Mexican women consuming diets of lower fat content, we found much lower levels of fat in human milk that were not fully compensated for by changes in lactose.

Dr. Prentice

That were nor compensated for?

Dr. Garza

That's right. We saw the same directional changes you did, but the reduction in fat was much greater than the increase in lactose, so that in populations with very low levels of fat (in the 10% to 12% range), the breastmilk fat content may be influenced dramatically.

Dr. Prentice

I certainly could believe that fat intakes might be limiting at that very low level. Did you find a difference in the shift between the manufactured fatty acids and the dietary fatty acids?

Dr. Garza

We didn't look at fat composition. Dr. Villalpando, has fat composition been examined since those earlier results were available?

Dr. Villalpando

We are looking at those data now. We see an increase in the medium-chain-length fatty acids, but the milk energy increase was not that impressive.

Dr. Prentice

Mike Crawford long ago suggested the same thing from Tanzanian studies, but there the total fat tended to stay the same but with larger amounts of medium-chain-length fatty acids.

Professor Howie

I apologize that this question is a little lateral to what you have been talking about, but I want to ask about the concept that breastfeeding mothers may not have to increase their own diet in proportion to the amount of milk they are giving the baby. In other words, if a mother is breastfeeding, the total energy cost to the community is less than if she were feeding herself and her baby by artificial means. That concept was discussed quite a bit a year or two ago, and I wonder if you have any comments on that and on its potential importance for nutrient provision.

Dr. Prentice

I think I would still say the same thing. There do appear to be women who are not able to increase their food intake, that is, their energy intake, and there do seem to be relatively simple compensations that can occur: a reduction in activity, for example. We are still not really sure that in lactation there is much in the way of changes in costs like basal metabolic rate so on, although there may well be in pregnancy, but fairly minor and adjustments may be satisfactory to enhance efficiency. These include accessing energy from fat stores; many, but not all, women in that situation will lose some of their fat stores while they are lactating. Certainly, in the Gambia some women put on weight during lactation at the time of year when food in good supply. But they are obviously eating enough is for both weight gain and milk production. So, yes, I think we would still be saying the same, that there are compensations for the energy needs of lactation.

Problems of establishing lactation

Michael W. Woolridge

Abstract

The problems associated with the establishment of lactation can be viewed primarily from the mother's perspective but should also be viewed from that of the caregiver supporting her and the maternity facility providing her with care.

Factors intrinsic to the mother

The first time a mother puts her baby to her breast, she is doing something for which nothing will have adequately prepared her. Childbirth and breastfeeding are comparable in this respect; unfortunately, anticipation of the former may prevent her from giving adequate consideration to the latter, particularly to practical issues. Clinical experience suggests that ensuring that practical issues are correct can be vital to a successful outcome for breastfeeding, yet it rarely proves possible to address them adequately antenatally. The result is that the mother and her newborn, both novices to the process, go through an extremely rapid learning curve that can run completely smoothly or may be fraught with difficulties. Much will depend upon whether the mother encounters problems, and her perseverance and determination in overcoming them. Cultural factors during her upbringing and the expectations of society are likely to influence her persistence, but for individual women little direct influence can probably be exerted over these.

Factors extrinsic to the mother

The pathway to success is not solely determined by factors intrinsic to the mother (or her baby) but also by the quality of care she receives both antenatally in preparation for breastfeeding and post-nasally. Several extrinsic factors can therefore be proposed that are likely to have a beneficial impact on the individual mother's chances of success:

  • good antenatal education and preparation
  • optimal post-natal support, delivered by appropriately trained health-care professionals
  • continued community support from a social network (partner, peers, and relatives, lay helpers or counselors, and health-care workers)

Despite the potential impact of individual-specific factors, it is imperative for the health-care system to offer wellstructured support, ensuring the mother's access to welltrained and motivated staff, to offer all women the best chance of success.

For convenience, the factors leading either to a successful or to an unsuccessful establishment of lactation will be addressed under three broad headings:

  • cultural influences on breastfeeding
  • perinatal practices in hospital
  • individual-specific influences

Before addressing these issues, I would like to focus on the physiological constraints on the establishment of lactation, looking at the factors that regulate both milk synthesis and effective milk transfer from mother to baby.

How long does it take to establish breastfeeding?

This key question can be addressed by reconsideration of classical physiology. Technically, the new mother must acquire the practical skills for handling her baby and positioning and fixing her baby on the breast. This may take from several days to a few weeks. The more fundamental physiological question is "How long does it take for a mother's milk supply to match her baby's needs?" This question has largely been overlooked, although the evidence has been available for some time.

What triggers the onset of milk production?

At one time the view was current that early and frequent breastfeeding was instrumental in the early establishment of milk supply [1]. The data, however, only support a benefit of frequent suckling: early initiation, per se, has been shown to be without impact [1, 2]. This is because separation and delivery of the placenta, not early suckling, acts as the primary trigger for lactogenesis (the onset of milk production). During pregnancy the breasts have been primed for milk production by a "cocktail" of maternal hormones, some intrinsic to the mother (prolactin, growth hormone, insulin, thyroid hormone) and others originating from the placenta (oestrogen, progesterone, placental lactogen, chorionic gonadotrophin). At birth the placenta is delivered, thus removing a significant source of the steroid hormones (oestrogen and progesterone) that have blocked the action of circulating prolactin upon breast tissue. Lactogenesis then begins, and measurable increases in milk output are detected between 30 and 72 hours after delivery [3, 4]. It is important to appreciate this fact, as retained placental products can be one of the few physiological constraints on the establishment of milk production. Any remaining placental tissue can secrete sufficient steroid hormones and thus continue to suppress the onset of milk synthesis [5].

Variability in lactogenesis

There are dramatic differences between women in both the initial changes in the rate of milk synthesis and the initial level of milk production. There can be a fivefold difference in the initial level of milk output, with infant intakes of between 200 and 900 g/24 hours on the fifth day post-partum [6]. This initial level is unrelated to birthweight; only at four to six weeks of age does infant weight predict intake [79]. Thus, production rates more likely reflect intrinsic variability between women. Physiological factors likely to affect this include variation in the amount of secretory tissue, in circulating hormone levels, and in the sensitivity of response to these hormones, a function of the hormone receptors associated with the secretory tissue.

One implication, however, is that milk production (triggered by placental delivery) is established without clear reference to the baby's size; it is only as a result of the interplay between the mother and her infant that the broad limits on milk output become refined to match the baby's needs. This, in effect, is a "calibration" process, which will involve upregulation of milk supply in the majority of women, whose initial milk output is low, but occasionally down-regulation of supply in women for whom it is initially excessive.

The crucial point is that breastmilk production (supply), which has been initiated "blind," must be progressively fine-tuned (calibrated) to meet the baby's needs (demand). If during this time the baby were offered calories from another source (for example, artificial formula), the blunting of appetite so caused might lead the mother's breasts to underestimate her baby's true needs, with the resultant danger that milk output might be calibrated at an inappropriately low level.

There is clinical evidence (personal observation, author's clinic) that in some women this process of down-regulation may be irreversible. So, if milk output fails to be optimized in the early weeks because of poor management, or if appetite is depressed because of competing calories from an alternative source, then once milk output has been set below the baby's overall needs, it may not be possible to reverse the process. For this reason, the avoidance of complementary milk feedings or "topup" bottles of formula is essential, as they are highly likely to interfere with the establishment of an adequate milk supply.

They can have a further non-physiological effect by undermining the mother's confidence in her milk supply, causing her to feed less frequently. In addition, an artificial bottle teat can represent a gratifying oral stimulus, in simple tactile terms, causing the infant to shift its preference from the breast to the bottle teat (this is discussed at greater length below). Pacifiers and nipple shields can pose a similar threat to the successful establishment of breastfeeding.

How long does this calibration process take?

Published data indicate that milk production continues to rise from birth to around four to six weeks, at which point it tends to reach a plateau [3]. A recent study has placed the population average for peak milk output at just short of five weeks [10], although this underplays the considerable variation that exists between women (five days and six months were the most discrepant points in a small sample of 30 women [6].

Nonetheless, evidence from a compilation of data (cross-sectional) from 16 studies of exclusively breastfed infants [3] indicates that milk output rises sharply until four to six weeks, then levels off at an average of 750 g/day for a singleton. (If a mother has twins, her milk output will continue to climb beyond 750 g/day to around 1,500 g/day, indicating that there is no absolute constraint on an individual woman's milk output, simply that 750 g/day represents the normal level at which milk output stabilizes for a singleton.) When the introduction of weaning foods is delayed, milk output is held at this level for weeks or months [11], until the introduction of solids causes fewer breastfeedings to be offered and milk supply to decline. In many cultures, however, weaning foods are introduced early. In Thailand, for instance, they are invariably introduced by one month of age. In such circumstances, there is a suggestion that they compete calorically with breastmilk, driving milk output down, rather than truly supplementing intake [10].

Factors affecting the establishment of lactation

Cultural Influences on breastfeeding

Breastfeeding fails far more commonly for cultural reasons than for biological reasons. There are few physiological constraints on a successful outcome for breastfeeding. In contrast, the wealth of factors impacting upon the individual woman from family, friends, health-care workers, and the world at large exerts an enormous influence on her. Just as these factors are acknowledged to influence the probability of her initiating breastfeeding, so, too, they are likely to exert an influence over her tendency to continue once she has started.

It is axiomatic to a successful outcome that women should want to breastfeed; women who encounter and overcome breastfeeding problems usually attribute their success to their own perseverance and determination. How do health-care workers inspire in women the desire to breastfeed, and how do they influence their motivation to succeed?

Women's attitudes and beliefs are shaped by their own experience but are also fashioned by cultural pressures, and it may be difficult for health-care workers to exert much influence over these. Nonetheless, epidemiologic research continues to identify the widespread health benefits of breastfeeding to both the mother and her infant [12-14]. If women are to make a truly informed choice on how to feed their infants, then health-care workers have an obligation to provide mothers antenatally with all relevant information about these benefits and about the hazards associated with artificial feeding, irrespective of any pre-existing choice the mother may have.

The role of health-care workers

In the past, a supportive environment for the new mother would have been provided by the extended family, whose members would have undertaken most of the routine tasks that would otherwise fall to the mother. In traditional rural communities of the developing world, cultural taboos on undertaking household tasks may apply for four to six weeks after delivery [15], the time taken for the milk supply to become established. The absence of the extended family in industrialized cultures suggests that motherhood generally is undervalued. In many cultures, particularly those in transition, family ties have been eroded and the extended family has become so fragmented that new parents may have little contact with relatives who would traditionally have provided help and support. Furthermore, in those cultures where bottle-feeding has predominated over the past decades, a vast cultural expertise on breastfeeding has been lost. Under such circumstances, one would hope that health-care workers (midwives and the primary health-care team in the community) would be in a position to make up these deficiencies by providing a collective professional expertise. In practice, however, such an idealized picture does not exist. Little emphasis is given to the management of breastfeeding in professional training, and health-care workers commonly lack both the breadth of knowledge and the core practical skills to enable them to manage lactation effectively. This situation should be rectified as soon as is practicably achievable, by including lactation management in the core training curriculum of every health-care worker whose designated role includes management of the nursing couple (midwives, for example). The emphasis should be on the acquisition of key skills through the mentor-apprentice system, and the combination of knowledge and skills is essential if women are to receive the expert support they need from health care staff.

Perinatal practices that affect the establishment of breastfeeding

It is legitimate to view the factors that either help or hinder the establishment of breastfeeding from the perspective of the maternity facility providing health care. Although largely unpredictable events can shape an individual mother's chances of establishing breastfeeding, there is enormous scope for hospital practices and staff attitudes to impact upon breastfeeding success.

  • In general, these factors can be grouped as follows:
  • antenatal parent education
  • quality of professional training in knowledge and skills
  • hospital policy on key practices
  • extended post-natal support, including both routine community support and specialist clinical support

The quality of support in each of these areas can be set through policy formulation and implementation by the maternity facility.

The impact of mafernity care practices

The expectation is of a supportive health-care system, but the reality may be even worse than indicated above. Too often, medical practices in hospital have impeded or hindered the successful establishment of lactation. Historically, separation of the mother and baby immediately after birth was rationalized without empirical justification [16]; such a policy necessitated nurseries for the care of the newborn, which further encouraged the routine giving of supplementary fluids, including formula. Abolishing nurseries as a concept and encouraging the mother to be the primary caretaker with responsibility for her infant through routine "rooming-in" is fundamental to reversing these outmoded practices.

A global campaign, the Baby-Friendly Hospital Initiative, sponsored by international health agencies (WHO and UNICEF) and supported by national governments, is now in place to reverse this situation, by ensuring that hospital practices are designed to protect and promote breastfeeding.

TABLE 1. Ten steps to successful breastfeeding

1. Have a written breastfeeding policy that is routinely communicated to all health-care staff

2. Train all health-care staff in skills necessary to implement this policy

3. Inform all pregnant women about the benefits and management of breastfeeding

4. Help mothers initiate breastfeeding within half an hour of birth

5. Show mothers how to breastfeed and how to maintain lactation even if they should be separated from their infants

6. Give newborn infants no food or drink other than breastmilk unless medically indicated

7. Practise "rooming-in"-allow mother and baby to remain together 24 hours a day

8. Encourage breastfeeding on demand

9. Give no artificial teats or pacifiers (also called dummies or soothers) to breastfeeding infants

10. Foster the establishment of breastfeeding support groups and refer mothers to them on discharge from the hospital or clinic

Source: ref. 7.

Under this initiative, hospitals are encouraged to match standards of post-natal care set out in the WHO/UNICEF "Ten Steps to Successful Breastfeeding" (table 1) and to seek external assessment against these criteria. If they are successful in demonstrating compliance with the global criteria, they can be designated as a "Baby-Friendly Hospital," in effect, a global charter mark in recognition that they have made a policy commitment to making the mother and her baby the focus of a supportive, caring environment in which breastfeeding can flourish. The core practices of the Ten Steps are as follows:

Policy formulation.. To minimize the tendency for new mothers to be given conflicting advice, it is vital for all health-care staff to adhere to the same set of practices. The best way to do this is for the maternity facility to establish a clear policy for the management of the new mother and her infant, training all health-care staff to a level where they understand the need to comply with this policy and are able to implement it with confidence. Monitoring staff compliance, breastfeeding intention, and outcome should then become a routine part of the audit cycle. Policies can be refined only if they are strictly implemented, followed by routine monitoring of specific clinical outcomes. Only then can the policy be modified to reduce any adverse outcomes.

Professional training. This requires a commitment to increasing the knowledge and skill base of hospital staff. Eighteen hours of training in lactation management, including at least three hours of supervised clinical practice, is urged by WHO/UNICEF as the minimum necessary for any member of the health care staff (previously untrained in lactation management) who has contact with the breastfeeding mother and her infant. Nonetheless, if routine training (a midwife, for example, might receive prequalification) combined with post-qualification skill development enable nursing staff to overcome routine problems of breastfeeding, these can be deemed both adequate and appropriate, whatever the duration.

Antenatal education. The quality of antenatal education, including whether the proposed method of feeding receives adequate discussion, is highly influential in determining whether women make a truly informed choice on how to feed their infants. It is also to be hoped that all potentially breastfeeding women receive sufficient preparation to avoid or overcome several common initial breastfeeding problems.

Early contact between mother and baby. Early initiation of skin-to-skin contact between the mother and infant, leading spontaneously to the first breastfeeding, is likely to be of fundamental importance in establishing close affectionate ties between them. In the immediate postpartum period, the mother is regarded as passing through a "sensitive period" [18], and the baby shows raised alertness at this time [19]. Although early skin-to-skin contact with the mother will undoubtedly help to reinforce the newborn's ability to seek and locate the breast [19, 20] and to facilitate recognition of the newborn [21, 22], there is little functional need for the altricial human newborn to "imprint" on its mother. For the human infant, it is more important to secure the mother's sustained emotional attachment, so that she continues to provide vital warmth, nourishment, comfort, and protection.

Therefore, early mother-infant contact serves the infant primarily by securing maternal attachment [23] and, as such, it is a biological imperative. Ensuring prolonged highquality contact in the immediate post-partum period, therefore, deserves to be a core practice of intrapartum care, irrespective of how the mother subsequently chooses to feed her infant.

Although there is some empirical support for a maternal sensitive period, there remains the question of whether giving high-quality skin-to-skin contact at a later stage may not also be capable of facilitating the development of emotional attachment, or, conversely, whether subsequent unrewarding or fractured breastfeedings may undo any initial benefits. Of the many studies conducted to evaluate the impact of enhanced early access of the mother to her infant, only one [18] has considered whether there are any deficits if the enhanced contact (45 minutes private, skin-toskin) is provided at a later stage (12 hours after delivery) compared with immediately after delivery. It showed a nonsignificant reduction in affectionate behaviour. A significant graded reduction in affectionate behaviour was observed, compared with a control group of mothers permitted only visual contact with their babies after delivery. Therefore, the evidence is rather slight to contest the possibility that prolonged, high-quality, skin-to-skin contact offered at any subsequent time might be capable of matching some, if not all, of the benefits of early mother-infant contact. If the mother has been deprived of early contact because of intrapartum medication or surgical procedures, high-quality contact should be encouraged with as much enthusiasm at a later stage. Furthermore, professional care should always be available during early breastfeedings and should strive to ensure they are as rewarding and problem-free as possible.

Further key practices. Although practices such as rooming-in and demand feeding may be regarded as essential to breastfeeding success, at a more general level they may be regarded simply as extending the newborn infant the courtesy of being regarded as an individual in its own right, rather than as an imperfectly formed automaton to be directed as we see fit. This change in philosophy in the way we view the human newborn is essential if we are to recognize that the newborn has much right to choice as the mother, although there is an obvious practical constraint on this choice being "informed." If the infants were in a position to make an informed choice on how they would be fed, on health grounds they would undoubtedly choose to be breastfed. It is difficult to see what cultural objections they might raise! So, we must learn to set their rights alongside the mother's and the father's in reaching a decision about the method of feeding. Although it is possible to constrain the infant's pattern of feeding to conform to a Western "idealized" cultural norm- as Pinilla and Birch [24] have shown for night feedings-there is no evidence that this benefits long term habit formation in the child, whereas it may prove detrimental to the infant's emotional development [25].

Avoiding bottles and teats. We have already dealt with the physiological reasons for avoiding unnecessary supplementation and the use of artificial teats and pacifiers. Each of the WHO/UNICEF Ten Steps is research-based, and although this step (step 9) is perhaps the least well supported, it can be defended by arguing both from first principles and from clinical experience. It is important to reemphasize at this point that we are considering events during the critical period of the establishment of lactation. It is acknowledged that different rules may apply during established lactation, when we accept that the occasional offering of bottles for social reasons (preferably of the mother's own expressed breastmilk) is unlikely to disrupt breastfeeding success.

Evidence from a study in Brazil indicates that the use of pacifiers is associated with a shorter duration of breastfeeding [26], as predicted. Clinical experience also suggests that pacifiers can impede the successful establishment of breastfeeding. Although the mechanism is not clear, certain lines of evidence can be considered.

First, ultrasound studies [27, 28] indicate that during suckling the mother's breast distorts and conforms to the internal geometry of the baby's mouth. Milk removal is achieved by the baby's compressing the base of the teatlike shape formed from the breast and nipple between his gums, and expressing milk from the sinuses lying within the "teat bulb" with a peristaltic wavelike action of the tongue. On a bottle teat, the infant attempts to achieve the same action, but because the artificial teat is more rigid, there is. instead, a tendency for the soft tissues of the baby's mouth to deform to accommodate to the geometry of the teat. Expressing milk from the teat bulb may be resisted by the less compliant material from which the artificial teat is constructed, with the result that the baby adapts by a shift towards extracting milk more by suction than by peristaltic expression. If the baby develops a reliance on one method of milk extraction over the other, he may not adapt well when offered both breast and bottle or when shifting between the two. To date, no specific carryover effect has been scientifically demonstrated; it has only been inferred from clinical observation.

Additionally, artificial teats may constitute a "supernormal" sign stimulus [29, 30], causing greater tactile stimulation of the baby's mouth than the more compliant breast. Whereas the breast naturally retracts elastically, the artificial teat remains in place, requiring little effort from the baby to hold it in his mouth. The supernormal stimulus, represented by the artificial teat, can compete for attention with the natural stimulus of the breast, and the baby, if exposed to it at an early stage, may be unable to ignore it. The outcome is that the baby may develop a preference for the artificial over the natural (nipple shields can be comparable in this respect). The term nipple confusion has been coined for the behaviour of the baby who refuses the breast in favour of the bottle or pacifier, but such a term may be insufficiently descriptive. The term acquired teat preference may be more accurate and would still embrace the established breastfeeder who refuses the bottle.

Another possibility is that bottle-feeding bypasses the triggering of the baby's natural adaptive reflexes for feeding and the maturation of the natural repertoire of responses necessitated by breastfeeding (rooting, gaping, drawing elastic breast tissue into the mouth, and suckling) [31]. There may also be a critical window during which the infant's natural response repertoire matures, so that time spent sucking on an artificial teat may represent both a lost opportunity and enhancement of an aberrant response repertoire.

Finally, the excessive use of soothers can mean that the baby is put to the breast either too infrequently or for too short a time, with the result that the baby does not secure sufficient nutrition. Not only can this adversely affect the infant's nutritional status, it will also disrupt the mechanism of supply and demand. At older ages, we have seen infants who are growing inadequately or are failing to thrive simply because pacifiers have been introduced. This appears to be due largely to the net reduction in suckling time and its effect on both immediate intake and future supply, which is only reversed when the mother makes active efforts to withhold the pacifier.

The use of pacifiers can also cause the earlier return of fertility, resulting in closer child spacing. In many cultures this may have an adverse impact on maternal as well as infant health [14, 32].

Cup-feeding. One way around the problem of giving additional fluids, where they are medically indicated, is to give them by cup or spoon [33]. In many centres, cup-feeding has been successfully reembraced and appears to be associated with a greater success rate for establishing breastfeeding.

A multicentre trial has been initiated in the United Kingdom to formally test such a view.

Individual-specific influences during the establishment of lactation

Practices that can either promote or impede breastfeeding success for the individual mother and her newborn can be broadly grouped into the following categories:

  • obstetric procedures intrapartum and use of analgesia
  • paediatric medical interventions necessitating admission to the neonatal intensive-care unit or step-down care nursery
  • maternal pathophysiology of milk production
  • routine post-natal practices affecting mother and infant care
  • quality of post-natal care and support

For the individual mother, there may be unexpected predisposing factors that militate against the successful establishment of breastfeeding.

In rare circumstances, the baby may be born with an oral anomaly that will require a specialist's attention, or the nature of the baby's birth (for example, pre-term, small for gestational age, or congenital abnormality) may require separation from the mother for medical care. Although medical services should be able to tackle many of the clinical problems with relative ease, the role of the mother at this time can often be overlooked. The one significant thing the mother may be able to do for her infant under these circumstances is to express her breastmilk, yet too few centres recognize the need to attach equal significance to this non-acute aspect of clinical care.

Excluding such medical crises, however, the baby may be sleepy or lethargic as a result of intrapartum analgesia (as from pethidine) [20] or may be irritable following an instrumental delivery. The resulting behaviour, either a lack of response by the baby or signs of discomfort when the baby is handled, may make it very difficult for the novice mother to handle her baby positively and with confidence, and she may feel her efforts to breastfeed are being rejected. Concern should also be raised over increasing reports that modern epidurals and gastric suctioning, either alone or in combination, adversely affect the initiation of breastfeeding; their impact should be evaluated epidemiologically.

The foetus may have had access to its thumb, fingers, or hand in the womb (often observed during antenatal ultrasound examination) and may have had the opportunity to acquire an artificial sucking style. If the foetus has become used to sucking on a discrete, relatively rigid object for several weeks, the infant may find the elastic, retractile tissue of the nipple and areola less attractive in tactile terms and thus may be reluctant to adapt to sucking at the breast. This theory could be readily evaluated by independent assessment of ultrasound scans and early sucking behaviour.

The main reason for raising this theoretical possibility is that it represents a potential individual-specific predisposing factor. We cannot yet predict which babies will or will not find the offering of artificial teats counter-productive to the establishment of breastfeeding, but simple adherence to the policy recommendation in step 9 of the Ten Steps should avert such a problem. It is explicit that this policy relates to the management of the normal full-term infant and that there are permissible clinical circumstances for departing from it.

Caution should be exercised, however, to protect against two harmful inferences: that because a baby has been observed on ultrasound to be thumbsucking in utero, problems will automatically arise with breastfeeding; or that difficulties of fixing and attachment in the early days are due to antenatal thumbsucking, so that no remedial efforts will be made. Neither of these inferences is defensible. Rather, the issue is raised because awareness of the possibility may help caregivers provide appropriate support rather than leaving the mother on her own to come to terms with an unrewarding infant who refuses to feed from the breast. It may be necessary for this baby to relearn how to suck correctly in the context of breastfeeding, in which case the offering of bottles, pacifiers, or finger foods will only perpetuate the artificial oral preference. A baby's early tendency to refuse the breast will undermine the learning experience for the new mother, whereas acknowledgement of her predicament and the offering of appropriate help and support will be encouraging and empowering.

Successful achievement of the technical aspects of breastfeeding will also be militated against if the mother is given inexpert help in attaching her baby at the breast in the early days [34]. Forcing her baby to the breast, or holding him there against his will, is likely to frustrate the woman's own efforts and can lead to many common complaints. The baby may also find these efforts aversive and develop a behavioural coping strategy that presents itself as breast refusal or rejection; once developed, this behaviour can be very distressing to both mother and infant and is often difficult to reverse.

Finally, research conducted with professional referrals to a clinical support service for breastfeeding women [6] has identified several classes of problems, all of which may be perceived as breastmilk insufficiency. While 98% of professional referrals to the clinical service were for reliable symptoms (for example, inadequate weight gain, unsettled infant behaviour, and sensations of reduced supply), up to 85% of them could be reversed by straightforward practical steps that included:

  • technical improvements to physical aspects of the breastfeeding process
  • optimizing feeding management (feeding frequency and duration, pattern of breast usage)
  • providing support and encouragement

Four demonstrable causes of insufficiency were identified. Genuine pathophysiologies of milk production represented only 2% of clinical referrals. Another category (5% of referrals) represented physiologically low milk output, while the remaining two (8% of referrals) would normally be regarded as lactation failure of maternal origin, but were in fact acquired conditions owing to suboptimal management of the nursing couple (for more detailed discussion, see ref. 6).

Conclusions

The factors most likely to contribute to a mother's initial success with breastfeeding are support and encouragement provided by health-care workers who are skilled and knowledgeable in managing lactation. These professionals must work within a system that is similarly caring and supportive, the policy of which recognizes the intrinsic rights of both the mother and the baby, allowing them unrestricted access to each other (as would be the case if the mother delivered at home). More proactively, the health care system and its staff should positively encourage those practices that have been shown to have a beneficial impact on the establishment of breastfeeding, while eradicating all practical hindrances. Finally, it is to be hoped that the mother will have a relatively trouble-free breastfeeding experience, or at least that her motivation and persistence with breastfeeding will be sufficient for her to overcome any problems she may encounter. A sensitive and supportive attitude from health-care staff will be highly valued by women and can contribute significantly to their success by boosting their confidence in their ability to breastfeed.

References

1. Salariya EM, Easton PM, Cater Jl. Duration of breastfeeding after early initiation and frequent feeding. Lancet 1978;ii:11413.

2. Woolridge MW, Greasley V, Silpisornkosol S. The initiation of lactation: the effect of early versus delayed contact for suckling on milk intake in the first week

post-partum. A study in Chiang Mai, Northern Thailand. Early Hum Dev 1985;12:269-78.

3. Neville MC, Keller R. Seacat J. Lutes V, Neifert M, Casey C, Allen J. Archer P. Studies in human lactation; milk volumes in lactating women during the onset of lactation and full lactation. Am J Clin Nutr 1988;48:1375-86.

4. Hartmann PE, Owens RA, Cox DB, Kent JC. Breast development and control of milk synthesis. Food Nutr Bull 1996;17:292-304.

5. Neifert MR, McDonough SL, Neville MC. Failure of lactogenesis associated with placental retention. Am J Obstet Gynecol 1981;140:477-8.

6. Woolridge MW. Breast-feeding: physiology into practice. London: Royal College of Physicians, 1995:30-2.

7. Pao EM, Himes JM, Roche AF. Milk intakes and feeding patterns of breast-fed infants. J Am Diet Assoc 1980;77:540-5.

8. Butte NF, Garza C, Smith EO, Nichols BL. Human milk intake and growth in exclusively breast-fed infants. J Pediatr 1984;104:187-95.

9. Imong SM, Jackson DA, Wongsawasdii L, Ruckphaophunt S. Tansuhaj A, Chiowanich P. Woolridge MW, Drewett RF, Baum JD, Amatayakul K. Predictors of breast milk intake in rural Northern Thailand. J Pediatr Gastroenterol Nutr 1989;8:359-70.

10. Drewett R. Amatayakul K, Wongsawasdii L, Mangklabruks A, Ruckpaopunt S. Ruangyuttikarn C, Baum D, Imong S. Jackson D, Woolridge M. Nursing frequency and the energy intake from breast milk and supplementary food in a rural Thai population: a longitudinal study. Eur J Clin Nutr 1993;47:88091.

11. Howie PW. Protective effect of breastmilk against infection. Food Nutr Bull 1996;17:373-83.

12. Dewey KG, Finley DA, Lrdal B. Breast milk volume and composition during late lactation (7-20 months). J Pediatr Gastroenterol Nutr 1984;3:713-20.

13. Victora CG. Infection and disease: the impact of early weaning. Food Nutr Bull 1996;17:390-96.

14. Rasmussen KM, McGuire MK. Effects of breastfeeding on maternal health and well-being. Food Nutr Bull 1996;17:36472.

15. Schmitt BD. Prevention of sleep problems and colic. Pediatr Clin North Am 1986;33:763-74.

16. Thomson M, Westreich R. Restriction of mother-infant contact in the immediate postnatal period. In: Chalmers 1, Enkin MW, Keirse M, eds. Effective care in pregnancy and childbirth. London: Oxford University Press, 1989:1322-30.

17. Protecting, promoting, and supporting breastfeeding: the special role of maternity services. SCN News 1989:4.

18. Hales DJ, Lozoff B. Sosa R. Kennel JH. Defining the limits of the maternal sensitive period. Dev Med Child Neurol 1977;19:45461.

19. Widstrom AM, Ransjo-Arvidson AB, Christensson K, Matthiesen AS, Winberg J, Uvnas-Moberg K. Suction in healthy newborn infants. Acta Paediatr 1987;76:56672.

20. Righard L, Alade MO. Effect of delivery room routines on success of first breast-feed. Lancet 1990;336:1105-7.

21. Macfarlane A. Olfaction in the development of social preference in the neonate. In: Porter R. O'Connor M, eds. Parent-infant interaction. Ciba Foundation Symposium 33. New York: Elsevier, 1975:103-17.

22. Varendi H. Porter RH, Winberg J. Does the newborn baby find the nipple by smell? Lancet 1994; 334:989-90.

23. Gubernick DJ. Parent and infant attachment in mammals. In: Gubernick DJ, Klopfer PH, eds. Parental care in mammals. New York: Plenum Press, 1981:243305.

24. Pinilla T. Birch LL. Help me make it through the night: behavioural entrainment of breast-fed infants' sleep patterns. Pediatrics 1993;91:436-44.

25. Bowlby J. Attachment and loss. Vol. 1. Attachment. London: Hogarth Press, 1969.

26. Victora CG, Tomasi E, Olinto MTA, Barros FC. Use of pacifiers and breastfeeding duration. Lancet 1993; 341 :404-6.

27. Weber F. Woolridge MW, Baum JD. An ultrasonographic study of the organisation of sucking and swallowing by newborn infants. Dev Med Child Neurol 1986;28:19-24.

28. Bu'Lock F. Woolridge MW, Baum JD. The development of the coordination of sucking, swallowing and breathing: an ultrasonographic analysis of term and preterm infants. Dev Med Child Neurol 1990;32:66978.

29. Tinbergen N. The study of instinct. London: Oxford University Press, 1951:13-31.

30. Gunther M. Instinct and the nursing couple. Lancet 1955;i:5758.

31. Hopkinson J. Garza C. Management of breastfeeding. In: Nutrition during infancy. St Louis, Mo, USA: CV Mosby, 1988:298-313.

32. McNeilly AS. Breastfeeding and the suppression of fertility. Food Nutr Bull 1996;17:340-8.

33. Lang S, Lawrence CJ, Orme RL. Cup feeding: an alternative method of infant feeding. Arch Dis Child 1994;71:365-9.

34. Royal College of Midwives. Successful breastfeeding. 2nd ed. Edinburgh: Churchill Livingstone, 1991.

Discussion of paper by Woolridge

Dr. Vald/strong>

I have a question regarding the group of women with an irreversible decline in milk output. You can use lactation in adopted mothers as a comparison. It takes longer, and the production doesn't increase as in the first month. It steadily increases throughout the first six months. Why doesn't that happen in a biological mother?

Dr. Woolridge

Our finding is disconcerting, especially when one hears about grandmothers in Africa who are able to re-establish lactation simply through suckling. Some of our interventions to boost these mothers' supplies have been quite aggressive, to see if there was any way of improving output. We would not diagnose the mothers who responded either to increased suckling or to pharmacotherapy. Where there has been substantial down-regulation, it is often difficult to shift back up. Where there has been up-regulation from birth, the potential to carry on up-regulation is retained. Downregulation, if it is excessive, can be a harmful process. Clearly there are other factors, particularly psychosocial factors in women in industrialized countries, that seem to exert a block over and above the motivation to feed. But in physiological terms, this down-regulation could be a critical factor.

Dr. Rasmussen

I am wondering if any of the babies in what you call the behavioural category, contented failure to thrive, are the ones who were rejecting the breast. Is there any indication that they are responding to the taste of the milk? That is, are mothers eating things that the infants are allergic to or just don't prefer?

Dr. Woolridge

There is no evidence of anything long-term. Certainly there is evidence that the baby will refuse or reject the breast for a brief period, either with the return of the menstrual cycle or from a particular food that the mother includes in her diet. But we haven't seen any long-term cases of breast refusal. I will cite two anecdotes, however. One is a mother who had a severe case of thrush, and she had been given a whole set of pharmacological preparations by her general practitioner. She was putting Timodene, which is for athlete's foot, on her nipples, and the baby was going to the breast but pulling back. She also smoked, and we weren't sure if it was the taste of the nicotine or tar products in her milk. While chatting with her, I squeezed some of this Timodene out onto my finger and tasted it, and it was quite revolting. Clearly, the Timodene was responsible for this baby's reluctance to go to the breast, and that had been going on for eight weeks.

The next example is also quite disconcerting. Recently we saw two babies whose first breastfeedings after delivery had been interrupted to give oral vitamin K. The babies grimaced at being given the vitamin and then refused to breastfeed for the next five days. Now, if you want to teach a baby what is harmful and bad, you give it a feeding and then follow it with a distasteful flavour, a perfect case of one-trial learning. You have to be very careful about when oral preparations are given to the baby, and not give them in association with the first or subsequent breastfeedings.

Dr. Prentice

I wish to continue with the discussion about irreversibility, because certainly in our Gambian experience it is difficult to see how that fits in. Certainly, we see women whose breastmilk volume goes way down in the wet season, possibly because they have become very anorexic with various infections. Then their breastmilk volume will come back up again, will double, and they will be well past the six weeks of lactation at that stage.

Dr. Woolridge

If one accepts that the calibration process takes four to six weeks, the results of down-regulation may differ if the weaning process invades that critical period or comes after it.

Dr. Prentice

What we see is at a later stage. This makes me wonder about the underlying physiology: for example, the role of the number of lactation cells, and what affects their longevity. Are we observing down-regulation? Is the process truly irreversible? What proportion of your subjects producing less than 450 ml of milk were in the irreversible group? Could those you were calling lazy children get used to being down-regulated? Would those mothers respond by increasing milk volume?

Dr. Woolridge

There is some overlap between the groups in about 4% of the clinical population. So I am not suggesting that we should suddenly recalibrate our views, but it is a possibility to be aware of; that is, the process of down-regulation can create clinical dilemmas.

Dr. Victora

I have a question about one of the Ten Steps to Successful Breastfeeding, which relates to the use of pacifiers or dummies. We looked into the literature a couple of years ago and found virtually nothing. Since then, we have done a couple of studies in Brazil that showed that children who had a pacifier introduced in the first month of life were three times more likely to be weaned in the subsequent three to four months than children who were not using a pacifier. The magnitude of this effect was about as large as that of introducing a bottle with artificial milk, so we were quite impressed by our finding. Obviously, we can't know whether this is a cause-effect association, or if pacifier introduction is a maternal strategy for weaning the child. I wonder if you have any data on that, and also if you could let us know if you have had any success in the United Kingdom in preventing mothers from introducing the pacifier?

Dr. Woolridge

We did try to discourage the use of pacifiers up to the time Ed Mitchell found that pacifiers might be protective against sudden infant death syndrome. We are still quite anxious to find out what the explanation for that particular finding is. It is an area where there is huge reluctance, as many women in the United Kingdom use pacifiers quite extensively. Here is one scenario of how these behavioural problems come about. Let's say you have a baby who has had access to his thumb or fist in utero and has become used to sucking on a small, rigid, discrete object. Suddenly the object is no longer available. The baby is encouraged to go the breast, but it doesn't find the breast as physically discrete in terms of its tactile qualities. The baby initially refuses the breast, but the midwife is rather heavy-handed and insists that the baby go to the breast. The baby starts to fight and refuses the breast, and after about three days of this, someone eventually gives in and gives the baby a bottle. The baby thinks, "Wonderful, this is what I have been missing out on," as this is closer to the thing that the baby has been used to. There is some evidence in some babies that, if you like, some antenatal preconditioning changes their expectation of what they should get afterwards. I will show you one last slide. There is much talk about "nipple confusion," which is an expression I don't like. Having trained as a zoologist, I thought I would bring you a piece of Dutch ethology. This is a slide showing how you can fool an oystercatcher into incubating the wrong clutch of eggs. If you give it a clutch of eggs that is larger than its normal clutch, it will incubate those in preference to its own clutch. If you give it a football that is painted to look like its eggs, it will try to incubate that. This is what is called a supernormal stimulus. It's so good at switching on the animal that it can't be refused. Nature didn't expect scientists to come along and paint footballs the colour of eggs. I do think that bottle teats and pacifiers represent supernormal stimuli for the baby. If you like, they stimulate the mouth with a greater tactile strength. For some babies, if breastfeeding is unsatisfactory, they will actually refuse the breast in favour of this more tactile object.

Professor Hanson

You made a comparison between lactating mothers in the United Kingdom and in Thailand. I would like to ask if you could qualify that a bit. Does this mean you are comparing British mothers who are exclusively breastfeeding with mothers in a traditional society, where I am convinced they rarely breastfeed exclusively? For instance, on the Indian subcontinent, a number of traditional foods that are introduced early to the infant are heavily contaminated and may have severe consequences for the infant's future life. A number of severe infections originate from this feeding practice. Once they start other foods, exclusive breastfeeding is rare. Could you speak about this?

Dr. Woolridge

I think the boundaries are very blurred. In Thailand some women initiate weaning foods purely on an experimental basis, introducing very low levels of supplement from, say, one month to three months of age. It's only at about four months that they start to give those weaning foods in substantial amounts, but I agree about the potential contamination. What is intriguing in Thailand is that many of the traditional methods of preparing weaning foods make the food sterile. They will steam rice in a vine leaf, which removes the pathogen load. In the United Kingdom very few mothers actually exclusively breastfeed. The specific recommendation of the Department of Health is to delay the onset of weaning until three months, but when you survey women, you find that most of them have offered their babies something by 10 weeks of age. So in fact there is not quite the discrepancy you might expect between these two cultures.

Professor Hanson

I will not be using the term weaning food in the same way that you do, because from the start of breastfeeding, the whole family-for instance, in Pakistani societies-will participate in feeding the baby and will put all kinds of food in the baby's mouth. This certainly brings the risk of infection and doesn't bring much energy or useful food to them. It is a risk that I think is often disregarded. You would need someone to stay with the family to find this out. What has been called exclusive breastfeeding has often not been.

Dr. Hartmann

I would like to go back to the relationship between socioeconomic class and breastfeeding. The same sort of thing happens in Perth, Australia. In the high socio-economic class about 80% of mothers breastfeed to six months of age. But this is a very recent behaviour. I think the problem is that we haven't successfully reached the lower socioeconomic classes with the breastfeeding message, and that is why breastfeeding rates have reached a plateau.

Dr. Woolridge

I agree, and unfortunately that group is often also very difficult to target in many other respects, such as in relation to the discontinuation of smoking and the way in which they use their financial resources.

Dr. Rasmussen

I want to come back to the comment on the pacifiers and offer you an alternative theory from the maternal perspective. A hungry breastfeeding infant is a vigorous young person who may make the mother's nipples quite sore. The introduction of a pacifier can have what I call the "nipple-saving effect" on breastfeeding continuation in women who might otherwise discontinue. Now in that case you may have women whose breastfeeding is already very adequate, and the pacifier has no effect whatsoever. It may be superior to giving the baby other foods, or it might not be.

Dr. Woolridge

Clinically, our objective when we are counselling women with distressed, unsettled infants is based on the premise that the infant has an appetite-control mechanism and that the most likely regulator of that control is fat intake. We try strategies that maximize the efficiency of milk delivery, so that she can help her baby achieve a state of satiety. You are quite correct that, even when she has an ample supply of milk, if the baby is unsettled, she is likely to resort to a pacifier to find some other way of settling the baby, rather than have her nipple traumatized in the process. Clinically, we focus on the primary target of ensuring delivery of synthesized milk, and then we address colic and other concerns as secondary matters.

Dr. Vald/strong>

One thing I was surprised to see was the differences between economic classes. In the developing countries it is just the other way around: our lower-economic-level mothers nurse much more than those at higher levels. At the same time, we feel that mothers in the lower economic groups are easier to reach. We are much more successful in addressing and changing their behaviours.

Dr. Woolridge

Certainly, there are ways in which it is quite inappropriate to compare an industrial country with Thailand. In the United Kingdom in 1940, the picture is reversed. What is surprising is how difficult we are finding it to target women in the promotion of such a recently acquired practice. Artificial formula was quite appropriately developed as an emergency backup option, but the trouble is that it has become the first choice of too many people.

Dr. Vald/strong>

I have some comments related to pacifier use. I can't understand why the mother would have sore nipples.

Dr. Rasmussen

Poor positioning would do it.

Dr. Vald/strong>

If the mother correctly positions the infant when she breastfeeds, for whatever time, she won't have sore nipples. But what we observe, in waiting rooms for example, are mothers who naturally put the baby to the breast when the baby cries. There, you have short feedings. The mother who uses a pacifier instead of putting the baby to the breast loses an opportunity to feed.

Dr. Pollitt

Just a short comment in connection with this issue of "nipple confusion." We have to remember that sucking on a pacifier is different from sucking on a breast. With the pacifier there is no negative pressure, and the activity of the tongue differs.

Dr. Woolridge

There is also no fluid delivered, so there is no need for phase-locked sucking, swallowing, and breathing, whereas on the breast these different activities have to be phase-locked. On a pacifier breathing is carried out independently from sucking.

Professor Hanson

I'd like to come back to the point of motivating women in poor countries to breastfeed exclusively. We were impressed to find that a motivation campaign in very traditional areas-villages, subslums, and city slums-results in substantial increases in this practice. Even traditional societies can be approached very successfully.

Social and biological determinants of lactation

Salvador Villalpando, Samuel Flores-Huerta, Mardia L-Alarcand Ignacia Cisneros-Silva

Abstract

During the last decades breastfeeding rates have fallen to such a level that at least one

million infant deaths annually have been attributed to the replacement of breastfeeding by formula-feeding. After the recent World Summit for Children, unprecedented efforts were targeted to reverse this trend. The evolution of breastfeeding patterns and related practices in Mexico is presented as a case study. Before the Baby-Friendly Hospital initiative, the rate of breastfeeding initiation and the average breastfeeding duration in Mexico were among the lowest in developing countries. The use of formula in hospitals was common. Knowledge about breastfeeding and awareness of its advantages were low among the public and health professionals. The International Code related to breastmilk substitutes became law, and the Baby-Friendly Hospital Initiative was included in the National Plan for Health in 1991. Formula manufacturers decided voluntarily to stop advertising their products. After five years, several surveys show noticeable changes in hospital policies and practices regarding breastfeeding promotion and improvement in the rate of breastfeeding initiation and exclusivity. Total duration of breastfeeding, public awareness, and mothers' knowledge about the basics of breastfeeding are increasing. Despite continued inadequate post-partum support and counselling, and an inconsistent effectiveness in conveying to the public the benefits of breastfeeding, progress has been made in the last five years and will be reflected in improved infant health in the near future.

Introduction

Humans are the only mammals whose offspring survives without natural lactation. This has been made possible on a worldwide scale by technological developments for modifying and preserving milk from other species [1]. As a result, the breastfeeding rate in developed countries has fallen dramatically. In the mid-1940s, about 50% of infants were breastfed up to three months in England and Australia; by 1971, only 25% of American babies were breastfed. Concerns regarding the negative effects of artificial feeding of infants resulted in the active promotion of breastfeeding as a healthier feeding mode. Currently, up to 80% or more of mothers breastfeed up to six months in some countries, although rates are highly variable [2].

A similar decline in the rate of breastfeeding has occurred in developing countries. It started 20 to 30 years later than in their affluent counterparts. The deadly consequences of such a decline are eloquently summarized by Stephen [3] in his report as a representative of the United States Government to the 34th World Health Assembly. He pointed out that at least one million infant deaths in developing countries are due to diarrhoea and malnutrition associated with formula-feeding. As part of the multinational agreement signed during the World Summit for Children, important national and international efforts were directed towards curbing and reversing the prevalence of formula-feeding in developing countries.

Mexico: A case study

To address the social and biological determinants of lactation establishment, I will present the case study of Mexico as an example, because Mexico lags behind many Latin American countries in improving the frequency and duration of breastfeeding [4]. The social determinants will be classified as (1) the general framework represented by the economy and the pertinent national policies, (2) the organizations acting as health-care purveyors, (3) the training and commitment of health-care professionals, and (4) the individuals participating in the process of lactation.

The magnitude of the problem in Mexico

Before the Baby-Friendly Hospital Initiative started its operation in Mexico in 1991, the frequency of breastfeeding was highly variable in rural, urban, and metropolitan communities. Recently, Pz-Escamilla reviewed the studies reporting the prevalence of breastfeeding in Mexico from 1953 to 1988 [5]. In these studies the percentage of women initiating breastfeeding ranged between 84% and 99% in rural and urban populations. For the purpose of this article, the data originally categorized as urban by PzEscamilla were separated into urban and metropolitan, defining metropolitan as cities of more than one million inhabitants during the year the studies were conducted. This distinction is relevant because of differences in rural-tourban migration rates and in the availability and accessibility of health care services. As seen in table 1, breastfeeding prevalences at birth varied widely among rural (73% to 99%), urban (79% to 94%), and metropolitan (59% to 86%) populations. Urban and metropolitan populations tended to have lower prevalences of breastfeeding. The prevalence was progressively lower at three and six months postpartum in the three categories. The most notable reduction occurred in the urban and metropolitan groups. The wide variability in the prevalence might be attributed to differences in the operational definitions of breastfeeding, differences in sampling procedures, and the extreme differences in the sample sizes of the referred series (median, 105 subjects; range, 50 to 5,011).

A more reliable picture might be obtained from three nationwide studies [6-8]. The proportion of never-breastfed infants in the 1986 National Health Survey in the 32 Mexican states [6] ranged from 5% to 34% (median, 21%). Another study, representing all geographic regions and both urban and rural populations, found an overall prevalence of breastfeeding in the first months post-partum varying from 60% among the urban elite to 89% in rural populations [7]. These figures dropped to 18% and 54%, respectively, at six months. The National Nutrition Survey of 1988, based on a probabilistic sample, reported that 13.8% of infants younger than four months never received breastmilk, while 60% were fed breastmilk for at least four months, but only 11.5% were exclusively breastfed for this period. They found significant regional differences in the prevalence of breastfeeding and determined in a hazard analysis that better living conditions (a proxy for socio-economic situation), higher levels of maternal education, introduction of other milks, and living in urban municipalities were detrimental to breastfeeding. Data about exclusive breastfeeding, defined as being fed breastmilk but no other milks or liquids, were available in only two series [7-9]. The prevalence of these feeding categories at one month postpartum was 19% (7) and 23% (8, 9), and at three months, 0% and 3%.

Surveys conducted after the Baby-Friendly Hospital Initiative was launched indicate that the prevalences of breastfeeding and exclusive breastfeeding are increasing. In metropolitan Mexico City, the initiation of breastfeeding was reported as universal [10]. Within the first month postpartum, breastfeeding prevalence was 76%, with an 11% rate of exclusive breastfeeding; at four months post-partum, the rates fell to 57% and 4%, respectively. Preliminary data from a larger study conducted in 36 public and private hospitals in 1994 and 1995 showed that before hospital discharge, the overall prevalence of breastfeeding was 87%, and the prevalence of exclusive breastfeeding was 70% (E. Rios, personal communication, 1995). Another study combining data from mother-infant pairs participating in a breastfeeding promotion programme and data from controls reported a 93% prevalence of breastfeeding at one month post-partum, falling to 74% at four months post-partum. No data on exclusive breastfeeding were available [11].

TABLE 1. Median (range) prevalence of breastfeeding according to residence and age of child in the series reviewed by Pz-Escamilla and Dewey [5]a

Age Rural Urban Metropolitan
No. series % breastfeeding No. series % breastfeeding No. series % breastfeeding
Birth 13 91
(73 -99)
9 85
(79-94)
5 66
(59-86)
3 mo 2 73.5
(63-84)
6 55
(33-78)
6 54
(19-80)
6 mo 9 77
(47-99)
4 52
(33-52)
6 36
(12-52)

a. The series represent samples or subsamples from individual geographic localities defined by the authors in each article.

Economics and national policies of breastfeeding

The manufacturers of infant formulas are frequently international enterprises. Their market interests go beyond formulas and even beyond specialized products for infants and children. In Mexico one manufacturer controls more than 75% of the infant formula produced within the country and more than 97% of the powdered formula. This almost monopolistic control gives manufacturers a great influence on market regulation [12, 13].

The International Code for Marketing Breastmilk Substitutes was adopted by the Mexican health authorities in 1989. Two years later, the Mexican Congress enacted the code into law. The Ministry of Health included the BabyFriendly Hospital Initiative in the National Plan for Health [14]. As a result, by the end of 1994, 15% of the 532 qualified hospitals in the country were awarded the title of Baby-Friendly Hospitals [15]. Before the Baby-Friendly Hospital Initiative was implemented in Mexico, formula and baby foods were advertised extensively and promoted heavily by hospitals, paediatricians, and nurses. A very high percentage of hospitals received free or reduced-price formula from manufacturers. Only 7 of 59 hospitals purchased all their formula, and only 2 paid full price [12]. Usually, hospitals were supplied by more than one manufacturer. In the majority of cases, hospital officers stated that such donations were unsolicited. In addition, manufacturers were allowed to distribute samples of formula to mothers at the time of hospital discharge. Mothers were approached outside the hospital premises in most cases, thus relieving hospitals from legal responsibility.

In 1993 all companies selling infant formulas in Mexico signed a voluntary landmark agreement committing themselves to stopping these practices. As a result, the report of the US Agency for International Development/Latin American and Caribbean Health and Nutrition Sustainability (USAID/ LACHNS) [16] found that distribution of free samples or gifts to mothers by formula companies almost vanished from the two hospitals surveyed. In a subsequent study of 36 hospitals conducted by Rios et al. (E. Rios, personal communication, 1995), officers from seven hospitals acknowledged accepting free or low-priced formula supplies.

Health-care Institutions

Perhaps the most contradictory aspect of Mexican healthcare institution policy related to maternal and infant health is the mandate by labour laws to provide mothers of infants a free six-month supply of a breastmilk substitute. In the past, conflicts within hospitals between the declared norm and the practice were frequent. In a survey of 59 hospitals in 1991, administrators claimed to have installed facilities and to have adopted routines favourable for breastfeeding. Nevertheless, investigators observed significant deviations from their claims [17]. For instance, none of the hospitals practiced early mother-infant contact. Although most claimed to have facilities for rooming-in, only 5% practiced it systematically. Most hospitals kept newborns in nurseries and provided mothers with portable cribs for the infants during the daily visits of the infants to the mothers' rooms. Infants were fed formula in the nurseries, having very few occasions to suckle at the breast. Only 4% of the hospitals allowed exclusive breastfeeding during the day; almost 16% did so during the night. The hospital schedules for breastfeeding were related more to staff shortages than to intentional policies. About half of the hospitals surveyed provided new mothers with written information about how to feed their babies at discharge. Although material encouraging breastfeeding predominated, it was astonishing to find that 20% of the hospitals provided information encouraging bottle feeding [17].

Preliminary data obtained by the follow-up study in 36 hospitals by the Nestle Infant Formula Audit Commission conducted by Rios from 1994 to 1995 (E. Rios, personal communication, 1995) provide evidence of a substantial improvement in those policies and practices. About half the mothers suckled their babies in their own beds, though only a small percentage were allowed to suckle within the first 30 minutes post-partum. About 80% of breastfeeding women had proper facilities in the hospital that enabled them to feed their infants throughout the day. At discharge 40% of the mothers reported they had participated in educational activities about breastfeeding, and 4% had received information exclusively about formula-feeding. The USAID/LACHNS report [16] found that elimination of infant formula from hospitals was a widespread practice, probably because breastfeeding is less time-consuming and produces substantial savings. In contrast, the implementation of other policies had less success. In two hospitals with full rooming-in, 40% to 60% of the infants were fed before the initiation of breastfeeding, most of them with oral glucose solutions. The funding for educational activities and counselling was low, and the intended educational messages were not conveyed efficiently.

A recent survey compared the performances of 14 public hospitals in Mexico City. Half were certified as Baby-Friendly Hospitals [18]. The evaluation was based on interviews with mothers on discharge from the hospital. The questionnaires explored the hospitals' policies related to the "Ten Steps to Successful Breastfeeding" [19]. Certified hospitals scored significantly better than noncertified hospitals in many areas: pre- and postpartum instructions on infant feeding, the numbers of infants suckled within the first 30 minutes of life, rooming-in, exclusive breastfeeding, non-use of feeding bottles, and availability of support groups. Encouragement from the health team to breastfeed was similar in both types of hospitals. Formula was prescribed for a negligible proportion of mothers. It must be underlined that despite the differences described, the non-certified hospitals have had a good level of compliance with the policies of the Baby-Friendly Hospital Initiative. The effect of rooming-in on the initiation of breastfeeding was compared in a cohort of 15,574 mother-infant pairs [20]. Sixty-eight per cent of the infants in the rooming-in programme breastfed within six hours after birth, and all were breastfeeding at discharge. None of the infants in the traditional wards did so. In spite of the shortcomings described, active breastfeeding programmes have a clear and positive impact on breastfeeding prevalence.

Another problem is the high proportion of Caesarean deliveries, which might interfere with the decision of women to breastfeed. A longitudinal study by our group [11] found that almost 30% of the women in a cohort delivered by Caesarean section. These figures are consistent with many other reports. Although women giving birth vaginally breastfed more frequently than those delivering by Caesarean section, breastfeeding rate differences vanished by 60 days post-partum, making it evident that rooming-in stimulates the initiation but does not lengthen the duration of breastfeeding.

Health professionals

There is a general notion that physicians and allied professionals in Mexico lack adequate skills to advise lactating women about initiating and sustaining lactation. Such a notion is based on the evidence that their knowledge of nutrition is very superficial [21]. Nutrition is not included in the curricula of medical schools as an individual discipline. The principles of infant feeding are taught in courses of paediatrics. The most popular textbooks of paediatrics have 3 to 6 pages of information on human lactation and 9 to 25 pages of information on artificial feeding, and comparable amounts of classroom time are devoted to these topics.

In a recent study more than 500 medical students and more than 170 residents from different Mexican universities answered a questionnaire exploring their knowledge of the basics of nutrition [22]. The critical grade for an appropriate level of knowledge was 4.3, which was higher than the average grade of the medical students and residents. In 1992 the National Centre for Maternal Lactation launched a programme to train health professionals in infant nutrition and breastfeeding. The Centre produced educational materials to support the future educational activities of those graduating from the Centre. There has been no published evaluation of this programme.

Individual beliefs

The multiple social factors that are important to the establishment of lactation vary among cultures. In Mexico regional differences often encompass significant cultural diversity. Such differences will be illustrated by data gathered from two independent cohorts of 346 urban and 216 rural mother infant pairs.

Communities studied

The rural setting is the Otomi Indian village of San Mateo Capulhuac north-west of Mexico City (n = 216). The 5,000 inhabitants live mostly from subsistence agriculture, with maize the main staple. There is little consumption of animal products. The diet of lactating women is marginal in energy and protein and low in fat. The level of physical activity is high [23].

The urban setting is represented by two neighbourhoods of Mexico City: Iztapalapa in the southeast (n = 170) and Tizapan in the south-west (n = 176). Both are densely populated by families of low-income workers living in small apartments. The diet of urban lactating women is closer to the Recommended Dietary Allowances [24] in energy and protein than that of rural women. Their lifestyle tends to be sedentary.

Besides the geographic differences, the two groups have significant differences in level of poverty, education, and accessibility to a paying job. There are also differences in sanitary facilities in the home. Although piped water was available in most rural households, it was not chlorinated, and fecal contamination was the norm (table 2).

In the rural community, 99% of the infants were predominantly breastfed in the first two weeks (other liquids could be provided except for non human milk). These high rates prevailed up to six months (table 3). None of the mothers failed to breastfeed their previous children, and all mothers reported being breastfed as infants. Formula was not commercially available in the village at the time of the study, although feeding bottles were present. The price of one can of formula in the nearest town was equivalent to one day's salary. The high prevalence of breastfeeding seems to have very strong cultural support, while formula-feeding was not practised for economic reasons. The breastfeeding rate was also high (93%) immediately after delivery in the urban group. It declined progressively in the post-partum period. By the third month fewer than threequarters of the women were providing any breastmilk to their infants, and only 40% of the mothers were predominantly breastfeeding. At the end of the sixth month, 52% of the mothers were feeding their infants any breastmilk, and only 25% were feeding breastmilk without additional nonhuman milk (table 3).

TABLE 2. Socio-economic characteristics of the communities

Characteristic Rural
(n = 216)
Urban
(n = 346)
Poverty level of the communitya 4 2
Household characteristics
piped water 93% 92%
flush toilet 6% 87%
dirt floor 64% 11%
refrigerator 5% 60%
crowdingb 91 % 80%
Maternal characteristics
education, median years (range) 3 (0-6) 9 (2-14)
living with partner 98% 87%
working outside home 2% 32%

a. 1 = mildest, 5 = worst (see ref. 24 for explanation of scale).
b. Three or more persons per room.

Continue

Discussion of paper by Villalpando et al.

 

Professor Hanson

May I just comment on history? The first described case of artificial feeding was by one of the Assyrian kings. Also, in archaeological investigations of cultures along the Indus, many spoons and feeding utensils that were obviously used for artificial feeding have been found. So all through history this has been common. In Sweden in 70 and 150 A.D. there were areas where there was no breastfeeding at all; nobody knows why. And there was a law in Norway from 1040 that mothers should breastfeed, obviously, because of the fact that many didn't, so this is an old thing.

Dr. Prentice

I would like to explore a little more with you and Dr. Woolridge the issue of women feeling that they have insufficient milk. This seems to come out of every culture that we've heard about today, and, certainly, my experience in Africa is similar. Women will say that they are worried that they don't have enough milk. Where formula or other foods are available, they'll move on to either. What is it that women expect of a baby that makes them feel that they don't have enough milk? Dr. Woolridge showed that a lot of perceived milk insufficiency is found in women with milk volume in the normal range. From my own experience, having breastfed in the United Kingdom and in Africa, British women expect children to stay asleep for long periods at night. The family expects it even if the mother doesn't, which puts a lot of pressure on women to somehow make the child not feed at such frequent intervals. I just wondered if similar sorts of cultural problems would be underlying your women's responses as well?

Dr. Villalpando

I think the infant's behaviour often raises the question of whether milk production is sufficient. It is not the same in rural areas, where the infants probably cry as much as urban infants, but they don't have any other option.

Dr. Vald/strong>

Our rural mothers may breastfeed 20 times a day. In the waiting room, they feed once, twice, or three times. When you ask them how many times they have breastfed today, they say maybe one, two, or five times, but they don't have this notion that taking the baby to the breast often is a bother. But for mothers from higher socio-economic groups, if the baby is not quiet for four hours, which was what they were used to when the babies were bottle-fed, they feel they don't have milk.

Dr. Woolridge

I think there is a total difference in outlook between a mother in the United Kingdom and a mother in Thailand. As we have just heard, the mothers in Thailand have no expectation of failing. They just assume it is the only option, and they will do it successfully. Intriguingly, they still report perceptions of insufficient milk, but it doesn't cause them to discontinue breastfeeding. It is a common cultural concern, even in that sort of society. I agree that in the United Kingdom there is an expectation that a baby should sleep for long stretches to fit in with the adult lifestyle. It's an inappropriate expectation, and much of it has been derived from formula-feeding.

Dr. McNellly

Mary Houston investigated this question of insufficient milk. She concluded that for many women it was a legitimate reason for giving up breastfeeding. If a woman says she doesn't have enough milk, she shouldn't carry on, because it's going to damage the child. Some women were certainly using that as a legitimate excuse to stop breastfeeding.

Dr. Villalpando

I think that is true for our urban group. As you could see, the individual who most often bought the first can of formula without any advice was the mother. She was really legitimizing her decision to stop breastfeeding by saying that she had insufficient milk production.

Dr. Van Eskrik

If I may comment on the Thai example, different methods produce very different pictures. I was doing ethnographic work in another part of Thailand, and the discussions about insufficient milk were quite different. Of course, they are not phrased that way, but I came across two things quite regularly, not in questioning but from observation. First, women were becoming concerned that their breasts were too small, that there was something wrong with their shape. There are pictures on calendars in every tiny hut, and a woman would be very strongly influenced to think about whether or not her breasts were adequate to this task. That's something that I think is changing quite rapidly. The second is a fundamental approach, strongly linked with Theravada Buddhism, that the capacity to nurture well is a result of merit stored from former lives. This means that women talk about themselves as being someone who is either a good nurser or not a good nurser, almost as if we would say that this is a characteristic that they would expect to see in themselves. It is also very interesting to think about how women classify themselves as both mothers and women. I know it doesn't fit with the kind of work you were doing, but at least it suggests perhaps another way to look at cultural factors.

Professor Howie

May I make a point about almost a war of communication that seems to be a common factor in developed and developing countries? I think one of your slides made the point how clever formula manufacturers are at getting their message across. In fact, they target health professionals even more than they target the patients themselves, and how successful that campaign is! We have seen literature distributed by the manufacturers who now have an obligation to state the advantages of breastfeeding. They give one page on the benefits of breastfeeding and maybe five pages about cracked nipples, tiredness, and breast abscess. In fact, the section that is supposed to encourage breastfeeding mothers is targeted so cleverly that it has exactly the opposite effect. What do you feel about making a systematic attempt to get better education that is not dominated by the formula manufacturers, so that some misunderstandings about breastfeeding can be overcome? We recently asked mothers who were breastfeeding if they knew that the baby would lose weight in the first few days after birth, and the number who knew this was about 5%. We are simply not getting basic information over to our mothers, and I suspect from what you are saying that there is a failure in Mexico, the United Kingdom, and many other countries.

Dr. Woolridge

There are two sides to this problem. One is to attack the problem of medical education by working with assistant professors of paediatrics who are lecturing to students, inviting them to seminars about lactation and so forth. This is a huge task. The other is the lack of a strong network of people promoting breastfeeding awareness to hospitals, physicians, and the general public to counteract the propaganda from formula manufacturers, because most literature handed to mothers is prepared by those companies.

Dr. Perez

What is more comfortable for a working mother three months after the child's birth, breastfeeding or bottlefeeding, and why?

Unidentified speaker

I would say breastfeeding. The situation, though, is that we put so many obstacles against mothers breastfeeding successfully that we have this notion that the mother and baby have to be changed to fit the circumstances of work and so forth. We shouldn't be changing human behaviour, we should be changing working conditions to fit breastfeeding.

Dr. Villalpando

Many years ago the labour laws in Mexico supported long post-partum leaves of absence intended to aid breastfeeding. However, fewer than half of the mothers breastfed for such a long period, so the outcome was the reverse of what many expected.

Dr. Rasmussen

Let me put it another way, that convenience is in the eye of the beholder. If you do a survey in the United States, uppereconomic-class women will tell you that breastfeeding is by far the most convenient, for all of the reasons we know. If you ask lower-economic-class women the same question, you don't get the same answer. Their lives are chaotic, they're on the bus, they're embarrassed to breastfeed on the bus. The last thing in the world they consider breastfeeding to be is convenient for them. The answer to Dr. Perez's question depends on a woman's life circumstances, and whether breastfeeding works for her. It's wonderful to have labour laws to say you're entitled to a maternity leave, and if you have a job or are protected by these laws, that may be wonderful in other ways. The United States is in the embarrassing position of not even having such laws, so I can hardly cast any stones. What about women who work in the informal sector for whom there is no protection whatsoever? Their labour is just as valuable to their families, the interference of their work conditions with breastfeeding may be as great or greater, yet they have no protection at all. In their case, convenience, again, may be an issue.

Dr. Vald/strong>

We are researching that area. We have a study on working women, and one aspect we are concerned about is women's satisfaction with breastfeeding. We were surprised that the mothers in the control group who did not breastfeed were very satisfied, and the mothers who exclusively breastfed or human-milk-fed for six months, even while working, were equally satisfied.

Professor Hanson

I use the Swedish example, where it is rare for mothers not to breastfeed. They are entitled to 18 months off, most of that period with full pay, so it works.

Dr. Vald/strong>

To go back to the issue of insufficient milk and mothers' perceptions, I think many women don't understand lactation well. They are encouraged to think that their milk will come in and their breasts will feel very full. But at about four to six weeks the breast physiologically adapts, so that they have less fullness and enlargement. Some women interpret the change in sensation to mean that they have less milk. They really need to understand that lactation is an adaptive process, and even though the breasts are quite soft, they still produce milk.

Professor Hanson

One issue I don't think is covered much in connection with the insufficient-milk syndrome is the contribution that the infant makes to the mother's perception about insufficient milk. We have to remember that the infant regulates its intake by many different aspects of its sucking behaviour. To a large extent, this is accomplished by differences in sucking amplitude or frequency. The infant has some degree of control over what actually takes place. We seldom look at the contribution the infant makes to the mother's decisions regarding feeding.

This also extends to another comment I want to make in connection with the determinants of milk production. There is an enormous variability in birthweight in different populations in the world. In Sweden, for example, the average is approximately 3,500 g. In Santa Maria Cauque, Guatemala, the average is approximately 2,600 g, a 900-g difference. There is likely a relation between an infant's birthweight and its sucking behaviour. The degree of breastfeeding success in different populations is also determined, in part, by other infant characteristics. Yet in general, there tends to be a greater emphasis placed on the mother as the one who will make the final decisions on what is going to happen, and not enough attention is given to the infant's roles.

Dr. Garza

Let me go back to the role the infant plays, because I think it is an important one. In studies we did about 10 years ago, we were interested in understanding whether infants were hungry whenever they demonstrated behaviours that the mother interpreted as hunger. We followed women longitudinally for four months beginning at about the third month postpartum. Women who were planning to breastfeed for 6 to 12 months were recruited. At the point they introduced solid foods, we asked why they were doing this. I think 100% of them said it was because the child was either fussy or not sleeping. They were interpreting this as evidence that the child was hungry and, therefore, that they were unable to sustain or increase milk production sufficiently to satisfy the infant.

The remarkable thing, however, was that when we measured the energy consumption of infants before and after the introduction of solid foods, we found no difference. Thus, I think children give certain cues that women interpret as hunger but that are, in fact, driven behaviourally by other needs. The child likely has reached the point where it wants to put something else in its mouth, and mothers tend to interpret those cues as hunger. Because the infant's behavioural response to other foods is often positive, their mistaken interpretations are reinforced. In fact, those responses appear to have nothing to do with physiological hunger defined in the usual terms. There are inappropriate periods in early infancy to introduce other foods. The physiological timing of complementary foods determined by behaviours other than hunger is dependent on a number of conditions that relate to the infant's surroundings.

Dr. Villalpando

Studies have investigated infant intake by 24-hour test weighings. Fewer than 50% of suckling episodes result in the intake of more than 50 g of milk. The remainder result in the intake of as little as 5 or 10 g of milk. This suggests that the infant is not really hungry. It's just sucking for the joy of sucking.

Unidentified speaker

I would like to return to the determinants of a woman's preference, because I cannot understand why generally in Latin America, fewer than 20% of women are fully breastfeeding at six months post-partum? We need to find an answer to that.

Unidentified speaker

I haven't heard anybody talk about the same woman with different babies in successive births. Is past behaviour predictive of future behaviour?

Dr. Victora

We did research on that. Some mothers who tended to breastfeed one child for a long time were likely to do the same with the next child. If mothers breastfed a very short time, the results were about the same in subsequent pregnancies. There was, however, a gray area when mothers breastfed from one to six or seven months. They were very unpredictable. One could not predict what would happen with the next baby.

I would like to go back to a point raised earlier. I think babies have very strong personalities. When we did our pacifier study, the main factor influencing pacifier use was the infant. Some babies just refuse them, and those are the babies who tend to breastfeed longest.

Dr. Prentice

To add a caveat to that, in our African experience, where 100% of women were breastfeeding for 18 months or so, women in successive lactations tended to show a characteristic breastmilk volume and breastmilk composition. Thus, it's a mixture of culture, maternal feelings, and the way a mother's breasts work.

Breastfeeding and the suppression of fertility

 

Alan S. McNeilly

 

Abstract

Breastfeeding suppresses fertility for a variable length of time, but when certain criteria are applied, it can be a reliable contraceptive. The individual variation in duration of infertility is directly related to suckling activity. As suckling declines, follicle growth resumes and ovulation may occur. Infertility is maintained by suckling-induced disruption of the normal pattern of pulsatile luteinizing hormone release and is related to an increased sensitivity of the hypothalamus to the negative feedback effects of oestradiol. Even if ovulation does resume, the corpus luteum function is often insufficient to maintain pregnancy. Attempts to alter suckling activity to prolong lactational infertility are not successful, but maintenance of reasonable suckling frequencies of normal duration can protect women from pregnancy for a prolonged period postpartum.

 

Introduction

It is quite clear that breastfeeding results in a suppression of fertility for a prolonged period of time, depending on the pattern of suckling behaviour [1-3]. Stimulation of the nipple during suckling results in three responses: first, the release of oxytocin from the posterior pituitary to allow release of the milk present in the breast to the baby; second, the release of prolactin, which is essential for milk production for the subsequent feeding; and third, the suppression of gonadotrophin secretion, which results in suppression of ovarian activity. When established, the pattern of suckling varies considerably, and this is dependent on the mother and child and is not necessarily controllable. Throughout lactation, the duration of lactation and the duration of infertility are directly related to the suckling pattern. Attempts to increase suckling frequency to maintain longer durations of amenorrhoea have not been successful, because the mother and the baby interact so that the amount of nutrition received by the baby remains fairly constant [4]. As suckling frequency is artificially increased above that established in lactation, there is a concomitant decrease in suckling duration at each feeding. Thus, the overall duration and intensity of suckling remain the same, and there is no overall effect on the duration of infertility. It is, therefore, important to understand all the different components of suckling that relate to the suppression of fertility, and these have been reviewed in detail recently [2, 3, 5]. This article briefly reviews the present state of knowledge regarding the principal mechanisms involved in suckling-induced infertility.

 

Ovarian activity and the interbirth interval

The components of the interbirth interval are important to understand before any discussion of the control of gonadotrophin secretion during lactation. The interbirth interval consists of four periods: (1) the recovery from pregnancy; (2) a period of amenorrhoea during breastfeeding; (3) the resumption of the ovulatory cycles (which may not take place if a new conception occurs); and (4) finally, a new pregnancy. Over a number of years, we have investigated the interactions between the suckling pattern and the resumption of ovarian activity in relation to the pattern of gonadotrophin secretion. In some women, where suckling is maintained at a high level, ovarian steroid secretion can be suppressed for a number of months and even years, even in well-nourished Western societies [1]. In other women, where suckling frequency is lower, ovarian activity will resume earlier. In Edinburgh it was shown that if the frequency of suckling is maintained above five times a day and the duration is maintained above 65 minutes a day, amenorrhoea will often be the consequence [6]. Although the exact frequency and duration of suckling required to maintain infertility vary among societies, it is usually possible to establish a guide for the suckling required [7].

During the period of lactational amenorrhoea, the plasma concentrations of oestradiol secreted by the dominant follicle(s) remain minimal, in contrast to the normal increase seen during the follicular phase of the normal menstrual cycle [2, 3]. These results suggest that there is minimal ovarian activity, as follicle development during the normal menstrual cycle is always associated with an increase in oestrogen secretion. During early lactation (up to 12 weeks post-partum), ultrasound visualization of the ovary confirmed the absence of follicle development [8]. At later stages in lactational amenorrhoea, however, although oestrogen secretion remained minimal, follicles up to preovulatory size (around 20 mm diameter) were detected by ultrasound [9]. The reason for the presence of follicles that secrete low amounts of oestrogen relates to the effect of suckling on the secretion of the gonadotrophins luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The low steroid-secreting activity of these follicles presumably relates to a reduced input of gonadotrophin, particularly of LH. This possibility will now be discussed.

 

Changes in FSH and LH

During the menstrual cycle, a rise in plasma FSH at the beginning of the cycle stimulates the growth of a cohort of follicles, which increase to around 10 mm in diameter by the mid-follicular phase. At this stage, a single follicle continues to grow up to around 20 mm in diameter, becoming the preovulatory follicle that will ovulate. The selection of this dominant follicle is dependent on a fall in the plasma concentration of FSH occurring about days 6 to 8 of the follicular phase. As the follicle grows, it acquires the ability to secrete oestradiol by conversion of androgen from the outer thecal layer of the follicle to oestradiol by the granulosa cells within the follicle. Only LH, released in pulses, stimulates thecal androgen production. FSH alone does not stimulate steroid secretion from the ovary. The increase in plasma oestradiol secreted by the developing preovulatory follicle leads to positive feedback and the discharge of the preovulatory surge of LH. This induces ovulation, luteinization of the follicle, and formation of the corpus luteum, which secretes progesterone in response to a slow pulsatile secretion of LH. The progesterone and oestradiol released by the corpus luteum decrease the pulse frequency of release of gonadotrophin-releasing hormone (GnRH) from the hypothalamus, which drives the pulsatile release of LH from the pituitary. The decline in GnRH pulsatile stimulation, together with inhibin A released from the corpus luteum, leads to a major suppression of release of FSH and an inhibition of follicle development during the luteal phase. If conception does not occur, the corpus luteum regresses and the resulting drop in steroid and inhibin concentrations results in an increase in FSH that initiates the next wave of follicle development. These events are all closely coordinated and regulated by the rate of pulsatile secretion of GnRH from the hypothalamus, which stimulates the pulsatile release of LH. During the follicular phase of the normal menstrual cycle, the GnRH/LH pulse frequency increases to around one pulse per hour, and any disruption or slowing in the pulsatile release of GnRH/LH prevents normal follicle development and reduces steroid secretion by the developing follicle.

During breastfeeding the plasma concentrations of FSH increase rapidly after birth. By four weeks post-partum, they are within the normal early follicular range, whether or not breastfeeding occurs [10]. These levels of FSH are maintained throughout the duration of lactational amenorrhoea and are substantially higher than those seen during the luteal phase of normal cycles. Thus, any apparent absence of follicular development associated with low oestrogen secretion cannot be due to lack of FSH. Indeed, it is probable that this maintained high level of FSH is the cause of the observed growth of follicles up to the preovulatory level. The low steroid secretion must relate to the difference in pattern of LH secretion.

The pattern of 24-hour profiles of LH secretion at four weeks post-partum is very variable. Most women show no evidence of pulsatile secretion of LH, whereas in some there is a resumption of LH pulsatile secretion. But this occurs at random and at a slow frequency [11]. In some women with slow pulsatile LH secretion, pulsatile release of FSH is also seen, a rare occurrence in the normal menstrual cycle that is related to the very low levels of oestrogen and inhibin released from the inactive ovary. As the pulse frequency of LH secretion increases, the pulsatile release of FSH is lost, and a natural pattern of FSH secretion similar to that in the normal cycle resumes. Thus, FSH pulses may occur, but only when the negative feedback from the ovary is suppressed. After four weeks there is a gradual increase in the frequency of pulses of LH, but for many weeks, particularly during lactational amenorrhoea, the pulse frequency remains erratic and below the normal follicular phase frequency required to stimulate normal oestradiol secretion from any developing follicle. Thus, although the plasma levels of FSH are sufficient to stimulate follicle development as seen by ultrasound, the suckling stimulus prevents the resumption of a normal frequency of pulsatile LH secretion, and the follicles make only limited amounts of oestradiol. The rate of return of normal pulsatile secretion is very variable among women, and it is this variation that causes the variation in the resumption of fertility. It is presumed that the variability is due to the differences in the patterns and intensity of suckling, and that this is why it is difficult to control.

The disturbance in the pattern of pulsatile LH release is almost certainly the cause of the lack of oestrogen secretion by follicles, resulting in a lack of ovulation. In a study in which GnRH pulses were replaced at the normal follicular phase frequency of once per 60 minutes in breastfeeding women at six weeks post-partum, at a time when ovarian activity was completely suppressed as indicated both by oestrogen and by ultrasound, normal pre-ovulatory follicle growth and oestrogen secretion were induced without a problem [8]. Ovulation occurred, although this was followed by an inadequate corpus luteum. When the pump was turned off and GnRH infusion stopped, ovarian activity was suppressed for at least 10 weeks in most women. Thus, restoring a natural, follicular-phase pattern of pulsatile GnRH secretion in breastfeeding women will induce the growth of normal pre-ovulatory follicles, indicating that the aberrant pattern of LH secretion during lactational amenorrhoea causes the failure of normal oestrogen secretion. Therefore, no pre-ovulatory LH surge would be induced, owing to the lack of oestrogen-positive feedback, and ovulation would not occur. Prolactin and suckling remained high throughout the period of GnRH pulsatile infusion between 6 and 10 weeks post-partum, showing that there was no direct interference of prolactin with gonadotrophin action at the ovarian level.

The mechanism by which suckling interferes with the normal pattern of GnRH release is unclear. The potential role for endorphins acting in the hypothalamus has been discussed elsewhere [3,12]. Infusion of the opiate antagonist naloxone failed to increase the secretion of LH and FSH in a significant manner in normal breastfeeding women [13]. Nevertheless, in women receiving the progesterone-only birth control pill, a small increase in LH and FSH release did occur. This could be expected, as the negative feedback effect of progesterone on GnRH pulsatile secretion during the luteal phase of the menstrual cycle is thought to be mediated by an increase in opiate tone within the hypothalamus. One interesting observation was that treatment with an opiate antagonist increased the amount of LH and FSH released in response to GnRH. At the present time, there is no explanation for this effect, because no opiate receptors have been described in the pituitary gland. It may be that the opiate tone is so high in the hypothalamus that we are unable to give sufficient opiate blocker to affect the system. Because of passage of the blockers to the infant through the breastmilk, however, it would be unethical to use higher doses than we originally used. Thus, a role for endorphins in the suckling-induced disruption of GnRH release remains unproven in women.

There is one final aspect of the control of GnRH release, and hence of LH and FSH release, which is very important. Treating breastfeeding and bottle-feeding women with oestrogen at different times during the return of fertility during lactation showed clearly that there was an increase in sensitivity to the negative feedback effects of oestrogen on LH and FSH secretion and a failure of positive feedback, leading to a failure of oestrogen to induce the pre-ovulatory surge of LH [14]. We have now shown that breastfeeding women are hypersensitive to oestrogen: the use of transdermal patches to increase plasma concentrations of oestradiol to early follicular phase levels results in a rapid inhibition of further pulsatile release of LH, attributable to an inhibition of GnRH release from the hypothalamus [15]. This could be crucial in our understanding of how suckling suppresses fertility, although the mechanisms are unknown. The increased sensitivity to oestrogen must be induced by suckling, because in breastfeeding women who wean their babies, there is an early return to the normal feedback sensitivity to oestrogen. The implications are that when the levels of FSH are sufficient to initiate and maintain the growth of large follicles, the slow pulse frequency of LH caused by the suckling stimulus is only sufficient to allow these follicles to release small amounts of oestradiol. However, the increase in sensitivity of the GnRH pulse generator to oestradiol means that the small amount of oestradiol released from the follicle will be sufficient to switch off further GnRH/LH release, and the follicle will stop making oestradiol. Thus, no pre-ovulatory LH surge will be generated, and ovulation will not occur. If suckling was rapidly cut down around this time, then the increased sensitivity of the GnRH pulse generator would disappear, a pre-ovulatory LH surge could be induced, and ovulation and pregnancy could occur without any major warning during lactational amenorrhoea. This is rare but does occur [6].

 

Prolactin

Plasma concentrations of prolactin decline during lactation, even though suckling is maintained. The amount of prolactin released during suckling declines with time, but each suckling episode is associated with an increase in prolactin, even though this may be small. The amount of prolactin released during the afternoon appears to be greater than in the morning, and this has recently being confirmed by 24-hour profiles of prolactin release [11, 16]. It is quite clear that early in breastfeeding, by four weeks post-partum, the normal increase in prolactin associated with sleep that occurs during the normal menstrual cycle resumes, and superimposed upon this is the prolactin response to suckling. The amount of prolactin released during suckling at night appears to be greater than that released during the day, but the pattern is very variable. By eight weeks, the amount of prolactin released over the 24hour period has declined, but every suckling episode still releases prolactin. The pattern of prolactin release is entirely dependent on suckling. In a woman feeding six to eight times a day, each suckling episode is normally associated with an increase in prolactin, followed by a decline almost down to baseline, provided the next suckling episode does not occur within two hours. If, however, suckling is very frequent, then prolactin levels do not decline between suckling episodes and high levels of prolactin are maintained. Only when suckling is stopped (for instance, during sleep) does the prolactin concentration decline, but as soon as suckling recurs at a high frequency, prolactin levels increase and are maintained high. The release of prolactin in response to suckling does not appear to be related to opiates, because infusion of the opiate receptor blocker naloxone does not influence the amount of prolactin released in response to suckling. In contrast, dopamine clearly suppresses prolactin release, even during lactation when prolactin levels are high. The dopamine receptor blocker metaclopramide causes a huge release of prolactin, 10- to 70-fold higher than that induced by suckling, showing that during lactation, dopamine still maintains a tight control on prolactin release.

Whether the high plasma concentrations of prolactin maintained throughout lactation are part of the mechanism through which suckling suppresses GnRH/LH release is unclear. Dopamine is the principal regulator of prolactin secretion, acting directly on the pituitary lactotrophs to suppress prolactin release. It has been shown in a few species that prolactin can regulate its own secretion by directly increasing dopaminergic tone and dopamine release from the hypothalamus, and dopamine can suppress GnRH release [3]. Nevertheless, blocking dopamine receptors with the dopamine antagonist metaclopramide at 12 weeks post-partum in fully breastfeeding women did not affect LH or FSH secretion or the pituitary responsiveness to GnRH, even though the treatment caused a massive release of prolactin, indicating that it was indeed active [17]. Thus, it appears that dopamine itself does not directly control the pattern of pulsatile GnRH release.

The interaction between prolactin and GnRH release is clearly important, because patients with pathological hyperprolactinaemia often have amenorrhoea and a disrupted pattern of LH/GnRH release [13]. Thus, it is tempting to assume that the high levels of prolactin associated with lactation suppress LH and FSH release, presumably by affecting GnRH release. Previous studies have indicated a reasonably close association between the number of subjects with high levels of prolactin and the duration of lactational amenorrhoea [for example, 1820]. Indeed, one study showed that women who have an increased release of prolactin in response to suckling have a longer duration of amenorrhoca [21, 22]. Nevertheless, in our own studies over a number of years, we have been unable to show any close association between the amount of prolactin released, the pattern of prolactin release, and gonadotrophin secretion. Indeed, over a 24-hour period, pulsatile secretion of LH often coincides with times of maximum prolactin secretion during suckling, particularly when the prolactin response to suckling is highest at night [16, 17]. Equally, it is clear that the pattern of return of GnRH pulsatile release is not like that in puberty, when maximum pulsatile release of LH occurs during sleep. It is possible that the effect of prolactin is very subtle and relies on the plasma concentrations of prolactin remaining above an inhibitory threshold, which would suppress the normal pattern of GnRH release. It is not clear how this threshold could be assessed, but in previous studies it was observed that women had variable basal plasma concentrations of prolactin during normal menstrual cycles after weaning (Howie PW, McNeilly AS, unpublished observations, 1983). These prolactin levels could differ by up to fourfold. During lactational amenorrhoea in these women, the level of prolactin below which ovarian activity resumed related directly to the level of prolactin during the menstrual cycle in the individual woman. More work is required to determine whether prolactin plays a major role in suppressing GnRH output, but it is clear that the pattern of prolactin secretion is directly related to the pattern of suckling. How suckling influences GnRH and, hence, gonadotrophin secretion remains unclear [3].

  Conception during lactation

The foregoing discussion has made it clear that suckling is the key to the suppression of fertility. The variable return of ovarian activity is related to the variable pattern of suckling input and how fast the baby feeds. It is known that conception rates in women who are still breastfeeding but have resumed menstrual cycles are lower than those in women who have resumed menstruation after stopping contraception. The reason for this has now become clear. When ovulation occurs during lactation, it is often associated with reduced or inadequate corpus luteum function, resulting in reduced progesterone secretion [23-25]. The implication is that conception in a number of cycles can occur, but inadequate luteal function prevents continuation of the pregnancy. In some women menstruation does not resume before the return of full fertility. The first ovulation is normal, and pregnancy may occur without a preceding menstrual period. This, however, is rare and in our experience is related to a rapid reduction in suckling input. The cause of this inadequate corpus luteum function is still not absolutely clear. In bottle-feeding women, the first menstrual cycle is often associated with inadequate luteal function, and this has been related to a reduction in the amount of LH released during the pre-ovulatory LH surge [24]. A similar situation may occur during breastfeeding, and as luteal function improves during subsequent ovulations, the amount of LH released during the pre-ovulatory surge also increases [6].

 

Summary

Suckling interferes with GnRH secretion early in lactation by disrupting the pattern of GnRH release, so that it does not occur at a constant rate of once every 60 to 90 minutes, the normal pattern seen during the follicular phase of the cycle. FSH levels are high, so follicles can develop, but oestrogen secretion is compromised by this inadequate LH input. As suckling declines, the pattern of GnRH release becomes more constant, and this relates to the increase in oestrogen secretion seen during the later part of lactation. Nevertheless, when this follicle discharges an LH surge to induce ovulation, the following luteal function may not be normal. This may be related to a decrease in the amount of GnRH released during the pre-ovulatory LH surge and the altered sensitivity to positive feedback caused by oestrogen. Only when weaning is almost complete does one normally see the resumption of normal ovarian activity in ovulatory cycles.

 

Conclusion

Suckling is the interaction between the baby and the mother, and this interaction is crucial to the suppression of fertility. The suppression of fertility is associated not with a complete suppression, but with a disrupted pattern, of GnRH pulsatile secretion. Whether prolactin is involved remains unresolved. Although the exact mechanisms by which breastfeeding suppresses fertility are not known, it is clear that suckling activity is the major controller of the duration of infertility.

 

Acknowledgements

It is a pleasure to acknowledge my colleagues Peter Illingworth, Peter Howie, Anna Glasier, and Clem Tay for all their help during these studies.

 

References

1. Howie PW, McNeilly AS. Effect of breastfeeding patterns on human birth intervals. I Reprod Fertil 1982; 65:545-57.

2. McNeilly AS. Lactational amenorrhea. Endocrinology and metabolism clinics of North America. Neuroendocrinology II. Philadelphia, Pa, USA: WB Saunders, 1993.

3. McNeilly AS. Suckling and the control of gonadotrophin secretion. In: Knobile E, Neill J. eds. The physiology of reproduction. New York: Raven Press, 1994: 1179-1212.

4. Diaz SP, Miranda P. Brandeis A, Cardenas H. Croxatto HB. A study on the feasibility of suppressing ovarian activity following the end of postpartum amenorrhea by increasing the frequency of suckling. Clin Endocrinol 1988;28:525-35.

5. Glasier AF, McNeilly AS. Physiology of lactation. Bailliere's clinics in endocrinology and metabolism. Endocrinology of pregnancy. London: Balliere Tindall, 1990.

6. McNeilly AS, Glasier AF, Howie PW, Houston MJ,Cook A, Boyle H. Fertility after childbirth: pregnancy associated with breastfeeding. Clin Endocrinol 1983; 19:167-74.

7. Gray RH, Campbell OM, Apelo R. Elsami SS, Zacur H. Ramos RM, Gehret JC, Labbok MH. Risk of ovulation during lactation. Lancet 1990;335:25-9.

8. Glasier A, McNeilly AS, Baird DT. Induction of ovarian activity by pulsatile infusion of LHRH in women with lactational amenorrhea. Clin Endocrinol 1986;24: 243-52.

9. Flynn A, Docker M, Brown JB, Kennedy Kl. Ultrasonographic patterns of ovarian activity during breastfeeding. Am J Obstet Gynecol 1991;165:2027-31.

10. Glasier AF, McNeilly AS, Howie PW. Pulsatile secretion of LH in relation to the resumption of ovarian activity postpartum. Clin Endocrinol 1984;20:415-26.

11. Tay CCK, Glasier AF, McNeilly AS. The twenty-four hour pattern of pulsatile luteinizing hormone, follicle stimulating hormone, and prolactin release during the first eight weeks of lactational amenorrhea in breastfeeding women. Hum Reprod 1992;7:951-8.

12. Illingworth PJ, McNeilly AS. Estrogens and progestogens in the postpartum period. In: Fraser IS, Jansen RPS, Lobo R. Whitehead M, eds. Guidelines to estrogens and progestogens in clinical practice. Edinburgh: ChurchillLivingstone, 1996 (in press).

13. Tay CCK, Glasier AF, Illingworth PJ, Baird, DT. Abnormal twenty-four hour pattern of pulsatile luteinizing hormone secretion and the response to naloxone in women with hyperprolactinemic amenorrhea. Clin Endocrinol 1993;39:599606.

14. Baird DT, McNeilly AS, Sawers RS, McNeilly AS. Failure of estrogen-induced discharge of luteinizing hormone in lactating women. J Clin Endocrinol Metab 1979;49:500-6.

15. Illingworth PJ, McNeilly AS, Seaton JEV, McKinlay C, ReidThomas V. Hypothalamic sensitivity to negative feedback of estrogen during breastfeeding. Hum Reprod 1995;10:1671-7.

16. Tay CK, Glasier AF, McNeilly AS. The 24 h pattern of prolactin secretion throughout lactation in women. Hum Reprod 1996 (in press).

17. Tay CCK, Glasier AF, McNeilly AS. Effect of antagonists of dopamine and opiates on the basal and GnRH-induced secretion of luteinizing hormone, follicle stimulating hormone and prolactin during lactational amenorrhea in breastfeeding women. Hum Reprod 1993;8:532-9.

18. Delvoye P. Badawi M, Demaegd M, Robyn C. Serum prolactin, gonadotrophins, and estradiol in menstruating and amenorrheic women during two years of lactation. Am J Obstet Gynecol 1978;130:635-40.

19. Duchen MR, McNeilly S. Hyperprolactinemia and long-term lactational amenorrhea. Clin Endocrinol 1980;12: 621 -7.

20. Fink AK, Fink G. Wilson H. Bennie J. Carroll S. Dick H. Lactation, nutrition, and fertility and the secretion of prolactin and gonadotrophins in Mopan Mayan women. J Biosoc Sci 1992;24:35-52.

21. Diaz S. Cardenas H. Schiappacasse V, Brandeis A, Croxatto HB. Circadian variation of basal plasma prolactin, prolactin response to suckling, and length of amenorrhoea in nursing women. J Clin Endocrinol Metab 1989;68:946-55.

22. Diaz S. Cardenas H. Brandeis A, Miranda P. Schiappacasse V, Salvatierra AM, Herreros CM, Seron-Ferre M, Croxatto HB. Early differences in the endocrine profile of long and short lactational amenorrhea. J Clin Endocrinol Metab 1991;72:196201.

23. McNeilly AS, Howie PW, Houston MJ, Cook A, Boyle H. Fertility after childbirth: adequacy of postpartum luteal phases. Clin Endocrinol 1982;17:609-15.

24. Poindexter AN, Ritter MB, Besch PK. The recovery of normal plasma progesterone levels in the postpartum female. Fertil Steril 1983;39:494-8.

25. Howie PW, McNeilly AS, Houston MJ, Cook A, Boyle H. Fertility after childbirth: postpartum ovulation and menstruation in bottle- and breastfeeding mothers. Clin Endocrinol 1982;17:323-32.

Discussion of paper by McNeilly

 

Dr. McLaren

Thank you for a very clear exposition of a very complex subject. 1 was particularly interested to learn about that double-assurance system that is nature's way of suppressing fertility, emphasizing the importance of this mechanism for spacing births.

Dr. Pz

You mention that the key is suckling, but what is the mechanism? How could one reproduce that?

Dr. McNelily

We do not know how to mimic the effect of suckling. If you increase prolactin by drug treatments, that has some effect on LH pulse generation, perhaps by an effect on GnRH rather than by a direct effect of prolactin. The bottom line is still that lactational infertility is driven by a change in GnRH pulse output, and we don't know how to regulate that.

Professor Hanson

Would a mother of a premature baby who is pumping or extracting her milk be able to stimulate her nipples to the extent that she would be able to induce infertility?

Dr. McNelily

Induced lactators make milk, but no one has really looked properly at reproductive performance, so there is no published literature. There are anecdotes that suggest that there is an effect on the resumption of menstruation when they express milk by hand but not with breast pumps, so I do not think it is just emptying the breast. I think it is actually nipple stimulation.

Professor Howie

I don't think that the situation in the pre-term infant has been studied systematically as it has been with term babies. Because pre-term babies will not be suckling with the same regularity or strength, their suckling might not have the same effect as that produced by the full-term baby.

Dr. Garza

There are some very limited data showing that use of the breast pump does not result in the same prolactin surges as direct suckling, probably not only because of the lack of physical stimulation, but also because of the lack of a psychosomatic component. It may be that the neural pathways do not respond in the same way. In the normalterm infant, do you know if anyone has compared the effects of nutritive and non-nutritive suckling on maternal endocrinology? The pattern of suckling is so different that there may be reason to suspect that one or another is more effective in sustaining the hormonal changes that lead to amenorrhoea.

Dr. McNailly

The problem is that when you look at the world literature, nobody uses the same definition. Now that a single definition has been developed, it should be used to describe suckling. In Thailand, with Dr. Sodsai Tovanbutra, we counted the number of sucks per suckling episode to determine if it was related to prolactin release. There was no relationship at all. So the idea that prolactin is one of the monitors of the suckling stimulus and GnRH pulse generation doesn't work. There was one defect. We just counted the number of sucks. We did not have a recorder, so we could not work out the intersuck interval. The problem is that we do not really know how to monitor suckling activity.

Dr. Woolridge

The data on pump use and prolactin are ambiguous. Professor Howie, I think that your study is the only one that shows the complete absence of a prolactin response during the use of an electric breast pump, but there are at least four published studies that show a reasonable prolactin surge. We have just completed a study with women who have established milk production with an electric pump, and they have been doing repeated within-measures studies. On every occasion, 24 women had a prolactin surge every time they used an electric pump. Maybe one of the reasons why non-nutritive sucking is effective is that the endocrine system may be more sensitive to particular types of sucking, such as that associated with low milk release. We have a pump that operates at twice the normal rate, and we are anxious to look at the prolactin surge.

Dr. McNeilly

Is the pump a suction pump, or is it actually a proper milking pump?

Dr. Woolridge

We have just compared single and double pumping with and without one of the Silastic inserts that give it a more physiological style of action. We were unable to show any impact of the Silastic inserts on prolactin release.

Professor Hanson

The effectiveness of suckling is especially important in poor countries, where 20% to 30% of newborns may be of low birthweight. Is the spacing between pre-term, lowbirthweight children shorter than that between full-term children?

Dr. Prentice

We have to remember that many low-birthweight babies in the third world are actually term babies. They are small for dates, but they are not premature, so we should not get confused.

Dr. Pollitt

There are large and significant differences between the sucking patterns of pre-term and term babies on the bottle. I do not know about the breast. But almost any parameter that you can think of or identify in the term baby is going to be different from that of the pre-term baby. In other words, the amplitude, the frequency, the duration of the burst, the length of the period without sucking, and so forth are all different. What is particularly interesting in the pre-term baby is that there is continuous sucking. There are no bursts, but instead there are continuous, varied, small-amplitude sucks.

Dr. McNeilly

It is very difficult to know exactly what part of the suckling stimulus is important. We have seen women who suckled 25 times a day and women who suckled 5 times a day, each with a total suckling duration of 60 minutes per day. They have the same patterns of gonadotrophin secretion and ovarian function, so clearly the brain is very adaptable at reading a signal coming from the nipple. I would not be surprised if there was an interaction between the baby and the mother as well, helping to amplify this stimulus. In Chile, Dr. Diaz* increased the suckling frequency in breastfeeding women in an attempt to switch off ovarian activity after it had resumed. The attempt failed, because although the number of suckling episodes was increased, the babies reduced the duration of each feeding so that the overall apparent suckling input was the same and the increased number of episodes had no effect whatsoever. The problem is that the system is so adaptable. To say you need so much suckling to maintain infertility is very difficult. What we should try to do is to determine the minimal parameters for each particular society, parameters that we can actually measure. In Edinburgh we chose frequency and duration of each feeding to see if that would give a guide to maintaining infertility. It worked in our particular group of women.

Dr. Prentice

Could you bring us up to date on the thinking about the mother's nutritional status? Our supplementation studies in lactating women suggested that feeding the women more resulted in their ovarian activity returning earlier, and we put that down at the time to the lower prolactin levels. Do you think that it is sucking frequency only, or does the mother's nutritional status have some impact?

Dr. McNelily

If you look at situations involving acute weight loss or chronic weight loss, you actually have to lose a lot of weight to switch off ovarian activity. Andrew Loudon, John Milne, and I** compared red deer on a restricted diet and on a full diet. We showed that on a restricted diet, the rate of milk secretion was much lower, so the calves kept going back more often. The supplements in your study may have subtly altered the suckling activity, perhaps the strength of sucking at each episode, without a change in the number of suckling episodes.

Dr. Prentice

In the context of the meeting, what you appear to be saying then is that if a well-nourished mother has a high suckling frequency, she is likely to have just as long a period of fertility as an undernourished mother. The common perception is that for women in the third world, breastfeeding as a contraceptive is all right, but for women in developed countries, it's not a particularly good method of contraception.

Dr. Rasmussen

My question relates to night feeding. We were all very intrigued by your previous night-feeding findings. They seemed to justify feeding our babies at night. Your comments now seem to have wiped out that justification. Can you tell us more about what you now know that makes you think night feeding is not important?

Dr. McNeilly

Our early studies suggested that a woman who was breastfeeding at night was likely to remain amenorrheic longer. As we accumulated more data, it became apparent that it was not necessarily the night feeds that were important. It now seems that if women feed six times a day, it can be between eight in the morning and six at night, and that will maintain the infertility.

Dr. Rasmussen

So it is just the number of times a day or the total minutes of suckling, not when in the 24-hour period it occurs. Earlier, you hypothesized that it was interfering with the LH surge at ovulation.

Dr. McNeilly

Yes, that's right, because at that time (10 years ago), that was our state of knowledge. But I think now, having accumulated more information, that the night feeding is not necessarily as important as we assumed. It is the suckling input during the 24-hour period that matters. In Keith Gordon's*** studies in monkeys, which have patterns similar to the human in resuming ovarian activity (pulsatile LH secretion and so forth), restricting suckling to either daytime or night-time has made no difference to gonadotrophin secretion, provided the suckling frequency remains the same. Furthermore, the anecdotal reports that we have from women who are working during the day and feeding only at night suggest that infertility is maintained, provided suckling is continued.

Dr. Vald/strong>

If a working mother breastfed more frequently at night but kept the same number of daily feedings, would that be enough to maintain amenorrhoea?

Dr. McNeilly

I think it probably would, but I would not like to be held responsible for that practice being adopted and then failing. It requires specific investigation.

Demographic effects of breastfeeding: Fertility, mortality, and population growth

Jane Menken and Randall Kuhn

 

Abstract

This article reviews the demographic effects of breastfeeding on fertility and child survival and, ultimately, on population growth. Extended breastfeeding both reduces fertility by prolonging birth intervals and increases child survival through improved nutrition, especially where adequate substitutes are not available. The results presented show, however, that although breastfeeding is a major determinant of fertility in the absence of other means of fertility control, prolonged breastfeeding alone cannot reduce fertility to levels consonant with slow or zero population growth. The benefits, at least for the first year of life, demonstrate the need for policies that promote breastfeeding and encourage compatibility between breastfeeding and other aspects of women's fives. In particular, policies are needed that permit women to breastfeed their children while, at the same time, improving their socio-economic circumstances through participation in the labour force.

 

Introduction

Breastfeeding is known to reduce fertility and increase child survival. It affects fertility by prolonging the interval between births. It increases child survival both directly, through the provision of beneficial nutrition to the child, and indirectly, through improved child spacing. In this article we review evidence that leads to these conclusions and consider two questions that relate the findings on breastfeeding to population growth:

  • Can long breastfeeding patterns reduce fertility to levels compatible with slow population growth under conditions of low mortality?
  • Can shorter breastfeeding patterns, which lead to both higher fertility and higher infant mortality, also lead to higher population growth rates? This outcome would require the fertility-enhancing effect of early weaning to overwhelm its negative effect on child survival.

We first consider how low fertility must be, when combined with the low mortality even the poorest countries have achieved in recent years, to lead, ultimately, to either very slow or no population growth. We next offer illustrative data on recent levels of fertility and mortality around the world. This section is followed by a discussion of the factors that determine levels of fertility, including breastfeeding, and then by an examination of the evidence relating breastfeeding to infant and child survival. We end with a set of policy recommendations.

 

Population growth

During the 1960s and 1970s, there were many assessments of the world population situation. Some were by alarmists who wrote of the "population explosion" and credited population growth with responsibility for many, if not all, of the afflictions of the developing world. Others, taking a more judicious view, still concluded that rapid growth, on balance, had consequences sufficiently detrimental to prospects for improving conditions in much of the world to warrant efforts to slow the increase in population by reducing fertility. Indeed, this has been the primary rationale for family planning programmes.

In 1974 the United Nations sponsored an International Conference on Population in Bucharest, Romania. Although some countries urged the adoption of policies aimed at slowing growth, primarily through family planning, out of that conference instead came the dictum that "development is the best contraceptive." However, this dictum was not followed by even its most fervent supporters in the developing world. Instead, developing countries increasingly turned to population policy and family planning programmes aimed at reducing fertility.

One of the major challenges to the received wisdom on population questions came in 1981 with the publication of Julian Simon's book The Ultimate Resource [1]. Simon, while not opposed to the principle that individuals should be able to control the number of children they have if they so choose, contested the view that rapid growth had deleterious effects. He argued that population growth is a significant and effective long-term stimulus to economic development, exerting its influence by, among other means, increasing the tempo of innovation. His views profoundly influenced the US Government's stance at the 1984 United Nations International Conference on Population [2].

Ten years later, the 1994 United Nations Conference on Population and Development was held in Cairo. The US position, like those of many other countries, had changed, with concern for human rights, the status of women, maternal and child health, and the environment being discussed in preparatory meetings around the world as well as at the conference itself.

Any discussion of breastfeeding and population must take place against the backdrop of these concerns. It must also take into account the fact that population growth, continued indefinitely into the future, will ultimately outstrip space on earth. There have been any number of demographers who have amused themselves (if no one else) with calculations of how long it would take for the population to reach numbers so large that each person had only one square foot of earth to occupy, or until the numbers represented mass equal to that of the earth, and so on. At an annual growth rate of 2%, it takes about 35 years for a population to double, at 3% it takes only 23 years, and at 4% it takes about 17 years. (The doubling time is about equal to 69/annual growth rate.) The non-trivial point of these calculations is that ultimately birth and death rates must again come into balance. In the past they were balanced at high levels of both fertility and mortality. The issue is whether they can be brought into balance for the world, as well as the currently developed nations, at low levels of mortality, which require correspondingly low levels of fertility.

 

Some mathematical relations

If fertility and mortality rates are constant over time, the mathematics of population growth lead to some important relationships that are useful in this discussion [3, 4]. The growth rate r is related to the average number of children a woman bears and to the survival of those children so they can contribute progeny to the subsequent generation. The net reproduction rate (NRR) is a measure that summarizes both fertility and child survival. It is defined as the average number of daughters a girl born today will contribute to the next generation. If birth and death rates are unchanging over time, results from mathematical demography show that r is related to NRR through the average age at which women bear their children. Thus, if that average age is 28 (as is characteristic of a wide range of populations) and r is expressed as a proportion (for example, if growth is 2% annually, then r = 0.02), then a powerful result of the mathematics of population growth [3, 4] is that

In (NRR) ~ 28r

so that

NRR ~ e28r.

NRR itself can be estimated from two other measures related to fertility and survival. The total fertility rate (TFR) is the average number of children borne by a woman who survives her entire reproductive span, in other words, to age 50. The number of daughters is about equal to TFR x .488, where .488 is roughly the fraction of children who are girls. The proportion of girls born today who may contribute children to the next generation can be approximated by the proportion surviving to the average age of child-bearing, for which we are using p(28). With these assumptions,

NRR ~ TFR ´ .488 ´ p(28).

Using this approximation, table 1 shows the NRR needed for growth rates ranging from 0% to 4% per year and, for TFR ranging from two to nine children, the p(28) that would lead to these growth rates. For example, an annual growth rate of 1% can be achieved with TFRs from three to nine, but the corresponding survival probability that would maintain this growth goes down sharply as the average number of children increases. Table 2 shows the p(28) values corresponding to life expectancies at birth that range from 20 to 80 years, taken from the West Model Life tables developed by Coale and Demeny [5]. The values that correspond to life expectancies of 50 years or more are in bold type in table 1. They clearly indicate that TFRs of five or more are associated with growth rates of at least 2.5% per year and doubling times of less than 28 years.

Continue

Discussion of paper by Menken and Kuhn

 

Unidentified speaker

If women in Bangladesh were to use contraception while they were breastfeeding, what would be the result?

Dr. Menken

I think the answer is that there is no reason to overlap other means of fertility control with breastfeeding in the first six months of life.

Unidentified speaker

But what if breastfeeding were to be replaced by a contraceptive device?

Dr. Menken

If you look at Hong Kong as a developing country, you find limited breastfeeding and massive use of contraception, leading to very low fertility (see table 5). If you look at the developed countries in the same table, it was assumed women breastfed for three months, but for most of those countries, breastfeeding was actually very limited. The damping of fertility came about through contraceptive use, so that if contraception is effective enough, it has a far more powerful effect overall than breastfeeding. Lactational amenorrhoea only prolongs birth intervals by a maximum of, say, 18 months. Long-term contraception can prolong them very much more, so that breastfeeding is not a competitor in the statistical race.

Unidentified speaker

No, no. You have not answered my question. You shifted to Hong Kong. I am asking you about Bangladesh. If you replaced breastfeeding by contraception in the Bangladesh conditions, what would happen?

Dr. Menken

In Bangladesh fertility has dropped radically as a result of family planning. There's been a long-term family planning programme that has offered contraception within people's homes in a society in which purdah is the common practice, so that women don't move freely out of their homes. The total fertility rate in Bangladesh is now under five, probably closer to four, and that decline has been achieved through the adoption of contraception. There has been some drop in breastfeeding, but it's mostly contraceptive use in combination with breastfeeding. Now, if you were to substitute poor contraception for the very good lactation practices (in terms of fertility-reducing effects), you might have a different effect. Suppose, for instance, you took women just post-partum and urged them to use DepoProvera and gave them the injection. If they stopped lactating and after three months decided they didn't like Depo-Provera, what would happen? Fertility would go up. But that has not happened in most societies.

What one wants is to promote a system in which women can lactate, but not necessarily forever, if that means they can't work. One wants to promote a society in which women can combine these various roles. We need to try to make it feasible to breastfeed enough to benefit the child and to have fertility-controlling effects.

Dr. Colombo

Two small questions. One is very technical about Dr. Bongaarts' list. He speaks of the biological probability that conception will follow a single act of intercourse. What can he mean by that? A single act of intercourse has a probability that changes along the menstrual cycle. It is zero for most times of the cycle. Even in the fertility window, it is not a rectangular distribution. The second question is this. In aggregating studies of historical demography, it has been found that there was a seasonal pattern in the birth rate. If we now compare the seasonal pattern north of the equator, it is opposite to that south of the equator. Is that biological or is it social?

Dr. Menken

Those are very good questions. I have been intrigued by the profound seasonality in fertility in Bangladesh for the last 20 years. Close to 50% of births occur in four months of the year, and you see this year after year. Some people said it was nutrition, and we did everything up, down, and sideways that we could do as demographers and yet found very little effect of nutrition. It turns out there is profound seasonality in the introduction of supplementation, that is, the move from full to partial breastfeeding. That appears to be related to the needs of the agricultural calendar and the jobs that women do. This move to supplementation appears to determine a great deal of the seasonality. We are about to do a study in Bangladesh, trying to measure ovulation to see whether there are differences in different seasons of the year, or whether differences in the intensity of breastfeeding explain part of the seasonality.

Dr. Colombo

So it's not a difference in the frequency of intercourse?

Dr. Menken

My hypothesis at the moment is that there are real differences in frequency of intercourse in different parts of the year. It would seem to me that seasonality is almost entirely socially determined, so it is not surprising that seasonality is different in different parts of the world, especially north and south of the equator.

Dr. McLaren

Could you respond to Dr. Colombo's other question about what Bongaarts meant about the chance of pregnancy?

Dr. Menken

If one figure is given, it is usually an average taken over the course of the month, so that if you assume there was a random chance of intercourse on any day, that average probably would apply. Bongaarts does include in his discussions of fecundability models the variation over the menstrual cycle in the probability that conception follows a single act of intercourse.

Unidentified speaker

I have a comment on the statement that breastfeeding has no effect on mortality after 12 months of age. I am not sure the literature is very clear-cut on that. I know at least two or three good studies that have shown an effect. The literature on morbidity certainly shows that the incidence of the number of infectious diseases is higher among nonbreastfed children, even after one year of age. The protective effect certainly goes down with age, but I think it's hard to draw a line, particularly in societies where the alternative to breastfeeding, even in the second year of life, will certainly expose the child to a high level of infection.

Dr. Menken

The data that I was referring to came from several countries in Latin America. These are reports rather than prospective studies. There is no question that the benefits of breastfeeding are greatest for the poorest. Those who have the least access to other alternatives protect their children the most through their breastfeeding practices. In fairly careful searches of the literature, the large population samples I found have not shown any significant effect after the first year. It is an important area of research, and I'd like to see the references you have. I should add, though, that even if mortality consequences exist, by that age overall mortality rates have gone down enough that even if the relative risk is high, it's not going to have a large effect on the overall mortality.

Unidentified speaker

In support of what you've just said, we followed a very large cohort of children prospectively in Pakistan, and it turned out that 90% of the infant mortality occurred before the age of six months; 34% occurred in the first week of life. Mortality is, indeed, very early.

Dr. McLaren

Thank you again. Our last paper today is by Dr. Kathleen Rasmussen. We've heard a lot so far about the benefits of breastfeeding for the baby, the effects of breastfeeding on fertility, but Dr. Rasmussen is going to tell us about the effects of breastfeeding on maternal health and well-being.

Effects of breastfeeding on maternal health and well-being

Kathleen M. Rasmussen and Michelle K. McGuire

 

Abstract

Lactation occurs as part of a reproductive and may have different effects on maternal nutritional status, depending on its duration and intensity. Thus, its effect on maternal health will differ with cultural setting and level of development. Lactation helps women to maintain a healthy body weight. Among well-nour-shed women, it may help to prevent obesity. Among poorly pour/shed women, breastfeeding also leads to weight loss, but with adequate birth spacing brought about by lactational anovulation, maternal depletion can be avoided. Lactation is probably not responsible for osteoporosis. Current evidence suggests that breastfeeding helps to prevent pre-menopausal breast cancer and is not associated with post-menopausal disease Furthermore, breastfeeding may also help reduce ovarian cancer. Positive effects of breastfeeding occur at all levels of development and are most likely when biological, political, and sociocultural conditions interact to support its initiation and continuation.

 

Introduction

The effects of lactation on maternal health and wellbeing are many and varied. For example, lactation helps women maintain a healthy body weight. This is perhaps the most obvious biological effect of breastfeeding on women's health and is one that will be considered in detail. In addition, the hormonal changes characteristic of lactation influence maternal behaviour in ways that are supportive of both breastfeeding itself and positive mothering behaviours in general [1-4]. There is even evidence from animal studies that there are factors in milk that influence the behaviour of the nursing young [5, 6].

 

Lactation occurs within a reproductive cycle

Lactation occurs as part of the reproductive cycle, and it may have different effects on maternal nutritional status, depending on its duration and intensity. Each time a woman reproduces, she goes through the cycle diagrammed in figure 1.

Each cycle may have very different characteristics. For example, the child could die in the neonatal period, and the cycle would then be very short. Alternatively, the woman might become pregnant while still breastfeeding; in this case there would be no non-pregnant, non-lactating interval. The woman and her husband could adopt some effective means of birth spacing and thus prolong the non-pregnant, nonlactating interval substantially.

The biological effect of breastfeeding on the nutritional status of the mother needs to be evaluated in the context of the whole reproductive cycle [7]. This is because some portions of the reproductive cycle deplete the mother, and some periods allow the mother to gain. Breastfeeding is commonly thought of as a time of depletion, but this is probably true only of the period of exclusive breastfeeding. Even this is not so in severely undernourished experimental rats, which actually gain fat while their nursing pups are starving [8].

In contrast, the period of partial breastfeeding may be one of repletion, and the longer it is, the more repletion may be possible [9]. Inasmuch as breastfeeding itself delays ovulation and therefore conception, breastfeeding may be associated with first depletion and then repletion of the mother. It is expected that the non-pregnant, non-lactating interval will serve as an opportunity for repletion. This assumption requires that the woman's food intake remain the same after the caloric demand of lactation has been removed and also that her workload does not increase above that which she experienced while nursing her infant. These assumptions may or may not be true and must be evaluated in a particular cultural or individual context.



FIG. 1. Diagram of the reproductive cycle showing birth interval and the periods of maternal depletion and repletion. *Non-pregnant, non-lactating

It should be clear, therefore, that the effects of breastfeeding on maternal health will be different in different cultural contexts or at different levels of development. The effects of breastfeeding on maternal health will also depend on the usual practices for exclusive or partial breastfeeding and on birth spacing. The effects of reproduction on a woman's health are cumulative over her lifetime, but because of the possibility that reproduction will result in net positive or net negative effects, the effects are not a simple multiple of the number of children borne. A more sophisticated analytical approach than this is needed if we are to understand the cumulative effects of reproduction, including lactation, on maternal health [7].

 

Lactation affects maternal health and well-being

Change In body weight

Women gain weight and body fat during pregnancy and tend to lose it during lactation [10]. The amount of weight gained during pregnancy is higher with better living circumstances [11]. The amount of weight retained after delivery shows this same discrepancy between poor and rich countries. In the United States, the rate of weight loss post-partum is often higher among lactating women than among non-lactating women (assuming that the women are not consciously dieting) [12]. The rate of weight loss is not constant [10]. It is greatest in the first few months postpartum and slows as solid foods are introduced into the infant's diet. Women may gain weight during partial breastfeeding and are especially likely to do so after weaning their infants.

Prevention of obesity

Among well-nourished women, lactation may help to prevent the weight and fat retention often associated with child-bearing. In fact, the effect of breastfeeding on helping a well-nourished woman return to a healthy body weight after delivery is fairly dependable [10]. Weight retention at the end of a reproductive cycle is influenced by the intensity and duration of breastfeeding. The data of lin and Rer [13] from Swedish women illustrate this point. They developed a "lactation score" that combined frequency and duration of breastfeeding. Among their subjects, weight loss from 2.5 to 6 months postpartum was greater as the intensity of breastfeeding increased. All women, however, lost weight in the subsequent 6 months, whether they breastfed or not, and the total weight loss after 12 months was the same among those who had been intensive breastfeeders as it was among those who had not. Unfortunately, in this study the investigators did not measure the weight change that occurred during the first 2.5 months post-partum, the time of greatest weight loss among breastfeeding women.

The data of Forsum and her co-workers [14] also provide information about the change in body fat that occurs during pregnancy and lactation among well-nourished women. They studied 22 Swedish women before and during pregnancy and during the first six months of lactation. Although by six months post-panum, women in this population of enthusiastic breastfeeders had lost nearly all of the weight and several kilograms of the fat that they had gained during pregnancy, they still retained almost 4 kg of the fat that they had gained. This fat was available to support continued breastfeeding in the second half of infancy and beyond. Unfortunately, no comparable data are available for non-lactating women.

Maternal depletion

In contrast, women living under poor circumstances are concerned about becoming too thin as a result of childbearing.* Data from more than 1,000 women in the Cebu Longitudinal Health Study in the Philippines [15] show that the direction of weight change in the post-partum period is associated with maternal weight immediately after delivery. Those who were the heaviest at this time gained weight during lactation, but women in other groups lost weight. Longer birth spacing might allow women in the other groups to return to their prepregnant weight before conceiving again.

A particularly relevant recent study [16] from Bangladesh goes even further. It accounts for initial maternal weight, duration of breastfeeding, and season in examining the effect of breastfeeding on maternal weight change. Weight loss was higher in lactating than in nonlactating women, and lower in women with low initial weight than in those with high initial weight. In this study, the rate of weight loss was highest 5 to 9 months post-partum and was near zero at 16 months post-partum. After this time, women gained weight. Nevertheless, season and time postpartum interacted so that women who reached the time of most intensive breastfeeding at a time of low food supply lost the most weight. Each additional birth was associated with a 280 g decrease in the mother's weight at conception. Furthermore, interpregnancy intervals of less than 18 months were far more important: each of these was associated with an 800-g decrease in the mother's weight at conception. The authors concluded that "women in Bangladesh have the potential to regain the weight they lose during the first 15 months or so of lactation despite a high and varying level of nutritional stress," but that this depends on adequate spacing between pregnancies to permit a woman to replace her reserves.

In summary, like their better-nourished counterparts, women living under poor circumstances lose weight during lactation. Furthermore, their weight loss is magnified by seasonal changes in their environment. Nonetheless, with adequate birth spacing brought about by lactational anovulation, women living under poor circumstances should be able to maintain a healthy body weight from one reproductive cycle to the next.

Changes in incidence of chronic diseases

Osteoporosis

As women live longer, osteoporosis is becoming a much more serious problem [17, 18]. It has been postulated that lactation might contribute to the development of osteoporosis because so much calcium is transferred from the mother to the infant in the milk during breastfeeding. Although the rate of calcium transfer from mother to infant is actually higher during the third trimester of pregnancy than it is during lactation [19, 20], the total amount of calcium transferred may be greater during lactation than during pregnancy if lactation is long enough [21]. However, many features of calcium metabolism change during lactation to compensate for the high rate of transfer of calcium from the mother to the infant [22]. For example, the rate of bone resorption increases [21], and renal calcium conservation also increases [20, 23].

Research presented or published recently shows clearly that bone mineralization returns to normal after lactation among well-nourished women with ample calcium intakes [21, 24]. The shorter the period of lactation, the sooner bone mineralization returns to normal. Nevertheless, if birth spacing is adequate, bone mineral densities will have returned to pre-pregnant values before the next conception. In a recently completed year-long trial, the milk calcium output of calcium-supplemented Gambian women with habitually low calcium intakes did not increase, and neither did bone mineral content [25]. Bone mineral content, however, did not decline during the first year of lactation, as has been previously observed among women with higher calcium intakes.

The effect of breastfeeding on hip fracture, one of the most debilitating consequences of osteoporosis, has not been studied often, but the three studies that have investigated this association among women living under good circumstances have come to the same conclusion [26]. In all of them, there was a reduction in the incidence of hip fracture with increased duration of lactation.

Thus, it appears that lactation per se is probably not responsible for osteoporosis or its consequences. A woman's body can adapt to varying calcium intakes and lengths of lactation. Thus, this concern, although intriguing at one time, can now be eliminated.

Breast cancer

It has long been known that the incidence of breast cancer is associated with a woman's reproductive history. In particular, breast cancer is higher among women with late onset of menstrual periods, late age at first birth, and few total births [27]. Evidence of an association between lactation and breast cancer has been inconsistent [27, 28].

The most recent work [29], using a large sample of women from a multicentre case-control study, showed that breastfeeding reduces the risk of pre-menopausal breast cancer in a dose-dependent fashion (the longer the total period of breastfeeding, the lower the risk of breast cancer). In the same study, there was no association of lactation with post-menopausal breast cancer. Many researchers think that breast cancer in these two periods has different origins, so this lack of consistency is perhaps not surprising. In summary, the current evidence points to a beneficial effect of breastfeeding in preventing premenopausal breast cancer, and no association of breastfeeding with the post-menopausal disease.

Ovarian cancer

There are also conflicting findings about a possible association of breastfeeding with ovarian cancer. In a recent multicentre collaborative study, there was a 20% reduction in the incidence of ovarian cancer with lactation [30], but this was not statistically significant. Nevertheless, the reduction in cancer incidence with increasing time spent pregnant was even greater. The authors speculate that this is because pregnancy is even more effective than lactation in suppressing ovulation.

Overall, we can say that lactation is not responsible for increasing the incidence of some chronic diseases in women and, in the case of pre-menopausal breast cancer, probably has a role in preventing this condition.

 

The effects of lactation vary with the circumstances of the woman's life

For women living in traditional societies (fig. 2), investigators have historically been concerned about undernutrition. In this situation, breastfeeding has both direct effects on maternal health and wellbeing and indirect effects that are mediated through fewer reproductive cycles. Some of the effects on the mother benefit the infant, in addition to the nutritional value inherent in the direct transfer of human milk. The infant also benefits from breastfeeding indirectly from the lengthening of the birth interval.

In transitional societies there is now concern about overnutrition in addition to concern about the undernutrition that skill remains. This creates a more complex picture than the last, because chronic diseases, particularly those associated with obesity, are becoming a problem (fig. 3).

In industrialized societies the concern is primarily about overoutrition and the "diseases of affluence." In this situation few women use breastfeeding for birth spacing, so the indirect effects of breastfeeding on maternal and child health via prolonged birth spacing are eliminated, but the direct effects remain and are important (fig. 4).



FIG. 2. Diagram showing how breastfeeding affects maternal and child health in a traditional society. Note that the effects of breastfeeding are both direct and indirect, via its effect on reducing the number of reproductive cycles



FIG. 3. Diagram showing how breastfeeding affects maternal and child health in a society in transition. Note that the effects of breastfeeding are both direct and indirect, via its effect on reducing the number of reproductive cycles



FIG. 4. Diagram showing how breastfeeding affects maternal and child health in an industrialized society



FIG. 5. Factors required to realize the benefits of breastfeeding for maternal and child health. Note that the appropriate biological, sociocultural, and political factors must all be present for the maximal positive effect

 

Conclusions and implications

This article has focused on the biological ways in which breastfeeding affects maternal health and well-being. To achieve these benefits, women must initiate and continue breastfeeding. As described earlier, for this to occur, the biological, political, and sociocultural environments must interact in a way that is supportive of breastfeeding (the shaded area of fig. 5).

As the figures illustrate, this interaction occurs in different ways under different living conditions. Appropriate interventions to promote and sustain breastfeeding will, therefore, differ with the circumstances. For example, in societies in which breastfeeding is the usual practice and mother and infant can be together all day, the usual activities to promote initiation of breastfeeding can work well. This may involve, for instance, supporting the Baby-Friendly Hospital Initiative. Supporting an adequate duration of breastfeeding and the timely introduction of complementary foods is more difficult but is, nonetheless, important. This may involve developing policies that are not now in place, especially for women who work in the informal employment sector. The principal future threat is urbanization and disruption of the culture in which breastfeeding is the norm.

In societies in which breastfeeding is not the usual practice, there are other concerns. In these societies, just getting women to consider breastfeeding is a problem, because there are strong societal pressures against starting to breastfeed. Therefore, supporting women to initiate breastfeeding in a relatively hostile environment is necessary, and this means more than just following the principles that are part of the Baby-Friendly Hospital Initiative. There are also pressures against women continuing to breastfeed. This is because women have taken on new roles in society that separate them from their infants and are living in situations in which their infants cannot be cared for by relatives. Thus, better maternity leave policies need to be developed, and child care near the mother's place of employment also needs to be provided.

In summary, lactation influences maternal and infant health in a number of positive ways. These vary with the circumstances in which women live, but positive effects are present at all levels of development. These positive effects of breastfeeding are most likely to occur when the biological, political, and sociocultural environments interact in ways that support both the initiation and the continuation of breastfeeding.

 

Acknowledgements

The thoughtful comments of Drs. Jean-Pierre Habicht, Cutberto Garza, and Grace Marquis are greatly appreciated.

 

References

1. Pederson CA, Caldwell JD, Jirikowski GF, Insel TR. Oxytocin in maternal, sexual and social behaviors. New York: New York Academy of Sciences, 1992.

2. Dawood MY, Khan-Dawood FS, Wahi RS, Fuchs F. Oxytocin release and plasma anterior pituitary and gonadal hormones in women during lactation. J Clin Endocrinol Metab 1981;52:678-83.

3. Drewett RF, Bowen-Jones A, Dogterom J. Oxytocin levels during breastfeeding in established lactation. Horm Behav 1982;16:245-8.

4. McNeilly AS, Robinson IC, Houston MJ, Howie PW. Release of Oxytocin and prolactin in response to suckling. BMJ 1983;286:257-9.

5. Smotherman WP, Robinson SR. Milk as the proximal mechanism for behavioral change in the newborn. Acta Paediatr 1994(suppl 387):64-70.

6. Blass EM. Behavioral and physiological consequences of suckling in rat and human newborns. Acta Paediatr 1994(suppl 397):71-6.

7. Winkvist A, Rasmussen KM, Habicht J-P. A new definition of maternal depletion syndrome. Am J Pub Health 1992;82:6914.

8. Rasmussen KM, Fischbeck KL. Effect of repeated reproductive cycles on pregnancy outcome in ad libitumfed and chronically food-restricted rats. J Nutr 1987; 117:1959-66.

9. Winkvist A, Jali F. Rasmussen KM, Habicht J-P. Maternal energy depletion is buffered among malnourished women in Punjab, Pakistan. J Nutr 1994;124: 2376-85.

10. Institute of Medicine (Subcommittee on Nutrition During Lactation, Committee on Nutritional Status During Pregnancy and Lactation, Food and Nutrition Board). Nutrition during lactation. Washington, DC: National Academy Press, 1991.

11. Hytten FE, Leitch 1. The physiology of human pregnancy. 2nd ed. Oxford: Blackwell Scientific Publications, 1971:440-60.

12. Dewey KG, Heinig MJ, Nommsen LA. Maternal weight loss patterns during prolonged lactation. Am J Clin Nutr 1993,58:162-6.

13. lin A, Rer S. Maternal body weight development after pregnancy. Int J Obesity 1990;14:159-73.

14. Forsum E, Sadurskis A, Wager J. Resting metabolic rate and body composition of healthy Swedish women during pregnancy. Am J Clin Nutr 1988;47:942-7.

15. Adair LS, Popkin BM. Prolonged lactation contributes to depletion of maternal energy reserves in Filipino women. J Nutr 1992;122:1643-55.

16. Miller JE, Rodriguez G. Pebley AR. Lactation, seasonality, and mother's postpartum weight change in Bangladesh: an analysis of maternal depletion. Am J Hum Biol 1994;6:511-24.

17. Barrett-Conner E. Epidemiology and the menopause: a global overview. Int J Fertil Menopause Stud 1993; 38(suppl):6-14.

18. Gunby ML, Morley JE. Epidemiology of bone loss with aging. Clin Geriatr Med 1994;10:557-74.

19. Kent GN, Price Rl, Gutteridge DH, Allen JR, Rosman KJ, Smith M, Bhagat Cl, Wilson SG, Retallack RW. Effect of pregnancy and lactation on maternal bone mass and calcium metabolism. Osteoporosis Int 1993; 1(suppl):S44-7.

20. Specker BL, Vieira NE, O'Brien KO, Ho ML, Heubi JE, Abrams SA, Yergey AL. Calcium kinetics in lactating women with low and high calcium intakes. Am J Clin Nutr 1994;59:593-9.

21. Sowers MF, Corton G. Shapiro B. Jannausch ML, Crutchfield M, Smith ML, Randolph JF, Hollis B. Changes in bone density with lactation. JAMA 1993 269:3130-5.

22. Prentice A. Maternal calcium requirements during pregnancy and lactation. Am J Clin Nutr 1994; 59(suppl):477S-83S.

23. Prentice A, Dibba B. Jarjou LMA, Laskey MA, Paul AA. Is breast milk calcium concentration influenced by calcium intake during pregnancy? Lancet 1994;344: 411 -2.

24. Hopkinson J. Butte N. Ellis K, Heinz C, Shypaillo R. Recovery of bone density during lactation. FASEB J 1995;9:A85 (Abstract).

25. Prentice A, Jarjou LAM, Cole TJ, Stirling DM, Dibba B. Fairweather-Tait S. Calcium requirements of lactating Gambian mothers: effects of a calcium supplement on breastmilk calcium concentration, maternal bone mineral content, and urinary calcium excretion. Am J Clin Nutr 1995;62:58-67.

26. Cumming RG, Klineberg RJ. Breastfeeding and other reproductive factors and the risk of hip fractures in elderly women. Int J Epidemiol 1993;22:68491.

27. MacMahon B. Cole P. Brown J. Etiology of human breast cancer: a review. J Natl Cancer Inst 1973;50:2142.

28. Kelsey JL, John EM. Lactation and the risk of breast cancer. N Engl J Med 1994;330:136-7.

29. Newcomb PA, Storer BE, Longnecker MP, Mittendorf R. Greenberg ER, Clapp RW, Burke KP, Willett WC, MacMahon B. Lactation and a reduced risk of pre-menopausal breast cancer. N Engl J Med 1994;330: 81 -7.

30. Rosenblatt KA, Thomas DB, WHO Collaborative Study of Neoplasia and Steroid Contraceptives. Lactation and the risk of epithelial ovarian cancer. Int J Epidemiol 1993;22:192-7.

Discussion of paper by Rasmussen and McGuire

 

Dr. McLaren

Could you comment on what may be one of the larger effects of breastfeeding on maternal health and well-being, that is, avoiding two pregnancies back-to-back and two children under one year of age?

Dr. Rasmussen

That is covered in my considerations of the health of the subsequent child.

Professor Hanson

I understand that there is a protein in human milk that induces programmed cell death in many malignant cell lines. Could it be that in a mother who has been lactating several times, there would be such milk proteins remaining in the gland, which could induce apoptosis of cells that in time might turn into cancers?

Dr. Rasmussen

An attractive hypothesis, but I don't know enough about it to answer your question. Does anyone else want to take it on?

Professor Howie

No, I wouldn't like to take it on. I was going to ask a different question. One of the features of prolonged lactation is the reduction of the number of reproductive cycles that a woman has in her life. As I understand it, most circumstances that produce such a reduction also produce a reduction in ovarian carcinoma. Do you know of any direct evidence of that in women who have breastfed for a long time?

Dr. Rasmussen

I am not aware of people having looked at that, but again, it is an attractive hypothesis.

Dr. Poliltt

You indicated that breastfeeding had an effect on maternal behaviour. Could you say something more about that? And a second question. The United States is going through major social changes. Many children of teenage mothers of lower socio-economic class are born out of wedlock, often without a father present, and the use of drugs (in particular, crack) has reached epidemic proportions. What is the benefit of breastfeeding for this group of mothers?

Dr. Rasmussen

Dr. Garza has strong opinions on maternal behaviour, so I will ask him to respond to your first question. The issue here is that there are changes in the maternal brain as a result of breastfeeding that change the mother's responses to painful stimuli. Mothers become more placid.

Dr. Garza

The only thing I would add is that there are some very intriguing animal data suggesting that oxytocin, for example, may change maternal behaviour. It is very difficult to think that a hormone that has played such a basic role in animal physiology would not also have a similar impact on people. But of all the benefits-nutritional, immunologic, and bonding -the last is the least well documented and the least studied both in animals and in humans. A number of investigators around the world are taking a closer look at this. One symposium held in Europe about three years ago looked at the behavioural effects of hormones that we normally associate with lactation.

Dr. Pollitt

As a behavioural scientist myself, I think it is very attractive to think in terms of what breastfeeding does and how it could affect maternal behaviour, for example, through oxytocin acting on the brain. But I don't think there are any hard data that would actually support the notion that breastfeeding changes maternal behaviour. Just to carry out such a study would be very difficult. The data on bonding have been primarily related to the issue of immediate contact between the infant and the mother and have not really been related to breastfeeding, as such.

Dr. Rasmussen

The point that you are making is correct. The hard data available are essentially nil. We are making an inference. I was very careful not to use the word bonding because of exactly the problems that you outlined. Bottle-feeding mothers do feel close to their infants, and what do we have as a measure of closeness? It's not easy.

On your second question, you posed the all-tooreal situation of the teenage mother in the United States. What do we recommend? Such young women are biologically capable of breastfeeding. The issue is whether we recommend it to them. Breastfeeding is done most effectively by women who are committed to it. Teenage pregnancy programmes around the country are giving these girls a lot of support, and some of the investigators are finding that these young women can successfully breastfeed with this kind of support. When you see that, you are seeing a whole lifestyle change, and they may be giving up some of the practices that got them pregnant in the first place. We would like to have a situation in which we could feel good about recommending breastfeeding.

Dr. Lawrence

Carol Bryant and colleagues did as controlled a study as you can on a teenage population under those circumstances. They randomly assigned young women to two groups. They educated the women in one group to breastfeed. In the other group, they supported the mothers in every other way but never mentioned breastfeeding. They measured the effects on the mother, and after one year, there was a clear difference. Those women who had breastfed had changed. They had established some self-esteem and had gotten hold of their lives, whereas the mothers who had not breastfed had not changed. They had not deteriorated, but they had not improved in their own self-image and some other behaviours.

Dr. Rasmussen

So, I do not know whether we can make this a general recommendation. It requires a whole lot of support to happen well, and that is the kind of thing that Carol Bryant is doing.

Dr. Lawrence

I have been involved in some support for grassroots projects on mother-friendly workplaces. When we are thinking of policy, we should include schools as the teenage mothers' workplace. It is really amazing how much can be accomplished if teenage mothers can be encouraged to stay in school. Were you including sociocultural environment?

Dr. Rasmussen

I was considering the support for breastfeeding in the mother's particular home environment. Did her husband or partner support it? Did her mother-inlaw, her mother, her family? I was thinking about various cultural environments. For example, upstate New York is pro-breastfeeding. Davis, California, is perhaps the classic pro-breastfeeding environment. In inner-city Baltimore, the breastfeeding rate is only 4%.

Dr. Prentice

What are your feelings about osteoporosis in women who do not have such high levels of calcium intake as those in Janet King's studies? What do we advise women who are breastfeeding in the United States and in the United Kingdom who wish to give up dairy products because they are worried about colic in the baby? We have seen quite a few breastfeeding women give up drinking milk completely because of concern about fat in the diet. Do you feel that the 300 to 400 mg daily calcium intake in these women would be sufficient to sustain repletion?

Dr. Rasmussen

The simple answer is that I don't know. There are a number of papers on women whose daily calcium intakes are 1,000 mg or more. They certainly have adequate calcium to make that repletion. I don't know of any study in which women with lower calcium intakes have been followed over a longer period. I am not sure how ethical it would be to randomly assign them to a calcium pill or no pill plus their usual intake. Certainly nobody has done a joint analysis of lactation history, usual calcium intake, and incidence of osteoporosis. You have hit a raw nerve, because I took calcium pills myself when breastfeeding, since I am a non-milk-drinker myself.

Dr. Prentice

In the Gambia we found a small loss of bone calcium in the forearm. In women who were fully breastfeeding with no supplementation at all, there was a repletion before 12 months. There is an urgent need to follow at least some groups of women who are consuming low amounts of calcium. It doesn't have to be a trial, just an observational study.

Dr. McLaren

Before closing this session on the impact of breastfeeding on fertility, I would like to ask Bishop McHugh to comment on a point that some of us were discussing earlier today: whether it is acceptable to the Catholic Church and to the Holy Father if a woman decides to breastfeed with the express intention of not getting pregnant, of delaying her next pregnancy, of spacing her family.

Bishop McHugh

It is an easy answer. Yes, it is all right. There is no prohibition or inhibition on the part of the Church for a woman to use breastfeeding or the LAM (lactation amenorrhea method) as a method of spacing or delaying future births. In fact, it is our intent to encourage that. As Dr. Perez said, it very often correlates with the use of the natural methods of family planning, and indeed, many people in natural family planning today make a direct effort to combine breastfeeding with natural methods of family planning, as the early phase of deferring the next birth. There would be no prohibition by the Church to the use of breastfeeding to defer subsequent birth.

Dr. McLaren

Thank you, Bishop McHugh. I think that is a very important point.

Dr. Menken

Could I follow up on that? I assume there would be no objection to the use of methods of detecting ovulation, if the people could develop better means. Natural family planning is based on one method, a rather crude method. Would there be any problems if there were better methods of detecting when ovulation occurs?

Bishop McHugh

I would say no. As a matter of fact, at the earlier meeting on natural family planning, a lot of data on more technical methods were presented, but the more technical you get, the less useful it is to a population, especially to a third world population. There is a direct effort being made to find more accurate methods of predicting ovulation.

Protective effect of breastmilk against infection

Peter W. Howie

 

Abstract

There is strong evidence that breastfeeding protects infants against infection in environments where clean water cannot be guaranteed, leading to substantial reductions in morbidity and mortality. This is particularly evident in the protection against gastrointestinal disease, although there is also evidence for protection against respiratory infection and otitis media. The evidence for a protective effect of breastfeeding against infection in developed countries has been more controversial, with criticisms being levelled at the methodology of many studies. Evidence is presented from a study in a developed country that met key methodological criteria to show that breastfeeding for 13 weeks offers substantial and continuing protection against gastrointestinal illness. Smaller, but still potentially important, protective effects against respiratory illness also occur. The results add strong support to policies that promote breastfeeding in both developed and developing countries.

 

Introduction

"Breast is best" is one of the most widely used and best-known slogans in the promotion of breastfeeding. There are several reasons to promote the support of breastfeeding for all mothers and babies, but one of the most important is the protection that breastmilk offers babies against infectious disease. There is very strong evidence from many studies that breastfeeding confers substantial protection against serious morbidity and mortality in those developing countries where access to clean water is not readily available [1-3]. This subject is discussed in more detail by Victora [4] in this issue.

Evidence both from epidemiologic studies in developing countries and from the physiological components of breastmilk strongly suggests that breastmilk has an important role in protecting babies against infection. In particular, lactoferrin, which binds iron necessary for coliform growth, and lysozymes, which have bactericidal activity against gram-positive and gram-negative organisms, are supportive of the antimicrobial effect of breastmilk. The influence of the immune system and the secretion of IgA in breastmilk is discussed in this issue by Hanson et al. [5]. Taken together, this evidence indicates a clear and important role for breastfeeding as a means of protecting infants from infection.

 

Breastfeeding and infant infection in developed countries

The central question in this article is the role that breastfeeding may have in protecting infants against infection in developed countries where clean water supplies are guaranteed. A number of authors have expressed skepticism that breastfeeding has such a role in developed countries [6].

In 1986 Bauchner et al. [7] reviewed all the articles that had appeared in the English-language literature since 1970 investigating the relation between infant feeding and health. They scrutinized all studies that contained at least 40 subjects in their sample and applied four key methodological criteria to evaluate the scientific quality and reliability of the studies. The criteria were the avoidance of detection bias, adjustment for confounding variables, a definition of outcome events, and the definition of infant feeding. They examined 14 cohort studies and 6 case-control studies. Eight of the cohort studies reported a protective effect of breastfeeding against infant infection, and six found no evidence of protection. Four of the casecontrol studies found evidence of a protective effect, and two did not. None of the studies found any evidence that breastfeeding might increase the vulnerability of infants to infectious disease.

The significant finding of the review by Bauchner et al. was that they identified significant methodological flaws in all but two of the studies, and even these two could be criticized for having inadequate sample sizes.

To avoid detection bias, it is necessary to ensure that comparative groups of bottle- and breastfeeding motherinfant groups are studied with equal vigour. For example, breastfeeding mothers may be more anxious and therefore more willing to report episodes of infection to their physicians. In addition, it is important to ensure that the interval between any possible infectious episode and the recording by the investigator is sufficiently short, because there is a high incidence of failure to recall significant episodes when the reporting interval is long.

In most developed countries, there is a strong social class bias between bottle- and breastfeeding mothers, with breastfeeding mothers coming from the higher socioeconomic groups. This and other differences between bottle and breastfeeding mothers can introduce important confounding variables that may explain differences in rates of infectious disease in children of the two groups that are not attributable to the method of feeding. Unless great care is taken to allow for confounding variables, it is not possible to attribute reliably any difference in infectious disease frequency to the effect of breastfeeding itself. Studies that do not take due account of confounding variables, therefore, must be regarded as scientifically flawed.

A third important factor is to make clear definitions of the outcome events and to apply them with equal rigour to both bottle- and breastfeeding groups of mothers. In particular, when studying the effect of infant feeding on diarrhoeal disease, it has to be borne in mind that the stool consistency differs between bottle- and formula-fed infants. Unless rigorously applied criteria are applied to the definition of infant disease, it is possible that spurious differences between bottle- and breastfed infants will be observed.

Finally, many mothers do not fall neatly into bottle- or breastfeeding categories, as early introduction of formula and solids, mixed feeding, and use of expressed breastmilk may complicate the definition of infant-feeding categories. It is important, therefore, that infant-feeding groups be defined precisely on the basis of carefully collected contempora neous information about the feeding pattern of the infant.

Applying these criteria, Bauchner et al. found methodological weaknesses in the great majority of the studies that had examined the potential protective effect of breastmilk against infection in young infants. They concluded that "breastfeeding has at most a minimal protective effect in industrialized countries." In my view it would have been more appropriate to conclude that a rigorous study of the potential protective effect of breastfeeding against infection should be carried out using a sample of sufficient size. Because of the methodological weaknesses in the previously published studies, it was equally as possible that an important protective effect of breastfeeding against infection had been concealed or minimized in some of the studies as that a protective effect had been reported that did not exist.

 

Dundee Infant Feeding and Health Project

Because of the unsatisfactory nature of the published reports, a study was performed in Dundee, Scotland [8], to investigate the relation of infant feeding and infectious disease using a methodology that took into account the requirements set out by Bauchner et al.

The specific aims of the study were (1) to compare the frequency of childhood illness in breast- and bottle-feeders after correcting for confounding variables and (2) to determine if the frequency of childhood illness is influenced by the duration of breastfeeding.

Study sample

Details of the study sample and the methods of recruitment have already been published [8]. A total of 750 mothers were recruited to the study, of whom 6 withdrew after delivering their babies. Because the objective of the study was to include only healthy babies of normal birthweight, a total of 70 babies were excluded because they either were delivered before 38 weeks with a birthweight of less than 2,500 g or spent more than 48 hours in the Special Care Baby Unit. This left 674 mother-infant pairs, who were followed up for two years with a 91.5% completed followup rate.

Avoidance of detection bias

To overcome the problem of detection bias, follow-up was carried out by both "hot" and "cold" pursuit. Medical, social, and obstetric data were collected at birth and used in allowing for confounding variables. Each mother-child pair was visited at home at 0.5, 1, 2, 3, 4, 6, 9, 12, 15, 18, 21, and 24 months after birth, and detailed information was collected about the child's feeding and health. Standardized questionnaires were used, and the visitors were given instruction sessions to standardize the method of data collection. In addition to this hot pursuit of information, further data were acquired by scrutiny of the general practice records to identify episodes of illness that were reported to the general practitioner but not to the health visitor. This method of data collection was applied with equal vigour to all groups of mothers in the study.

Definition of outcome event

The intention of the study was to define the effect that infant feeding would have on episodes of serious illness. The definitions of illness were adapted from those used by Chandra et al. [9] in a previous study. The episodes of infectious disease had to last at least 48 hours before they were considered significant. Gastrointestinal infection was defined as vomiting and diarrhoea, respiratory infection as coryza and cough or wheeze, and ear infection as painful discharging ear, all lasting for at least 48 hours. Infections of mouth and skin were determined by the presence of inflammation, and eczema was diagnosed by a physician on the basis of typical signs. The episodes of illness were reported to the study coordinator, and if there was any doubt whether an episode qualified for inclusion under the study criteria, a decision was taken by a paediatrician who reviewed the information without knowing the feeding category of the subject.

Definition of infant feeding

During each visit detailed information was collected about the infant's feeding in the previous 24 hours. This was done to ensure that accuracy of recall would be maximized. Information was collected about the number of breastfeeds, the number of formula feeds, the number of solid feeds, and the number of juice and water feeds. This information was used to calculate the dates of the first introduction of formula, cow's milk, and solid feed as well as the last date of breastfeeding.

On the basis of this detailed contemporaneous information about breastfeeding, babies were allocated to one of four groups. (1) Bottle-feeders were exclusively bottle-fed from birth. (2) Early weaners were breastfed for less than 13 weeks. (3) Partial breastfeeders were breastfed for 13 weeks or more, but formula or solid-food supplements were introduced before the age of 13 weeks. (4) Full breas-feeders were breastfed for 13 weeks or more, and no formula or solid-food supplements were introduced before the age of 13 weeks. The comparative analyses were carried out using these four infant-feeding groups.

Adjustment for confounding variables

A total of 40 potential confounding variables were identified in the groups of maternal factors, infant factors, and paternal factors. Although a number of factors differed between bottle- and breastfeeding mothers, the three most significant confounding variables among the main groups were social class, parental age, and maternal smoking. A regression analysis technique was used, and after allowing for these three factors, all other differences were nonsignificant. Reanalysis of data introducing a greater number of confounding variables made no difference to the final conclusions.

Calculation of sample size

The principal outcome variable was determined as the incidence of gastrointestinal disease in the first 13 weeks of life. This was expressed as the proportion of babies having one or more episodes of gastrointestinal disease during that time. On the basis of the data of Fergusson et al. [10], it was hypothesized that breastfeeding would lead to a reduction in the incidence of gastrointestinal illness from 16% to 8% in the first 13 weeks of life. It was calculated that a sample size of 560 mother-baby pairs would be needed to achieve a 90% certainty of a significant result at the .05 level (two-tailed test). Thus, the actual sample size of 674 resulting from the original recruitment of 750 mothers was more than sufficient.

 

Results

Incidence of gastrointestinal disease during the first 13 weeks

Figure 1 shows the percentage of babies with one or more episodes of gastrointestinal disease in the first 13 weeks of life, according to their infantfeeding category as defined above. The unshaded columns show the observed incidence of gastrointestinal illness, and the shaded columns show the adjusted incidence after allowing for the three confounding variables described above. The observed incidence of gastrointestinal illness in bottle-fed babies was 19.3%. This did not differ significantly from the observed incidence (18.3%) in babies who were weaned before 13 weeks, usually within a few days of birth. These incidences contrasted sharply with those in the partially and fully breastfed groups (4.8% and 2.2%, respectively). The latter two groups did not differ significantly in the frequency of gastrointestinal illness. When the incidence of gastrointestinal illness in the breastfed babies, whether partially or fully breastfed, was compared with that in the bottle-fed babies, there was a highly significant difference that persisted after adjustment for confounding variables (p < .001).

Similar comparisons were made among these four feeding groups for the periods 14 to 26 weeks, 27 to 39 weeks, and 40 to 52 weeks. The results are shown in table 1. Although the relation between breastfeeding and protection against infection became less clear-cut as time progressed, there was a persistent reduction in the incidence of gastrointestinal illness in those babies who had been fully breastfed for 13 weeks compared with those who were bottle-fed from birth. This difference persisted despite the fact that many of the mothers who fully breastfed their babies during the first 13 weeks had completely weaned them by the age of one year.

The relation between infant feeding and respiratory infection was also analysed (table 1). In general, the incidence of respiratory infection during the first year of life was less among partially and fully breastfed babies, but the differences were much smaller than those for gastrointestinal illness, and they were only observed during the periods from 0 to 13 weeks and from 40 to 52 weeks.

Effect of breastfeeding on hospital admissions for infectious disease

The effect of breastfeeding upon the incidence of hospital admissions of babies for infectious disease was studied, using babies who were bottle-fed from birth as the comparative group (fig. 2). When the results were expressed as an odds ratio, the incidence of admission was similar for babies who were breastfed for less than 13 weeks and for those who were bottle-fed from birth. By contrast, the incidence of admission was significantly lower for all the groups of babies who were breastfed for more than 13 weeks than for those who were bottlefed from birth. No significant protective effect of breastfeeding was observed against ear, mouth, eye, or skin infection, colic, eczema, or nappy rash.

 

Conclusions

Breastfeeding for 13 weeks reduces the rate of gastrointestinal illness in infants during the first year of life after correcting for confounding variables. The protective effect of breastfeeding is not dependent upon the avoidance of early supplements and persists beyond the period of breastfeeding itself. There is a similar but smaller reduction in the rate of respiratory illness in babies who are breastfed, for 13 weeks. Breastfeeding for 13 weeks also reduces the incidence of hospital admission owing to serious episodes of infectious disease



FIG. 1. Percentage of babies with one or more episodes of gastrointestinal illness during the first 13 weeks of life according to early infant-feeding group. Unshaded columns show observed percentages, and shaded columns show percentages adjusted for social class, parental age, and maternal smoking

TABLE 1. Numbers (percentages and percentages adjusted for social class, parental age, and maternal smoking) of babies with infections up to one year of age according to method of feeding in the first 13 weeks

Type of infection Weeks Bottle-fed (n=426) Early weanears (n=161) Breasfed % for adjusted rates 95% CI for diference between bottle- and breadfed
Partially (n=121) Fully (n=89) Bottle-fed vs early wearnes Partially vs fully breastfed Bottle-vs breasfed
Gastrointestinal 14-26 47 (19.1, 17.9) 33 (20.5, 20.2) 8 (6.6, 6.9) 7 (7.9, 8.7) 0.33 0.21 8.06a 4.0 to 16.2
27-39 55 (22.3, 21.8) 35 (21.7, 21.1) 20 (16.5, 16.5) 7 (7.9, 8.5) 0.03 2.79 4.03b 2.5 to 16.1
40-52 55 (22.4, 22.7) 21 (13.0, 12.8) 19 (15.7, 15.2) 6 (6.7, 6.6) 6.23b 3.85b 6.70a 5.1 to 18.5
Respiratory 0-13 100 (38.9, 37.0) 54 (32.0, 31.7) 29 (23.0, 24.2) 22 (23.2, 25.6) 1.22 0.05 6.35b 3.9 to 20.3
14-26 116 (47.1, 46.0) 76 (47.2, 47.2) 42 (34.7, 35.5) 34 (38.2, 39.9) 0.06 0.40 2.80 - 0.8 to 17.4
27-39 112 (45.5, 42.9) 85 (52.8, 52.6) 57 (47.1, 49.5) 32 (35.9, 39.6) 3.48 1.89 0.31 - 10.8 to 7.5
40-52 133 (54.1, 53.3) 72 (44.7, 44.6) 46 (38.0, 38.6) 38 (42.7, 44.2 ) 2.79 0.63 5.57b 2.7 to 21.1

Sourece: ref 8.
a. p<.01.
b. p<.05.



FIG. 2. Babies admitted to hospitals in their first year: odds ratio adjusted for social class, parental age, and maternal smoking according to duration of breastfeeding. breastfed is given an odds ratio of 1.0

 

Discussion

The conclusions of this article are entirely dependent upon the rigour of the methodology. Every precaution was taken to meet the methodological criteria set out by Bauchner et al. [7]. Assuming that the study is regarded as methodologically sound, it provides very strong evidence that breastfeeding offers substantial protection against gastrointestinal illness in developed countries. The 19% incidence of vomiting and diarrhoea during the first 13 weeks of life was very similar to the 16% incidence reported by Fergusson et al. [10] during the first four months of life in their study in Christchurch, New Zealand. Bearing in mind that the episodes of illness that were reported had to last for at least 48 hours, it is clear that babies who are bottle-fed from birth are exposed to a substantial risk of significant episodes of gastrointestinal illness not only during the first 13 weeks but throughout the first year of life, as shown by the much lower incidence of hospital admission among babies breastfed for 13 weeks or more.

A further analysis was carried out to examine the possibility that breastfeeding for less than 13 weeks would offer significant protection. The results showed that breastfeeding for 6 weeks did not confer the same level of protection as breastfeeding for 13 weeks, and confirmed the view that a minimum period of 13 weeks should be recommended to ensure a substantial degree of protection. Another important finding was that exposing infants to breastmilk for only the first few days of life is insufficient to offer any significant protection against infection, suggesting that exposure to colostrum alone is not enough.

This study provides strong evidence to support the promotion of breastfeeding for all mothers in developed countries [3,11,12]. It reinforces the need to provide mothers who wish to breastfeed adequate support and facilities in the form of health-service support, creche facilities, and adequate maternity leave. It is also possible that the benefits gained from breastfeeding in the early weeks of life may continue into later stages of infancy and childhood, and this possibility is being examined through further follow-up studies of this cohort of mother-baby pairs.

 

Acknowledgements

This study was supported by the Scottish Office Home and Health Department.

 

References

1. Plank SJ, Milanesi ML. Infant feeding and infant mortality in rural Chile. WHO Bull 1973;48:203-10.

2. Victora CG, Smith PG, Vaughan JP, Nobre LC, Combardi C, Teixeira AMB, Fuchs SMC, Moreira LB, Gigante LP, Barros FC. Evidence for protection by breastfeeding against infant deaths from infectious diseases in Brazil. Lancet 1987;ii:319-22.

3. Cunningham AS, Jelliffe DB, Jelliffe EF. Breastfeeding and health in the 1980s: a global epidemiological review. I Pediatr 1991;118:659-66.

4. Victora CG. Infection and disease: the impact of early weaning. Food Nutr Bull 1996:17:390-96.

5. Hanson LA' Wiedermann U. Ashraf R. Zaman S. Adlerberth 1, Dahlgren U. Wold A, Jalil F. Effects of breastfeeding on the baby and on its immune system. Food Nutr Bull 1996:17:384-9.

6. Kovar MG, Serdula MK, Marks JS, Fraser DW. Review of the epidemiologic evidence for an association between infant feeding and infant health. Pediatrics 1984;71(suppl):615-38.

7. Bauchner H. Leventhal JM, Shapiro ED. Studies of breastfeeding and infections. How good is the evidence? JAMA 1986;256:887-92.

8. Howie PW, Forsyth JS, Ogston SA, Clark A, Florey CD. Protective effect of breastfeeding against infection. BMJ 1990;300:11-6.

9. Chandra RK. Prospective studies of the effect of breastfeeding on incidence of infection and allergy. Acta Paediatr Scand 1979;68:691-4.

10. Fergusson DM, Horwood J. Shannon FT, Taylor B. Breastfeeding, gastrointestinal and lower respiratory illness in the first two years. Aust Paediatr J 1981; 17:191-5.

11. Habicht JP, Da Vanzo J. Butz WP. Does breast-feeding really save lives, or are apparent benefits due to biases? Am J Epidemiol 1986;123:279-90.

12. Standing Committee on Nutrition of the British Paediatric Association. Is breast feeding beneficial in the UK? Arch Dis Child 1994;71:376-80.

Discussion of paper by Howie

 

Dr. Colombo

I recognize that the protocol for your study was rigorous, but I was a little confused and concerned because of so many interacting variables. You studied 40 variables, but I want to know how some were excluded and others were retained as important variables to make this statistical analysis conclusive. Thank you for your lecture and expert use of statistics.

Professor Howie

I am not a statistician, but I think our study demonstrates the power of regression analysis techniques. They have made valid and robust statistical analyses of this kind possible, which has been a very important step forward in statistical methodology.

Dr. Woolridge

I would like to ask one question about what is generally regarded as a very elegant study. When you discussed the instance of gastrointestinal illness from 0 to 13 weeks, you said that receiving colostrum had no impact (or appeared to have no impact) on reducing the incidence of infection. Nevertheless, when you came to 40 to 52 weeks, the early weaners had comparable rates to the partial breastfeeders and seemed to be distinct as a group from both the bottlefeeders and the full breastfeeders. Have you any way of accounting for this disparity at 40 to 52 weeks? Might that be due to a failure to control for another confounding factor at that age?

Professor Howie

It is possible that what you say is correct. Some differences appeared to emerge later in the first year, and it is possible that colostrum is having some effect. It does seem, however, to be a marginal effect rather than a dominant one. All the data were subjected to the correction of confounding variables throughout the study, so the differences that you see were the true, observed, and corrected differences.

Dr. Woolridge

I was just thinking about the additional confounders that might apply at a later stage, such as contact with other infants or toddlers from toddler groups.

Professor Howie

Contact with other children was one of the points that we specifically included as a variable. If older children are coughing over the infant, this is obviously a very important variable and was a point on which we collected specific information that was included in the analysis.

Dr. Pollitt

Dr. Colombo said it is a very elegant study and very nicely done, but I am not sure if I know what the mother craft variable is, and that may answer my question. I would like to point out, however, that the nature of your confounders is not the same as the nature of the behaviour in your study. In other words, the confounders that you have chosen are primarily structural variables, whereas breastfeeding is really a process variable. It could very well be that there are confounders at the process level that could perhaps account for a little bit more of the variance of the differences between groups.

Professor Howie

As to the first point: mother craft is parent craft. This was measured as attendance at classes during the antenatal period giving advice about preparation for motherhood and labour and so on. This variable was very strongly related to social class. If you correct for social class, you would at the same time correct for the mother craft variable. You are absolutely right that you can only do the best with what is quantifiable information when allowing for confounding variables. Studies of this kind will always be open to the possibility that we have not identified some confounding variable that may be important but not measurable. Short of being able to do a truly randomized controlled trial (which is not possible for breastfeeding), the best you can do is to collect and measure as many of the direct and indirect confounders as possible. You are right that despite all our efforts, we still may have failed to capture one or more of the crucially important confounding factors.

Dr. Pollitt

I am not trying to sound overly critical. The point I am trying to make and with which you agree is that in these kinds of studies you can never control for all the potential confounders. The best model would be a clinical trial. What I do want to emphasize is that unless we get information at the process level, particularly in interpersonal communication or relationships, we will be missing a very significant portion of the pie. I can give an example of the process variable. In the case of breastfeeding, this is the dynamic interaction between the mother and the child that involves certain kinds of behaviours that result in feeding. In the same way, there may be other interpersonal aspects of the relationship between the mother and the infant that do not have to do with feeding but could be correlates of it and account for the outcome variable. You are absolutely right that the ideal is a clinical trial, but we cannot always do that.

Professor Howie

I think cigarette smoking is a process variable in the sense that you are talking about, and that was an important confounder. Many of the important variables are associated with social class and disappear when it is controlled for.

Dr. Colombo

These are the normal difficulties of experimental surveys. You cannot always do experiments because of ethical problems.

Dr. Menken

With your early weaners, what did you do to correct for the possibility that illness might cause the end of breastfeeding? You had data on those early weeks.

Professor Howie

Yes, we did look at illness causing early weaning. If we thought that was the case, then the illness was attributed to the feeding category they were in before they had the illness. We looked at that specifically, but in fact it was relatively uncommon. In the analysis we adjusted both ways, for if we assigned mothers who weaned during an illness to the breastfeeding or the weaned groups, this made no difference to the overall conclusions. That was a point raised in the Bauchner study [7] and we did try to take account of it.

Dr. Garza

I, too, want to congratulate Professor Howie for a very elegantly carried out study. The exchange with Dr. Pollitt reminded me of a plea that an American politician once made of a scientist. He said he was looking for a onearmed scientist to testify before Congress, because scientists always said, "On the one hand you have this, and on the other hand you have that." The politician wanted to know if we couldn't find the one-armed variety, so that we could be as unambiguous as possible.

The key word that Professor Howie used was breastfeeding, which does refer to a process, as opposed to a single biological variable such as human milk. My second point is that there are some historical studies that came to some very comparable conclusions, without the degree of rigour that your study had, particularly looking at the persistence effect. This suggests that maybe we are looking at something beyond breastfeeding to mother craft and other similar variables. On the other hand, there are some biologically plausible explanations that I think Professor Hanson will get to.

Another point I want to make concerns HIV. I think HIV is a terribly important issue, and I want to ask if there is anyone here who has more recent information. The most recent information I have is that the P24 antigen, which is a good indicator of replicating virus, has been found only in colostrum. Thus, if vertical transmission occurs, it may occur only in the colostral phase. This may be because there are so many cells in colostrum, and HIV is an intracellular virus. Although antigens have been identified in the cell-free medium, I don't know whether these have any significance for the nature of transmission.

Professor Howie

If that's true, that is a very important point. I wasn't aware of it, and I am sorry I can't comment.

Professor Hanson

I don't have as many answers as I would like to have, but there are a number of risk factors that we know about. The main risk is that of infection of the infant via the mother's blood at delivery. There is clear evidence that this does occur. The second risk situation is when an infected lactating mother transmits the virus to the baby in the milk, despite the protective factors in human milk. The statement of WHO is partially based on the fact that if breastfeeding were not practiced in areas of Africa, there would be an estimated 2,000 deaths from diarrhoea for each death from AIDS. This is a difficult matter, and there are two sides to it. I wasn't aware of Dr. Garza's point, and it is very important. However, African studies show that acute infection during lactation may be transmitted later than the colostral phase. This remains an open question.

Dr. Veld/strong>

Coming back to your study, I am really impressed with the sustained effect of breastfeeding against infection. I am also curious about how you reached the conclusion that there weren't any further advantages to breastfeeding for more than 13 weeks. Surely if babies continue to breastfeed, they will be better protected.

Professor Howie

From the hospital admission data it looked as though there was a step down in the advantages after 13 weeks. We reanalysed for breastfeeding lasting only six weeks, but this seemed to be too short a time to establish maximal benefit. On the other hand, it looked as though the benefits of feeding beyond 13 weeks fell for both disease incidence and hospital admission. The data do show that the feeding method in the early weeks has long-term effects. I don't know if Professor Hanson is in a position to comment on this, but I believe there is some evidence that the first 13 weeks is a period of immunologic vulnerability. I have heard of the concept of the gastrointestinal tract maturing at about 13 weeks, so that before this time the baby is particularly vulnerable to disease. It may be that protection during this time is particularly important, but I am not as expert in this as some other people here. We can only report the results as we found them.

Dr. Vald/strong>

We are doing a similar study. Infants were breastfed until an illness developed. Up to the age of six months, there was a real difference in the rate of infections between exclusively and non-exclusively breastfed infants.

Dr. Victora

I have a comment on the HIV problem. I was part of the WHO Working Group that drafted that resolution. As Professor Hanson mentioned, we had to calculate the number of deaths that would be prevented by avoiding breastfeeding and thereby reducing HIV transmission, versus the number of deaths that would be prevented by continuing breastfeeding. The initial problem is that in Africa you don't know which mothers are HlV-positive, because there is no widespread screening. This means that any kind of recommendation against breastfeeding would affect both HlV-positive and HlV-negative mothers. It is a major reason for concern, but with the current state of knowledge, the risks of HIV transmission through breastfeeding are much smaller than the risks of not breastfeeding, so that's why we arrived at the conclusion in favour of continuing breastfeeding.

Professor Howie

I certainly support the conclusion that the WHO came to, but as I am sure you are also aware, the concerns about HIV are being used by the milk manufacturers, particularly in Africa, to introduce a significant fear factor to the mothers, advising them to abandon breastfeeding. As you also say, this may lead to greater detriment than any benefits they may achieve. We have to be fully aware of this fear factor and make our views clear to the mothers.

Dr. Lawrence

Were there enough breastfeeders among the low-income mothers to enable you to analyse separately the impact of breastfeeding on the occurrence of disease in this group? This is important, because they are so often our targets.

Professor Howie

There was a deficiency in the number of breastfeeders in the lowest economic groups, but the benefits were striking in both the upper and lower socioeconomic groups. The main point of our study is that there has been a perception that advice in favour of breastfeeding is all right for the poor people of developing countries but is really irrelevant to the United States and Europe. What we found shows that this is not true at all. It puzzles me why we have an 18% vomiting and diarrhoea rate within the first three months in a place like Dundee, where we have clean water supplies. If we say that unclean water is the key issue, then Dundee should have far lower infection rates than Manila and other similar places. The fact that rates of gastrointestinal disturbance among bottle-feeders are so similar across cultures makes me wonder whether we are really observing infection. Alternatively, it may be some disorder of the gastrointestinal tract other than infection that is actually making the babies vomit and have diarrhoea. Maybe we haven't yet identified the true nature of the problem of early vomiting and diarrhoea.

Dr. Victora

You might find a lot of rotavirus infection, which is widespread in both developed and developing countries and has nothing to do with water supplies.

Dr. Garza

We did a study that looked particularly at lowincome populations in Houston about 15 years ago.

We never published it, because we weren't confident that we could deal with some of the issues that were raised, but we found very substantial differences in diarrhoeal and respiratory infections in babies of low-income women who were breast- or bottle-feeding. We controlled for socio-economic status in that we recruited only women who were delivering at our public assistance hospital. But when we looked at our two groups, we found that despite our efforts to control for socioeconomic status, the women who elected to breastfeed were taller and had infants with higher birthweights than the women who elected to bottlefeed. This suggests there is some inherent difference, even in a group of homogeneous socioeconomic status, between women who choose to bottle-feed and those who choose to breastfeed.

Effects of breastfeeding on the baby and on its immune system

Lars A. Hanson, Ursula Wiedermann, Rifat Ashraf, Shakila Zaman, IngegrAdlerberth, Ulf Dahlgren, Agnes Wold, and Fehmida Jalil

 

Abstract

Human milk is a very complex fluid with a number of components and multiple functions. New functions are continually being identified. It is clear that human milk can affect the immune system of the breasfed infant. This results both in enhanced vaccine responses and, at times, down-regulation of other immune reactivities, such as transplant rejection and the risk of developing certain immunologic diseases, such as type I diabetes. Breastfeeding presumably gives the infant the possibility for an optimal immune response by providing good nutrition, including a decreased risk of vitamin A deficiency. The control of the intestinal flora and the anti-inflammatory effects of maternal milk also increase the possibilities for an adequate immune response in the infant. Further study is needed of the roles of idiotypic and anti-idiotypic antibodies, growth factors, cytokines, and various anti-inflammatory factors in the maternal milk in the infant's host defence.

 

Introduction

Human milk is a very complex fluid with a multitude of proteins, cells, and other components. Knowledge is continually increasing about the effects of breastfeeding on the infant, including a number of direct and indirect effects on the immune system. Such influences are related to the fact that human milk is rich in various immunologically active factors, in particular the stable antibodies. Secretory IgA (SlgA) protects the mucous membranes of the infant's gastrointestinal and respiratory tracts, where most infections occur [1]. Mother's milk also contains IgG and IgM antibodies, hormones, antioxidants, vitamins, cytokines, growth factors, complement factors, prostaglandins, granulocytes, macrophages, B and T Iymphocytes, and so forth. Many of these milk components not only participate in the support of the infant's host defence but also affect the normal microbiological flora in the gastrointestinal tract. In addition, other tissues and organs, including the immune system, are influenced.

 

Breastfeeding enhances vaccine responses in the infant and may affect transplantation outcome

A significantly higher salivary SlgA antibody response was obtained in breastfed than in nonbreastfed Italian infants after parenteral vaccination with diphtheria and tetanus toxoids and after oral poliovirus vaccination [2]. Stool SlgA antibodies could not be used to measure the antibody response because of the presence of milk SlgA antibodies in the stool of breastfed infants. Instead, we analysed stool IgM, an isotype that is present at very low levels in maternal milk. The stool IgM response to parenteral tetanus toxoid and oral poliovirus vaccine was significantly higher in the breastfed group. These observations of the secretory antibody increases were obtained in infants 3 and 4 months of age. The infants had been vaccinated according to the ordinary vaccination schedule at 2, 3, and 12 months of age. Between the ages of 21 and 40 months, serum IgG antibodies to diphtheria toxoid and neutralizing serum antibodies to poliovirus were also significantly increased among the breastfed group compared with the formula-fed controls. These observations are in agreement with another study that determined the serum antibody response to the Haemophilus influenzae type b (Hib) polysaccharide capsule in breastfed and nonbreastled children who were vaccinated parenterally with an Hib protein conjugate vaccine [3].

The explanation for this effect of breastfeeding on the vaccine response is not entirely clear. We favour the hypothesis that at least some of the enhancing effect could be due to the anti-idiotypic antibodies (anti-antibodies) in human milk. We have shown the presence of such anti-antibodies against poliovirus in human milk [4]. In the proper concentration, antiidiotypes can enhance immune responses [5]. Nevertheless, it is not clear how milk immunoglobulins could be taken up by the child, and other explanations are possible. Thus, maternal milk contains nucleotides that might affect the infant's immune response by stimulating lymphocytes].

If breastfeeding is enhancing vaccine responses, one might expect long-term positive effects of breastfeeding on the host resistance of the breastfed infant. In fact, Silfverdahl et al. [7] found a long-term protective effect of breastfeeding against invasive H. influenzae infections such as meningitis and epiglottitis.

Several early studies suggested that tuberculin sensitivity was transferred via mother's milk [8, 9]. Even if the resulting tuberculin sensitivity in the infant was temporary, the observation suggested that T Iymphocytes present in milk could be transferred to the offspring. This may be the reason why vaccination against bacillus Calmette-Gun seems to induce a stronger T-cell response in breastfed infants than in non-breastfed infants [10].

Transfer of milk cells may also result in immunologic tolerance (selectively reduced immune response) in the baby. Thus, a low response to paternal cells can be induced in newborn mice by letting them suckle a foster mother with the same transplantation antigens as their father [11]. This phenomenon may explain why renal transplants from mothers survive longer in offspring they have breastfed than in those they have not breastfed [12]. In premature infant baboons given radioactively labelled human colostral leucocytes, radioactivity accumulated in the gut wall, liver, and spleen [13]. This suggests that the milk cells are really taken up and have the capacity to influence the immune system of the offspring. Such an influence might explain the finding that breastfeeding can decrease the risk of the offspring developing autoimmune type I diabetes later [14]. The risk of type I diabetes determined by genetic factors is 30% to 40%. Nevertheless, the risk of inheritance from the father is two to three times greater than that from the mother. This difference may be at least partially explained by the effect of breastfeeding, which seems to halve the risk. In this connection, it may be added that breastfeeding seems to diminish the risk of developing Iymphomas [15] and Crohn's disease [16]. This effect remains long after the breastfeeding has been terminated.

Breastfed infants respond to infections with respiratory syncytial virus with more interferon-y (IFN-y) than do non-breastfed infants [17]. The breastfed infants also produce higher total levels of SlgA in the urine than their formula-fed counterparts [18].

 

Breastfeeding, nutrition, and immunity

A major cause of undernutrition in poor countries is the frequent infections resulting from inadequate hygiene, with contaminated water, lack of latrines, ineffective vaccination programmes, inefficient primary health care, lack of education, and the like. As shown by Howie [19] in this Workshop, breastfeeding can effectively prevent many of those infections.

Breastfed infants are usually given extra water during the hot season. Several studies have shown that this is totally unnecessary [20, 21]. Extra water makes babies less thirsty, which causes them to suck less, so that less milk is produced. Therefore, during the hot season, when the risk of infection is highest, the babies will get less milk. We have shown in a study from Pakistan that infants given water have more frequent diarrhoeal attacks and a significant reduction of weight and of head circumference compared with those who are exclusively breastfed [21]. Whereas breastfeeding provides optimal nutrition to the infant, deficient or absent breastfeeding is clearly a risk factor for inadequate nutrition. The subsequent frequent infections add to the undernutrition, which can impair host defence in a number of ways. It is not always clear, however, that these disturbances of the immune system are of clinical relevance.

We have shown that vitamin A deficiency in rats causes a severe immunodeficiency, followed by a greatly reduced capacity to respond to vaccines and to resist infections, such as diarrhoea and septic arthritis [22, 23]. These animals also have severe protein-calorie undernutrition owing to the loss of appetite caused by the lack of vitamin A. When the vitamin deficiency is corrected by giving retinyl palmitate (vitamin A), their immune response normalizes, although their body weight remains some 30% less than normal.

Immunodeficiency in vitamin A-deficient rats is characterized by a 90% reduction of the intestinal SlgA antibody response to an oral cholera vaccine and a similar reduction of IgE antibody responses to soluble proteins. There is also a reduced IgM and IgG antibody production in response to T cell-dependent antigens. In addition, there is an upregulation of certain TH1 activities.

When these animals are colonized orally with a strain of Escherichia coli, the whole gut contains large numbers of bacteria, which translocate and are thus found in the local Iymph glands. The rats get diarrhoea and at the same time show increased levels of IgE antibodies to the colonizing bacteria and a normalization of the SIgA response, possibly owing to an adjuvant effect of the bacteria in the lymph nodes. These observations may be relevant to several unexplained problems with infection among non-breastfed infants in poor countries [24].

The most common cause of death between 3 and 28 days of age in poor populations in Pakistan is neonatal septicaemia [25]. The causative bacteria most likely originate in the intestinal flora. The subclinical vitamin A deficiency may increase the risk of translocation of intestinal bacteria so that these bacteria reach the bloodstream. The major cause of death after 28 days of age is diarrhoea, and 84% of the deaths occur after prolonged diarrhoea. Again, early subclinical vitamin A deficiency may pave the way for prolonged diarrhoea.

In Pakistan 34% of the mortality in the first two years of life occurs in the first week and 90% in the first six months [25]. Measures to protect infants during this sensitive period of life are therefore crucial. Vitamin A deficiency is common in mothers and infants in our study area in Pakistan (unpublished data), as in many other pans of the developing world. A significant reduction of this early mortality might be attained by giving the mothers vitamin A directly after delivery and ensuring that they start breastfeeding immediately, thus transferring most efficiently both vitamin A and SIgA antibodies.

In a pilot study in a Pakistani village, we have seen the effects of introducing a health programme that involves breastfeeding promotion, improved primary health care, and education of mothers. Infant modality, stunting, and the prevalence of diarrhoea were all decreased by 50% within two years (F. Jalil, personal communication, 1995). It will be of interest to see what supplementation of breastfeeding mothers with vitamin A might do in this setting.

 

Breastfeeding and the intestinal flora

Other kinds of indirect effects on the infant's host defence presumably follow from the effects of breastfeeding on the intestinal flora. Non-breastfed infants in poor areas are quickly colonized by several potentially pathogenic aerobic bacterial strains, which show a continuous flux in the gut. In contrast, exclusively breastfed Swedish infants show a stable, more slowly developing intestinal flora, dominated among the aerobes mostly by a single strain of E. coli or sometimes Klebsiella [26]. This difference in the diversity of the enterobacterial flora in breastfed and non-breastfed infants has also been seen in other countries in Europe [27]. Certain E. coli may be favoured by breastfeeding, and so is their expression of the adhesin called type 1 fimbriae [28],* which, in contrast to other E. coli adhesins, is not associated with virulence. This may be due to the fact that type 1 fimbriae bind directly to mannose residues on phagocytes, which promote phagocytosis [29]. Other adhesins that may function as virulence factors seem to be suppressed by breastfeeding.

It is obvious that various milk factors can prevent adhesion of certain E. coli to host tissues, presumably influencing the immune response. One example is shown in figure 1. Among such anti-adherence substances in milk are SlgA antibodies and various analogues to epithelial receptors that bind Vibrio cholerae, E. coli [30], V. cholerae enterotoxin [31], pneumococci, and H. influenzae [32]. Recently, a milk component, presumably a glucosaminoglycan, has been shown to inhibit the binding of human immunodeficiency virus (HIV) to its CD4 receptor on lymphocytes [33]. The continuous exposure of E. coli to milk components in the gut of the breastfed infant induces continuous changes of surface structures presumably tied to decreasing virulence [34].

Breastfed infants have higher counts of Staphylococcus aureus, S. epidermidis, and enterococci in the gut than nonbreastfed infants [35-37]. In contrast, breastfed infants do not have higher counts of bifido-bacteria, as is often presumed [38].

It seems likely that the immune response may differ in breastfed infants, who have a stable intestinal flora in which the aerobes are dominated by E. cold of little or no virulence, and non-breastfed infants, who have a variable flora containing various pathogens and who therefore are at high risk of diarrhoea and other infections. It could also be that various milk components modify the exposure to certain antigens or their presentation to the infant's immune system.

 

Human milk is anti-inflammatory

Mother's milk contains a number of anti-inflammatory factors with anti-oxidant activity that are able to block chemotaxis of granulocytes and inhibit production of free radicals, peroxidase, and so forth [39]. It is possible that these functions may enhance the well-being of the neonate by preventing inflammation. The neonate is colonized with gram-negative bacteria producing endotoxins in the gut that may induce the production of inflammatogenic, catabolic, and appetite-reducing cytokines such as interleukin1 (IL-1), IL-6, and tumour necrosis factor-a (TNF-a). This cytokine production may be prevented by capacities of the breastmilk. which may be one explanation why non-breastfed infants lose significantly more weight during the first week of life than those exclusively breastfed [40]. In this connection, it is interesting that human milk lactoferrin, a major milk protein, can block endotoxin-induced IL-6 release from human cells [41]. On the other hand, a similar effect is obtained with undenatured bovine millk lactoferrin and its bactericidal peptide lactoferricin.

Human milk contains cytokines such as IL-1, TNF-a, IFN-g , IL-6, transforming growth factor-(TGF-. and IL-10 [42-44]. Cytokine production can be induced from milk cells as well. Thus, the milk T cells can produce IL-2, IL-3, IL-4, IL-10, IFN-g , and TNF-a [45], and the macrophages can produce IL-1a IL-1p, IL-lra (IL-1 receptor analogue), IL-6, IL-8, and IL-10. It is presently unknown whether all these cytokines, with capacities to strikingly influence immune responses, can also have such effects on the breastfed infant's immune reactivity. It is likely that their presence and potential activities are under strict control. The cytokine-modulating effect of lactoferrin mentioned above may be an example of such a control function.

 

Acknowledgements

Our studies have been supported by the Swedish Agency for Research Cooperation with Developing Countries and the Swedish Medical Research Council (no. 215).

A combined discussion of this paper and the paper by Victora can be found after Victora's paper on page 397.



FIG. 1. Diagram showing that defatted colostrum can prevent adherence of Escherichia cold strains with certain adhesins to a colonic epithelial cell line

 

References

1. Goldblum RM, Hanson LA, Brandtzaeg P. The mucosal defence system. In: Stiem RT, ed. Immunologic disorders in infants and children. 4th ed. Philadelphia, Pa USA: WB Saunders, 1996:159-99.

2. Hahn-Zoric M, Fulconis F. Minoli I, Moro G. Carlsson B. Bger M, R. Hanson LA. Antibody responses to parenteral and oral vaccines are impaired by conventional and low protein formulas as compared to breast-feeding. Acta Paediatr Scand 1990;79:113742.

3. Pabst HF, Spady DW. Effect of breast-feeding on antibody response to conjugate vaccine. Lancet 1990;336: 269-70.

4. Hahn-Zoric M, Carlsson B. Jeansson S. Ekre O. Osterhaus AD, Roberton, DM, Hanson LA. Anti-idiotypic antibodies to poliovirus in commercial immunoglobulin, human serum and human millk. Pediatr Res 1993; 33:47580.

5. Stein KE, Sstr. Neonatal administration of idiotype or anti-idiotype primes for protection against Escherichia cold K13 infection in mice. J Exp Med 1984;160:1001-11.

6. Carver JD, Pimentel B. Cox Wl, Barness LA. Dietary nucleotide effects upon immune function in infants. Pediatrics 1991;88:359-63.

7. Siliverdahl R. Bodin L, Hugosson S. Garpenholt Werner B. Esjr E, Lindqvist B. OlcP. Protective effect of breastfeeding on invasive Haemophilus inluenzae infection: a case control study in Swedish preschool children (submitted for publication).

8. Ogra SS, Weintraub D, Ogra PL. Immunologic aspects of human colostrum and milk. III. Fate and absorption of cellular and soluble components in the gastrointestinal tract of the newborn. J Immunol 1977;119:245-8.

9. Schlesinger JJ, Covelli HD. Evidence for transmission of lymphocyte response to tuberculin by breast-feeding. Lancet 1977;2:529-32.

10. Pabst H. Grace M, Godel J. Cho H. Spady D. Effect of breastfeeding on immune response to BCG vaccination. Lancet 1989;1:295-7.

11. Deroche A, Nepomnaschy 1, Torello S. Goldman A, Piazzon 1. Regulation of parental alloreactivity by reciprocal F1 hybrids. The role of lactation. J Reprod Immunol 1993;23:235-45.

12. Campbell DA, Lorber Ml, Sweeton JC, Turcotte JG, Niederhuber J. Beer AK. Breast-feeding and maternal-donor renal allografts. Transplantation 1984;37:3404.

13. Jain L, Vidyasagar D, Xantou M, Ghai V, Shimada S. Blend M. In vivo distribution of human milk leukocytes after ingestion by newborn baboons. Arch Dis Child 1989;64:930-3.

14. Dosch HM, Martin JM, Robinson BH, Akerblom HK, Karjalainen J. An immuno basis for disproportionate diabetes risks in children with a type I diabetic mother or father. Diabetes Care 1993;16:949-51.

15. Davis MK, Savitz DA, Grauford B. Infant feeding in childhood cancer. Lancet 1988;2:365-8.

16. Koletzko S. Sherman P. Corey M, Griffiths A, Smith C. Role of infant feeding practices in Crohn's disease in childhood. BMJ 1989;298:1617-8.

17. Chiba Y. Minagawa T. Mito K, Nakane A, Suga K, Honjo T. Nako T. Effect of breast-feeding on responses of systemic interferon and virus-specific Iymphocyte transformation in infants with respiratory syncytial virus infection. J Med Virol 1987;21:7-14.

18. Goldblum RM, Schandler RJ, Garza C, Goldman AS. Human milk feeding enhances the urinary excretion of immunologic factors in low birth weight infants. Pediatr Res 1989;25:184-8.

19. Howie PW. Protective effect of breastmilk against infection. Food Nutr Bull 1996;17:373-83.

20. Almroth SG. Water requirements of breast-fed infants in a hot climate. Am J Clin Nutr 1978;31:1154-7.

21. Ashraf RN, Jalil F. Hanson LA, Karlberg J. Giving water during breastfeeding affects diarrhoeal incidence and early short term growth in a poor environment. Acta Paediatr (in press).

22. Wiedermann U. Dahlgren U. Holmgren J. Hanson LA. Impaired mucosal antibody response to cholera toxin in vitamin Adeficient rats immunized with oral cholera vaccine. Infect Immun 1993;61:3952-7.

23. Wiedermann U. Hanson LA, Kahu H. Dahlgren U. Aberrant Tcell function in vitro and impaired T-cell dependent antibody response in vivo in vitamin A-deficent rats. Immunology 1993;80:581-6.

24. Wiedermann U. Hanson LA, Bremell T. Kahu H. Dahlgren U. Increased translocation of Escherichia cold and development of arthritis in vitamin A deficient rats. Infect Immun 1995;63:3062-8.

25. Khan S. Jalil F. Zaman S. Lindblad BS, Karlberg 1. Early child health in Lahore, Pakistan: X. Mortality. Acta Paediatr Suppl 1993;390:109-17.

26. Adlerberth 1, Carlsson B. de Man P. Jalil F. Khan SR, Larsson P. Mellander L, Svanborg C, Wold AK, Hanson LA. Intestinal colonization with Enterobacteriaceae in Pakistani and Swedish hospital-delivered infants. Acta Paediatr Scand 1991;80:602-10.

27. Orskov F. Biering-Sorensen K. Escherichia cold serogroups in breast-fed and bottle-fed infants. Acta Pathol Microbiol Scand B 1975;83:25-30.

28. Lodinova ZR, Slavikova M, Tlaskalova HH, Alderberth 1, Hanson LA, Wold A, Carlsson B. Svanborg C, Mellander L. The antibody response in breast-fed and non-breast-fed infants after artificial colonization of the intestine with Escherichia cold 083. Pediatr Res 1991; 29:396-9.

29. Bar-Shavit Z. Goldman R. Ofoh 1, Sharon N. Mirelman D. Mannose-binding activity of Escherichia cold a determinant of attachment and ingestion of the bacteria by macrophages. Infect Immun 1980;29:41724.

30. Holmgren J. Svennerholm AM, AhrCH. Nonimmunoglobulin factors in milk inhibit bacterial adhesions (haemagglutination) and enterotoxin binding of Escherichia cold and Vibrio cholerae. Infect Immun 1981; 33:136-41.

31. Lagreid A, Kolsto-Otnaess AB. Trace amounts of ganglioside GM1 in human milk inhibit enterotoxins from Vibrio cholerae and Escherichia coli. Life Sci 1987;4:55-62.

32. Andersson B, Porras O, Hanson LA, LaBergard T, Svanborg EC. Inhibition of attachment of Streprococcus pneumoniae and Haemophilus inpuenzae by human milk and receptor oligosaccharides. J Infect Dis 1986;153:232-7.

33. Newburg DS, Viscidi RP, Ruff A, Yolken RH. A human milk factor inhibits binding of human immunodeficiency virus to the CD4 receptor. Pediatr Res 1992;31:22-8.

34. Gothefors L, Olling S, Winberg J. Breastfeeding and biological properties of fecal E. cold strains. Acta Paediatr Scand 1975;64:807-11.

35. Balmer SE, Wharton BA. Diet and faecal flora in the newborn: breastmilk and infant formula. Arch Dis Child 1989;64:1672-7.

36. Lundeqvist B, Nord CE, Winberg J. The composition of the faecal microflora in breastfed and bottle fed infants from birth to eight weeks. Acta Paediatr Scand 1985;74:45-51.

37. Simhon A, Douglas JR, Drasar BS, Soothill JF. Effect of feeding on infants' faecal flora. Arch Dis Child 1982;57:54-8.

38. Wold A, Hanson LA. Defence factors in human milk. Curr Opin Gastroenterol 1994;10:652-8.

39. Goldman AS, Goldblum RM, Thorpe LW, Hanson LA. Antiinflammatory properties of human milk. Acta Paediatr Scand 1986;75:689-94.

40. Rassin DK, RC, Minoli 1, Moro G. Taurine and cholesterol supplementation in the term infant: responses of growth and metabolism. J Parenter Enteral Nutr 1990;14:3927.

41. Mattsby-Baltzer 1, Roseanu A, Motas C, Elverfors J. Engberg 1, Hanson LA. Lactoferrin inhibits the endotoxin-induced IL6 response in human monocytic cells. Paediatr Res (in press).

42. Bocci V, von Bremen K, Corradeschi F. Franchi F. Luzzi E, Paulesu L. Presence of interferon-[y ] and interleukin-6 in colostrum of normal women. Cytokine Res 1993;12:21-4.

43. Rudloff HE, Schmalstieg FC, Mustaha AA, Palkowetz KH, Liu KS, Goldman AS. Tumor necrosis factor-a in human milk. Paediatr Res 1992;31:29-33.

44. S 0. Isolation of interleukin-1 from human milk. Int Arch Allergy Appl Immunol 1987;83:19-23.

45. Skansen-Saphir U. Lindfors A, Andersson U. Cytokine production in mononuclear cells of human milk studied at the single-cell level. Pediatr Res 1993;34:213-6.

Infection and disease: The impact of early weaning

Cesar G. Victora

 

Abstract

Although the protective effect of breastfeeding against infectious diseases has been long suspected, it has only recently been adequately quantified This article reviews the available epidemiologic evidence. Breastfeeding provides marked protection against diarrhoeal morbidity and severity (as measured by its duration, level of dehydration, or case-fatality rate), and mortality. This is true for acute watery diarrhoea as well as for dysentery and persistent diarrhoea. A dose-response pattern is observed: the risk level for children receiving both breastmilk and artificial milk is between that of exclusively breasfed children and that of completely weaned children. Even the introduction of water or herbal teas to a previously exclusively breasfed infant increases the risk of morbidity and mortality. The protection is greatest for young infants, and the period immediately after weaning seems to carry the highest risk. Although breastfeeding does not seem to have an appreciable effect on the incidence of acute respiratory infections as a whole, there is evidence of an effect on the incidence of pneumonia, on the incidence of hospitalization for pneumonia, and on mortality from respiratory infections. The level of protection against pneumonia, however, is lower than that against diarrhoea. Breastfeeding also protects against onus media and other infections, including neonatal sepsis, meningitis, and bacteraemia, although the number of relevant studies is small. A simulation exercise shows that a 40% reduction in the prevalence of nonbreastfeeding would prevent up to 15% of diarrhoea deaths and 7% of pneumonia deaths occurring in regions with a short breastfeeding duration, such as urban Latin America. In regions where breastfeeding durations are longer, the emphasis should be on maintaining these high rates and increasing the proportion of young infants who are exclusively breastfed. The present review confirms that breastfeeding promotion is an essential child survival strategy.

 

Introduction

The protective effect of breastfeeding against infectious diseases has long been known. Several studies from Europe in the eighteenth and nineteenth centuries indicated that nonbreastfed infants were two to three times more likely to die than those who were breastfed [1, 2]. In the last 10 to 20 years, however, there has been a resurgence of interest in breastfeeding, and a large number of new studies have been produced.

Recent studies have shown improvements in sampling and in the operational diagnoses of different infectious diseases, as well as in data processing and analysis. In addition, a number of recent publications have addressed key methodological issues that may distort the findings of studies of breastfeeding and disease [3-6]. These issues include self-selection, reverse causality, and confounding.

Self-selection may occur when infants are weaned because they were not thriving on breastmilk. Those who continue to be breastfed, therefore, may represent a subgroup of particularly healthy infants. Reverse causality takes place when an infection leads to weaning, rather than the opposite. Confounding results when early weaning is associated with demographic, socio-economic, or environmental characteristics that may also affect morbidity. Such confounding factors may lead to a spurious association between breastfeeding and protection from infection. Some recent studies have attempted to avoid these pitfalls through specific improvements in their design and analysis [5]. Unless otherwise noted, the studies reviewed here were adjusted for confounding variables. Several investigators have also attempted to account for reverse causality and self selection.

Virtually all studies of breastfeeding and infection have observational designs, such as case-control, cohort, or crosssectional studies. Intervention trials would solve many of the methodological problems inherent to these designs, but the random allocation of mothers and infants to a breastfeeding or a control group is not ethically justified. In addition, ensuring compliance with a recommended feeding practice is extremely difficult, and the sample sizes required for studies with morbidity outcomes, in the presence of low compliance, would be enormous.

Another problem is that studies have addressed different types of disease outcomes. Some investigators have studied overall morbidity from, for example, diarrhoea or respiratory infections. Others have concentrated on more severe diseases, such as persistent or dehydrating diarrhoea or pneumonia. Finally, some studies have assessed mortality. The risk factors for acquiring an infectious disease may be quite different from the prognostic factors leading to a severe episode and finally to death. Therefore, an apparent lack of consistency between different studies may be due to the fact that different disease outcomes were being investigated.

Other participants in this Workshop have addressed the mechanisms through which breastfeeding protects against infections, as well as the epidemiologic literature from developed countries. I will concentrate on the epidemiologic evidence supporting this protective role, based on studies from less-developed countries. It is important to separate studies from developed and less-developed areas, because the effects of breastfeeding are modified by a number of socio-economic, environmental, and dietary factors. For example, greater protection is likely to occur where there is poverty, crowding, or unsafe drinking water or where weaning foods are contaminated or of low energy density. Studies from developed countries, therefore, cannot be extrapolated to the rest of the world.

This review makes no claim to be exhaustive, as a number of comprehensive summaries of the literature on this topic are available [7-12]. Rather, I will use examples from a few investigations-with a strong bias towards studies in which I was involved -to highlight the key epidemiologic and public health issues.

 

Impact on diarrhoea

Feachem and Koblinsky [8] reviewed 35 studies on diarrhoeal incidence from 14 countries. There was a clear protection associated with breastfeeding, but this varied according to the child's age. The relative risks for nonbreastfed infants compared with all those who were breastfed, either exclusively or par tially, were 3.0 up to two months of age, 2.4 at three to five months, and about 1.4 thereafter. According to this review, protection after infancy was not evident.



FIG. 1. Risk of dehydration (odds ratio) from diarrhoea in infants in Brazil in 1992 according to type of milk

Epidemiologic studies show that breastfeeding protects against shigellosis and cholera. Breastmilk also contains antibodies against a large number of other gastrointestinal pathogens [13]. It also protects against neonatal necrotizing enterocolitis [14].

Breastfeeding appears to provide even higher protection against more severe forms of diarrhoea. In a study we carried out in Brazil, dehydrating diarrhoea (defined by the presence of a persistent skinfold plus at least two other signs of dehydration) was 6.0 times more frequent among non-breastfed infants than among exclusively breastfed infants (fig. 1) [15]. If a child already had diarrhoea, the risk of developing dehydration was 3.3 times greater for the nonbreastfed infant [16].

Another indication of severity is the duration of the diarrhoeal episode. When 400 Brazilian infants were followed from birth to the age of six months, those weaned during the first week of life had a risk of diarrhoea three times greater than those who were exclusively breastfed (including those also receiving water or herbal teas). When the analysis was restricted to episodes of persistent diarrhoea lasting 14 days or more, the relative risk was 5.1.

Yet another indicator of severity is case fatality. In Rwandan children hospitalized with diarrhoea, the casefatality rate was three to four times lower for those who were breastfed [17l. Breastfeeding, therefore, seems to provide even greater protection against severe diarrhoea than against mild diarrhoea.

The evidence from mortality is also compelling. Several studies from the first half of this century showed a protective effect of breastfeeding. For example, Newsholme [18] compared infants who died of "epidemic diarrhoea" in Brighton between 1903 and 1905 with a population-based control group. Reanalysis of his data with logistic regression (fig. 2) shows that after adjustment for age, infants receiving condensed milk were 91 times more likely to die than those on breastmilk. The odds ratio for infants on cow's milk was 40. These relative risks are probably inflated by reverse causality and other biases.



FIG. 2. Risk of death (odds ratio) from diarrhoea in infants in England in 1903-05 according to feeding pattern



FIG. 3. Risk of death (odds ratio) from diarrhoea in infants in Brazil in 1984-85 according to feeding pattern



FIG. 4. Risk of dehydration (odds ratio for incidence) from diarrhoea in infants in Brazil in 1992 according to time since weaning



FIG. 5. Prevalence of diarrhoea (relative risk for percentage of days ill) in infants under two months of age in Peru in 1988 according to feeding pattern. Arrow shows doubling of prevalence when infant receives liquids in addition to breastmilk

Our study from Brazil showed odds ratios for diarrhoeal mortality of 14.2 for totally weaned infants and 4.2 for those on both breastmilk and artificial milk, compared with those on breastmilk alone [19].

Figure 3 shows the results of this study for several feeding patterns. Children receiving only artificial milk were at a particularly high risk. The addition of any supplements, either artificial milk or food, resulted in at least a two- to threefold increase in the risk for breastfed infants.

In this study, deaths were broken down according to the clinical characteristics of the diarrhoeal episode. Nonbreastfed infants were 21 times more likely than exclusively breastfed infants to die of acute watery diarrhoea, 10 times more likely to die of persistent diarrhoea, and 3 times more likely to die of dysentery [20].

The greater vulnerability of young infants was confirmed by this study, because the protection was even higher before two months of age (odds ratio of 23 for the nonbreastfed infant under two months). A related issue is the especially high vulnerability of infants who were recently weaned. Figure 4 shows additional results from the abovementioned study of dehydrating diarrhoea [15, 16]. The risk was highest for infants who had recently been weaned and decreased thereafter.

A major issue raised in the last 10 years is the importance of exclusive breastfeeding for the prevention of diarrhoea. Figure 5 shows the results of a Peruvian longitudinal study in which the percentage of days on which a child had diarrhoea was related to feeding patterns [21]. There was a doubling in the prevalence when the child received liquids such as water or herbal teas in addition to breastmilk. The diarrhoea mortality study from Brazil also showed that each additional fluid feeding resulted in a 40% increase in the risk of death from diarrhoea among breastfed infants [19, 22]. More recently, a study from the Philippines showed that giving fluids to breastfed infants two months of age resulted in a two- to threefold increase in the incidence of diarrhoea [23]. Both the Peruvian and the Filipino studies showed that the benefits of breastfeeding were considerably less after the first six months.

 

Impact on respiratory Infections

Fewer studies have addressed the effect of breastfeeding on respiratory infections. This may be partly because of the difficulties in operationalizing and standardizing the diagnoses of these infections under field conditions.

A recent review of studies from less-developed countries showed that although breastfeeding did not seem to provide important protection against acute respiratory infections as a whole, there was evidence of an effect on the incidence of pneumonia and of hospitalizations for pneumonia, as well as on mortality from respiratory infections [24]. For example, figure 6 shows the results of two recent case-control studies from two Brazilian cities in which the outcome was radiologically confirmed pneumonia [25, 26]. The risks for partially breastfed and non-breastfed children were clearly greater than those for exclusively breastfed children.



FIG. 6. Risk of pneumonia (odds ratio for incidence) in children under two years of age in two Brazilian sites, Porto Alegre and Fortaleza, in 1993-95 according to type of milk



FIG. 7. Risk of otitis media (odds ratio for incidence in last month) in infants six months of age in Brazil in 1993-94 according to duration of breastfeeding



FIG. 8. Incidence of neonatal infections in a randomized trial of human milk (HM) versus formula in India in 1984 [30]

Breastfeeding also affects the case-fatality rate of respiratory infections. In Rwanda non-breastfed children were twice as likely as breastfed children to die of pneumonia [17]. Non-breastfed Brazilian infants were 3.6 times more likely to die of acute lower respiratory tract infections than those who received breastmilk and no artificial milk. Infants receiving both human and artificial milk had an intermediate odds ratio of 1.6 [19, 27].

An interesting but somewhat unexpected finding from two of the Brazilian studies deserves further investigation. Regardless of the type of milk consumed, infants who received non-milk food complements were 2.3 times less likely to develop pneumonia [25] and 3.2 times less likely to die [27].

The protection provided by breastfeeding against otitis media is well established, mostly through studies from developed countries [6, 9]. Figure 7 shows the results of a recent study of six-month-old Brazilian infants [28]. There is a clear gradient in the risk of medically confirmed otitis media in the preceding month, according to the duration of breastfeeding. It is interesting to compare these findings with those shown in figure 4, where the most recently weaned babies showed the highest risk of dehydrating diarrhoea. This contrast, along with the finding that the protection against otitis media is also well documented in developed countries, suggests that the mechanism may involve the anatomical development of the upper respiratory system rather than any environmental risk factors.

 

Impact on other infections

Breastfeeding is known to protect against other infections, including neonatal sepsis, meningitis, and bacteraemia [11, 13]. Despite one study that failed to find protection against mortality from measles [29], the Rwandan study showed that case fatality from measles was reduced by one-third for breastfed infants [17].

The only randomized intervention trial examining the relation between breastmilk and infection that I am aware of was carried out in India. This study compared the effects of different milk combinations given by bottle to high-risk newborns [30]. Septicaemia, conjunctivitis, diarrhoea, and umbilical sepsis were the most common infections observed. Figure 8 shows that there were separate effects of pasteurization and of formula introduction on neonatal infection rates.

The Brazilian case-control study of mortality [19] included deaths from meningitis, skin infections, measles, whooping cough, neonatal sepsis, and tuberculosis. Because of the small number of cases in each category, these were grouped together. Compared with infants receiving breastmilk without any artificial milk, non-breastfed children were 2.5 times more likely to die of these infections. Infants receiving both breastmilk and artificial milk were at lower risk (odds ratio, 0.4), but this difference was not statistically significant.

 

Summary of the evidence

This review began with a discussion of methodological problems affecting observational studies and argued that experimental, community-based studies would in general not be feasible or ethical. The Indian trial described above was an exception, since it was a hospital-based study for highrisk neonates who were all bottle-fed [30]. In some circumstances, however, one may carry out quasiexperimental studies in the community advantage of existing interventions. In the Brazilian city of Guaruja lactation centre has been well established for several years [31]. Mothers giving birth in the city hospitals are invited to join the centre, and about half of them eventually attend at least once. This is obviously not a random process, because mothers who attend may differ from those who do not, but in this study it was possible to interview the mothers in the hospital before they were invited to join the centre and to collect a large amount of baseline data. There were some differences between attenders and non-attenders in social and demographic variables. There were no differences in reported maternal attitudes towards breastfeeding, but attenders were more likely to have received breastfeeding advice during pregnancy. These confounding factors were handled later in the data analysis.

All mothers were followed up until the child was six months old. At four months, 42% of attenders were exclusively breastfeeding, against 12% of nonattenders. At six months of age, after adjusting for the above-mentioned confounding variables, the incidence of diarrhoea in the previous two weeks among non-attenders was 1.7 times that among attenders, a significant difference (fig. 9). Nonattenders also had almost twice as many hospital admissions as attenders for diarrhoea since birth, but this difference was not significant (p = .09). This study brings us closer to an experimental design. Because the comparison is based on attendance and not on successful breastfeeding, reverse causality bias is avoided, as well as some of the self-selection bias (in fact, mothers facing difficulties may be more, rather than less, likely to attend). Self-selection and confounding are further reduced by obtaining prior information about attitudes and practices regarding breastfeeding at the time of delivery, and by adjusting in the analyses for any differences. It is reassuring that the protection provided by breastfeeding against diarrhoea is confirmed in a stricter study design.

The main findings of this review may be summarized as follows. Breastfeeding reduces the incidence of diarrhoea. In addition, for children who have already developed diarrhoea, breastfeeding reduces the severity of the episode, whether measured by duration of the episode, risk of dehydration, or case-fatality rate. As a consequence, breastfeeding strongly protects against diarrhoeal mortality. There is a clear effect of age, with the greatest protection among young infants. There is also evidence that recently weaned infants may be more vulnerable. Although partial breastfeeding results in a reasonable degree of protection against diarrhoea, exclusive breastfeeding for young infants is essential to achieve the highest protection. This is because the mere addition of water or herbal teas to the diet sharply increases the incidence of diarrhoea and mortality due to diarrhoea.

The protection afforded by breastfeeding against respiratory infections is not well established. However, studies from less-developed countries clearly show a protective effect on severe respiratory infections, as measured by the incidence of pneumonia and by hospitalizations and mortality due to respiratory infections. There is also consistent evidence of protection against otitis media. A dose-response trend is clear in several studies, with partially breastfed children having intermediate levels of risk. Nevertheless, the protection is several times smaller than that provided by breastmilk against diarrhoea. This finding is consistent with biological knowledge, because in addition to its systemic effects, breastmilk has a direct effect on the gastrointestinal immune system and flora, as well as leading to the avoidance of possibly contaminated weaning foods.

Evidence of the impact on infections other than diarrhoea and respiratory infections is not as clear-cut, but several studies suggest some level of protection.

On the basis of simulations we recently performed for the World Health Organization [24], our group has calculated the likely impact of breastfeeding promotion on mortality from diarrhoea and respiratory infections, the two major killers of children in the world. Data on three typical populations that differed in the duration of breastfeeding were taken from the WHO Collaborative Study on Breastfeeding (table 1) [32]. Based on the literature, it was estimated that full or partial breastfeeding would lead to a 50% reduction in deaths from respiratory tract infections and a 66% reduction in deaths from diarrhoea among children aged under 18 months. It was further assumed that it would be possible to reduce the prevalence of non-breastfeeding by 40%, a reasonable figure based on results from intervention studies. Table 2 shows the proportions of deaths among infants under five years of age that would be prevented through this intervention.



FIG. 9. Risk of diarrhoea (odds ratio for diarrhoea in the last two weeks) and hospital admission in infants six months of age in Brazil in 1993 in the control and intervention (lactation centre) groups [31]

Breastfeeding promotion would obviously have very limited impact in areas where most children are already breastfed, such as rural Africa, South Asia, and Central America. It would have a substantial impact, however, in areas where early weaning is common. These include many urban and rural areas in South America and South-East Asia as well as some of the largest African cities. These calculations are conservative, because the benefits of partial breastfeeding are not considered, but they serve to illustrate the potential life-saving effect of breastfeeding promotion.

The Bible says, "Blessed is the womb that bore you and the breast that you sucked" (Luke 11:27). Recent research is confirming how correct this statement is.

 

Acknowledgements

I would like to thank my colleagues Sandra Fuchs and Fernando Barros for their contribution to the Brazilian studies reviewed here.

TABLE 1. Percentage of children not breastfed according to age in populations with different durations of breastfeeding

Age (mo)

Duration of breastfeeding

Long

Intermediate

Short

0-5

0%

7%

19%

6-11

2%

16%

40%

12-17

12%

31%

62%

Source: ref.32

TABLE 2. Expected percentage reduction in mortality among children under five years of age resulting from a 40% decrease in the prevalence of non-breastfeeding in populations with different durations of breastfeeding

Cause of death Duration of breastfeeding

Long

Intermediate

Short

Diarrhoea

1.0%

11.6%

14.8%

Pneumonia

0.5 %

3.3 %

7.0 %

 

References

1. Wickes IG. A history of infant feeding. Arch Dis Child 1953;4:233-40, 416-22.

2. Knodel J. Van der Valle E. Breast feeding, fertility and infant mortality. An analysis of early German data. Pop Stud 1967;21:109-31.

3. Habicht JP, DaVanzo J. Butz WP. Does breastfeeding really save lives, or are potential benefits due to biases? Am J Epidemiol 1986;123:279-90.

4. Sauls HS. Potential effect of demographic and other variables in studies comparing morbidity of breast-fed and bottle-fed infants. Pediatrics 1979;64:523-7.

5. Victora CG. Case-control studies of the influence of breastfeeding on child morbidity and mortality: methodological issues. In: Atkinson SA, Hanson LA, Chandra RK, eds. Breastfeeding, nutrition, infection and infant growth in developed and developing countries. St. John's, Canada: ARTS Biomedical Publishers and Distributors, 1990:405-18.

6. Bauchner H. Leventhal JM, Shapiro ED. Studies of breast-feeding and infection. How good is the evidence? JAMA 1986;256:887-92.

7. Jelliffe DB, Jelliffe EFP. Human milk in the modern world. Oxford: Oxford University Press, 1978.

8. Feachem RG, Koblinski MA. Interventions for the control of diarrhoeal diseases among young children: promotion of breastfeeding. Bull WHO 1984;62:271-91.

9. Kovar MG, Serdula MK, Marks JS, Fraser DW. Review of the epidemiologic evidence for an association between infant feeding and infant health. Pediatrics 1984;74:615-38.

10. Jason JM, Nieburg P. Marks JS. Mortality and infectious disease associated with infant-feeding practices in developing countries. Pediatrics 1984;74:702-27.

11. Cunningham AS, Jelliffe DB, Jelliffe EFP. Breastfeeding and health in the 1980s. A global epidemiological review. J Pediatr 1991;118:659-66.

12 Victora CG. Breastfeeding, morbidity and mortality. In: Chandra RK, ed. Proceedings of the Conference on Nutrition and Immunology. St. John's, Canada: ARTS Biomedical Publishers and Distributors, 1992: 63-72.

13. Hanson LA, Ashraf R. Carlsson B. Mattsby-Baltzer I, Motas C, Hahn-Zoric M, Mata L, Herias V, Cruz JR, Lindblad BS, Karlberg J, Jalil F. The Second John Soothill Lecture: breastfeeding, infections and immunology. In: Chandra RK, ed. Nutrition and immunology. St. John's, Canada: ARTS Biomedical Publishers and Distributors, 1992:45-60.

14. Lucal A, Cole TJ. Breast milk and neonatal necrotizing enterocolitis. Lancet 1990;336:1519-23.

15. Fuchs SC. Risk factors for dehydrating diarrhea: a case-control study. Ph.D. thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil, 1993.

16. Victora CG, Fuchs SC, Kirkwood BR, Lombardi C, Barros FC. Breastfeeding, nutritional status and other prognostic factors for dehydration among young children with diarrhoea: a casecontrol study. Bull WHO 1992;70:467-75.

17. Lepage P. Munyakazi C, Hennart P. Breast feeding and hospital mortality in children from Rwanda. Lancet 1981;i:40911.

18. Newsholme A. Domestic infection in relation to epidemic diarrhoea. J Hyg 1906;6:139-48.

19. Victora CG, Smith PG, Vaughan JP, Nobre LC, Lombardi D, Teixeira AM, Fuchs SC, Moreira LB, Gigante LP, Barros PC. Evidence for a strong protective effect of breast-feeding against infant deaths due to infectious diseases in Brazil. Lancet 1987;2:319-22.

20. Victora CG, Huttly SR, Fuchs SC, Nobre LC, Barros FC. Deaths due to dysentery, acute and persistent diarrhoea among Brazilian infants. Acta Paediatr 1992; S381:7-11.

21. Brown KH, Black RE, Romana GL, Kanashiro HC. Infant feeding practices and their relationship with diarrhea and other diseases in Huascar (Lima), Peru. Pediatrics 1989;83:3140.

22. Victora CG, Smith PG, Vaughan JP, Nobre LC, Lombardi D, Teixeira AM, Fuchs SC, Moreira LB, Gigante LP, Barros PC. Infant feeding and deaths due to diarrhoea: a case-control study. Am J Epidemiol 1989;129: 103241.

23. Popkin BM, Adair L, Akin JS, Black R. Briscoe J. Flieger W. Breastfeeding and diarrhea! morbidity. Pediatrics 1990;86:87482.

24. Victora CG, Kirkwood BR, Ashworth A, Black RE, Rogers S. Sazawal S. Campbell H. Gove S. Interventions for preventing pneumonia among young children: nutritional risk factors. Geneva: WHO, Child and Health Development Division, 1996.

25. Victora CG, Fuchs SC, Flores A, Fonseca W. Kirkwood B. Pneumonia among Brazilian children: a hierarchical analysis. Pediatrics 1994;93:977-85.

26. Fonseca W. Kirkwood BR, Victora CG, Fuchs SC, Flores JA, Misago C. Risk factors for childhood pneumonia among the urban poor in Fortaleza, Brazil: a case-control study. Bull WHO 1996;74:199-208.

27. Victora CG, Smith PG, Vaughan JP, Barros FC, Fuchs SC. Risk factors for deaths due to respiratory infections among Brazilian infants. Int J Epidemiol 1989;18:901-8.

28. Amaral JJF. Prevalencia e fatores de risco pare infec respirat aguda em crian aos seis meses de vida em Pelotas. Master's dissertation, Universidade Federal de Pelotas, Brazil, 1995.

29. Aaby P. Bukh J. Lsse IM, Smits AJ, Smedman L, Jeppsson O. Lindeberg A. Breastfeeding and measles mortality in GuineaBissau. Lancet 1981;ii:1231.

30. Narayanan I, Prakash K, Munthy NS, Gujral W. Randomized controlled trial of effect of raw and pasteurized human milk and of formula in the incidence of neonatal infection. Lancet 1984;ii:1111-3.

31. Barros FC, Semer TC, Tonioli Filho S. Tomasi E, Victora CG. The impact of lactation centres on breastfeeding patterns, morbidity and growth: a birth cohort study. Acta Paediatr 1995;84:1221-6.

32. World Health Organization. Contemporary patterns of breastfeeding. Geneva: WHO, 1981:31-8.

Discussion of papers by Hanson et al. And by Victora

 

Dr. McLaren

I have two questions. The first is for Professor Hanson. I was very interested in your data on type I diabetes. You showed that the genetic component was inherited from the father two or three times more often than from the mother, and that the risk was twofold more in bottle-fed than in breastfed babies. It would be very interesting to know whether the risk was equally from the father and the mother in the bottle-fed babies. In other words, it would be helpful if you could separate out the bottle-fed and the breastfed and look at the inheritance from the father and the mother. My guess is that this hasn't been done, or you would have told us. If it turned out to be equally inherited from the father and the mother, then it would support your interpretation. I also wonder whether other autoimmune factors have been looked at, because more and more diseases today seem to be autoimmune in character.

Professor Hanson

You are right. That analysis has not been done. The origin of the interest in this study was that the inheritance from the father and the mother differed, and that the difference may be at least partially attributed to the mother's breastfeeding. There is a large Finnish-Canadian study examining the possibility that bovine milk proteins may be part of the initiation of the autoimmune process, but this is still an open question. As for other autoimmune diseases, some have been discussed, but there are no data yet. The results of experimental studies in newborn mice administered, via the milk, cells from the mother with the same transplantation antigen as the father showed a modifying effect on the reactivity of the offspring against the paternal transplantation antigen. Obviously, maternal cells in the milk can influence normal as well as abnormal immune responses in the offspring. I very briefly mentioned

Crohn's disease, whose origin is unknown, but we know that cytokines are involved in the inflammation in the gut. Obviously, the motherinfant relationship through breastfeeding is not just passive, as we used to think; it is also active. The fact that vaccine responses are enhanced and transplant rejection is diminished is quite significant.

Dr. McLaren

My second question is more general and is relevant also to Dr. Victora. It arises from something that Professor Hanson said about the greater risk of gastrointestinal infection among the babies in Pakistan who had extra water. I had always thought that during very hot weather, both in Pakistan and in England, babies actually needed water as well as breastmilk. Perhaps that is wrong, but if it isn't wrong, then did babies in Pakistan who did not get extra water have some other deleterious consequence? In other words, is extra water needed when it is very hot?

Professor Hanson

There have been a number of studies showing that the extra water is not necessary. We have investigated this in Pakistan during the hot and dry season, and considering the concentration capacity of the kidney, extra water is totally unnecessary. It just brings the risk I suggested; if you give the baby water during the hot season, it will suck less, and less milk is produced. I would strongly discourage this, as it brings increased risk of infection. Last summer was very warm in Sweden, up to 30° to 35°C, and the newspapers erroneously stated that one must give extra water to breastfed infants. This is a very common belief, and in many traditional societies the mothers say, "Oh, yes, you have to give extra water." This has very unfortunate consequences in poor countries with a high risk of infection, especially during the hot season, as we have shown an increased number of episodes of diarrhoea and impairment of short-term linear growth, even of head circumference.

Dr. Victora

I have nothing to add to Professor Hanson's comment.

Dr. Garza

I would like to add a slight modification to what Professor Hanson has said, which I think you would agree with. Although what Professor Hanson has said is certainly true of breastfed infants, because the renal challenge of human milk is so low, that is not true of children who are fed substitutes, because the renal challenge is high enough that those children do need extra water. It is very important that we do not leave here thinking that all infants regardless of how they are fed don't need extra water. I realize that does not contradict what you said earlier.

Dr. Prentice

I just wanted to add to that the case in support of prolonged breastfeeding, because that also seems to provide water for children for long periods. Studies in Bangladesh and elsewhere have shown that the severity of dehydrating diarrhoea is reduced in children who are still receiving breastmilk in the second year of life, showing that it is a very important source of clean water.

Dr. Rasmussen

I wish to put a question to Dr. Victora. In your presentation you seemed to indicate that there was a period after the end of breastfeeding when the infant was particularly vulnerable. Yet we have heard elsewhere, particularly from Professor Howie, that the positive benefits of breastfeeding seem to go on for some period of time, and there are others who have reported the same finding. Those reports don't seem to be in accord.

Dr. Victora

They don't seem to me to be in accord, either. I think we always run the risk of lumping together all infections and different parts of the world in our breastfeeding studies. There are so many variables that may affect how breastfeeding may or may not protect under certain circumstances. Therefore I don't think it is a surprise that we find apparently contradictory results. We found particularly strong evidence of a vulnerable period for dehydrating diarrhoea for three months after weaning. If, however, we look at diarrhoea mortality as a whole, there is no evidence of a vulnerable period by the other case-control study I presented. Overall, 62% of those deaths were due to persistent diarrhoea, so that we are talking about different syndromes with different pathophysiologies. It may well be that this vulnerable period is present for some infections but not for others. I would like to see more studies separating the different clinical types of diarrhoea to see whether this is confirmed. You may remember that my findings regarding otitis media were quite different, showing a long carry-over effect of breastfeeding, so that we are talking about entirely different things.

Dr. Colombo

Dr. Victora, if I did not understand well, it is because my English is limited. You spoke of a survey in which you started from the death of the infant in the hospital, and then you went back to get information and calculated rates of mortality. What are the numerator and the denominator of these rates?

Dr. Victora

The study was not only hospital-based. Eighty-five per cent of the deaths occurred in the hospital, but the data on the other 15% came from cemetery registries or from other registration offices. I have calculated the odds ratios from the case-control study: for example, the cross-product ratio in a two-by-two table of exposure against disease. These odds ratios correspond mathematically to the incidencedensity ratios. We could actually have shown the population rates, because the entire population was under surveillance, but in that particular presentation only the relative risks or odds ratios are changed.

Dr. Garza

You concentrated most of your comments on the impact of early weaning. Would you care to comment on the effects of delayed weaning? I know you have studied this in the past, but do you have any recent data that would help us evaluate how long breastfeeding is protective?

Dr. Victora

No, I don't. My studies go up to two years of age, and I can find a protective influence on infection up to that age.

Dr. Garza

What about the nutritional status?

Dr. Victora

The nutritional status studies we have carried out tend to show that at some stage around one year of age, children who are no longer breastfed tend to grow faster than those who are breastfed, showing, therefore, an inverse association between growth and breastfeeding. Again, there are many caveats because this varies from society to society. Dr. Prentice recently reviewed work from China showing the opposite trend. I guess my reading of the literature on breastfeeding during the second year is that most studies show this inverse association, that is, breastfed babies grow less rapidly than babies who are not breastfed. Nevertheless, there may be a number of confounding variables, self-selection and other factors that may affect the association. On the other hand, all the studies on mortality or infection in relation to breastfeeding in the second year of life tend to show a positive effect, although not all of them are significant, as Dr. Menken mentioned yesterday. So, we have this dilemma in the second year, whether this poorer growth is enough to justify any policy change. My feeling is that the positive effects of breastfeeding are greater than the negative ones.

Dr. Garza

When you say growth, do you mean weight-for-age, lengthfor-age, or both?

Dr. Victora

Different studies have looked at different things. My own studies have shown a greater effect on weight-for-length, but there are studies from other countries showing effects on length-for-age as well.

Professor Hanson

You say they grow more, but do you know what is optimal growth? Another question concerns your mentioning the lasting effects of breastfeeding. I do not think I have made myself clear on that point. The newborn would have relatively few Iymphocytes with which to respond against different microorganisms. Breastfeeding obviously enhances the response, and the result is that there will be many more lymphocytes in the baby to respond to each micro-organism, which means that there will be a lasting effect, because next time the immune response will have many more cells to respond with and will be more efficient. This would be a lasting effect of the immune enhancement from breastfeeding.

Dr. Prentice

I want to get some clarification from Dr. Victora about the effects he sees up to two years. Do you mean you see effects in children who are still receiving milk for two years or in those who were exclusively breastfed for three months and showed effects for two years afterwards?

Dr. Victora

No, I was referring to children who were still receiving breastmilk in the second year of life.

Professor Howie

May I ask Professor Hanson a question? I was very impressed by your data that showed lower responses to immunization in formula-fed than in bottle-fed babies. My question is whether this leads to any suggestion that bottlefed babies with lower antibody responses are more prone to the relevant diseases, or are the levels of response still sufficient to mount protection? This could obviously be important for diseases such as tuberculosis in Africa, where the HIV epidemic is expressing itself very strongly as an increased incidence of tuberculosis.

Professor Hanson

That is a very good question. Let me first say that the control groups were really two groups on different formulas, feeding at different protein levels. There was no difference between those two, but the breastfed group did better. Now, your question, of course, requires that we know the protective level of the antibodies we measure. That is known for just a few infections, like rabies and Haemophilus infuenzae-type infections. Actually, we also know the protective level for diphtheria toxin antibodies, so there we could find an answer for you, but, otherwise, I think we have to rely on the general principle that more antibodies give a better chance of protection. On the other hand, I should add another observation we made with Dr. Cruz of INCAP (Institute of Nutrition of Central America and Panama) in Guatemala. If the mother is infected with diarrhoeal agents during pregnancy, the antibodies she has in her milk against certain pathogens come down during the period of infection. Then they return again. This may mean that it is important to prevent maternal infection during lactation, so that the protection of the breastfed infant does not decrease. We know the protection of the breastmilk relates to the amount of secretory IgA antibody to cholera bacteria and toxin and to Shigella, Campylobacter, and so forth.

Dr. Garza

Professor Howie's question related to the quantity. I know that you have also looked at the quality of the antibody in mother's milk in relation to the mother's nutritional status. Are there any differences in the quality of the antibodies that are made by breastfed and bottle-fed infants, in terms of avidity and other properties?

Professor Hanson

What a nice question. I don't know the answer, but avidity is the capacity of the antibody to bind. The more effectively it binds, the better it neutralizes toxins, and the better it may protect. I don't know the answer, because nobody has done the study, which needs to be done. Nevertheless, we have shown that moderate undernutrition of the mother does not impair the avidity of the milk antibodies.

Dr. Rasmussen

I have a question for Professor Hanson that is off the subject of lactation. What you said this morning would cause me to revise my teaching in maternal health, so I wish to be clear about what you said. You contended that the immune system controls pregnancy, if I am paraphrasing you correctly. I would like you to confirm exactly what you said, and ask you what mechanisms may be involved.

Professor Hanson

Two years ago I would not have believed this new concept. There are a number of animal studies, and now more and more human studies, to support the conclusion that the cytokines from the maternal-antipaternal immune response are a driving force during pregnancy. Thus, the trophoblasts are stimulated to grow primarily by interleukin-3 (IL-3) and granulocyte-colony stimulating factor (G-CSF). They stimulate placental formation. The decidua is prepared by cytokines to receive the blastocyst. Cytokines induce the production of human chorionic gonadotrophin (hCG) and progesterone, as well as placental prolactin. Cytokines finally induce the production of the prostaglandins that result in delivery. IL-8 comes in both at menstruation and at delivery, so that a lot of neutrophils come in, surely to defend the bleeding surfaces open to infections, but also to provide the collagenase that opens up the cervix. IL-6 induces the baby to produce surfactant protein A. It all comes together in a most remarkable way. This is the positive side, with an overweight of TH2 cells driving and protecting pregnancy by production of IL-3, IL-4, IL-5, IL6, and IL-10. If there is a predominance of the TH1 cells stimulated by IL-12, then there may be too much interferony on tumour necrosis factor-a (TNF-a), resulting in intrauterine growth retardation or even abortion. IL-10 can down-regulate the TH1 cells to produce less interferon-y. So the question is obvious: can we demonstrate intrauterine growth retardation that can be prevented by IL-10? Of the 20% of children with low birthweight in Pakistan, 75% have intrauterine growth retardation, and in India the figures are even higher.

Breastfeeding child development

Ernesto Pollitt and Patricia Kariger

 

Abstract

The literature reviewed in this article suggests that breastfeeding positively influences cognitive development. Studies comparing the effects of early feeding methods on cognition consistently show mental test score advantages for breastfed infants over bottlefed subjects. Also, breastfeeding may function as a buffer against adverse developmental outcomes from early traumatic events such as low birthweight or neurologic insults. It is recognized that breastmilk contains long-chain polyunsaturated fatty acids that are necessary for the normal development of the retina and cerebrum. Yet, breastfeeding may not always promote optimal development in children. Infants breastfed by mothers using alcohol or marijuana have lower scores on developmental tests. Thus, while breastfeeding has the potential for contributing to the healthy development of infants, it may also be capable of transferring toxic substances known to interfere with normal development.

 

Introduction

Human biology and psychology provide support for the hypothesis that breastfeeding benefits mental development. On the one hand, biochemical components of breastmilk affect particular elements of the neural circuitry that contribute to information processing [1-3]. On the other hand, in addition to the emotional ties that arise between mother and infant from suckling, it is plausible that breastfeeding helps the development of interpersonal communication between infant and caretaker [4].

Several lines of research bear on the issue of the effects of breastfeeding on mental development.

The most obvious is the search for a direct relationship between the presence or absence of breastfeeding, at one end, and measures of cognition, at the other end. A second line, which has received little attention in the literature, refers to breastfeeding as a primary or secondary preventive agent. Finally, there is research that raises a caveat to the idea that breastfeeding can do no wrong. At issue is whether breastfeeding could operate as a developmental risk factor by the transfer of toxic elements such as alcohol that could limit mental development.

 

Direct effects of breastfeeding

Several studies have attempted to test the hypothesis that breastfeeding gives infants developmental advantages over those who are bottle-fed. Limitations in research design prevented most of these studies from carrying out a fair test of the hypothesis. By definition, correlational studies do not address issues of causality because of the uncertainty that all potential confounders have been controlled for.

Because developmental scales that are used to test infants and toddlers do not assess the same psychological constructs as those assessed by intelligence tests administered to older children, we have separated studies of infants and toddlers from the remaining studies. Longitudinal studies that include assessments at both ages were placed in both age groups.

Infants and toddlers (table 1)

Five studies [5-9] are included in this group. All used the Bayley Scale of Mental Development for the developmental assessment. Because the study by Rogan and Gladen [7] also included evaluations with the McCarthy Scales at three, four, and five years of age, we included their later results in the following section.

The definition of the independent variable (feeding method) varies among the studies and prevents pooling the data to draw any generalizations. For example, the number of types of feeding methods ranges from two [6] to five [7]. Likewise, the nutrient composition of the formulas given to the bottlefed babies was generally not reported, and the nature and number of potential confounders accounted for and the socio-economic status (SES) of the subjects varied among studies.

TABLE 1. Studies of the effect of breastfeeding on development in infants and toddlers

Study Study design Sample Exclusion criteria Outcome variables Significant results
Temboury et al., 1994 [6] Prospective, longitudinal, correla- tional study Cognitive development measured once between 18 and 29 mo Data on background variables Collected when subject was tested Subjects classified by method of Feeding: bottle, breastfed < I mo (n = 99); breast, breastfed 23 mo (n = 130) 229 newborns from Madrid hospitals; about half middle and half lower SES Gestational age <36 wk Birthweight <2,400 g Perinatal complica- tions Major birth anoma- lies Poor 5-min Apgar score Breastfed for 2 mo Follow-up testing not completed Bayley MDI and PDI scores at 18-29 mo Covariates: Maternal education, age, working status SES No. of siblings Psychosocial risk Testers also coded for shyness, temper tantrums, hyperactivity Low MDI scores at 18-29 mo were predicted by:
  R P
bottle-fed low maternal 1.86 .044
education 2.90 .012
no. of siblings 2.63 .002
tantrums 2.38 .016
 
Rogan & Gladen, 1993 [7] Prospective, longitudinal, correla- Tional study Mothers interviewed about feeding Methods from birth to 5 yr Cognitive development measured at 6, 12, 18, and 24 mo Subjects classified by duration of breastfeeding and weaning age: 600+ full-term infants from mostly white, middle SES, well- educated families in North Carolina, USA Mothers did not intend to breast- feed or lacked in- terest in being in long-term study Bayley MDI and PDI scores at 6, 12, 18, and 24 mo Confounders: Maternal age, race, occupation, educa- tion, smoking and drinking during pregnancy Child's sex, birth weight, birth order Mean differences at 24 mo: Very long vs short: +6.7 points, MDI Very long vs bottle-fed: +5.6 points, MDI; +5.9 points, PDI Positive effects for maternal age and birth order were also found
short 97 0-4 < 9
medium 184 0-4 >9 or
    5-19 <19
long 294 5-19 >19 or
    >20 <49
Very long 177 >20 >50
bottle-fed   0 0
Morrow- Tlucak et al., 1988 [5] Prospective, longitudinal, correla- tional study Cognitive development measured at 6,12, and 24 mo Household characteristics measured at 12 and 24 mo Subjects classified by duration of breastfeeding: bottle only (n = 157); breast <=4 mo (n = 39); breast >4 mo (n = 23) 229 mostly low SES infants whose mothers were recruited during prenatal care visits at a Cleveland hospital Gestational age <37 wk Perinatal complica- tions Admission to neonatal care unit Known maternal drug use or psychosis Primary language not English Child placed for adoption Delivery and discharge on weekend Family intends to move from area Bayley MDI and PDI scores at 6, 12, and 24 mo HOME scores at 12 and 24 mo Confounders: Race, parental edu- cation, maternal intelligence, cigarette use, ma- tennal disciplinary attitude Mean MDI score advantages for breastfed vs bottle only:
Breastfed group Age tested (mo) Point advantage
<=4 mo 12 +4.80*
>4 mo 12 +10.1
<=4 mo 24 +7.40**
>4 mo 24 +13.9
*F = 3.24; p = .041 **F = 3.76; p = .025 Regression analyses indicated breastfeeding uration still signif icantly related to MDI score at 12 and 24 mo, even with confounding variables and HOME scores entered in the analyses
Young et al., 1982 [8] Retrospective, cross-sectional, correlational study Cognitive and motor development measured once at 6, 8, 10, 12, 14, or 16 mo Mothers reported feeding method used Subjects classified by feeding method: artificial, breastfed <= mo; mixed, breastfed, then given cow's milk after 2 mo of age; breastfed breastfed >7 mo 1,000 infants selected from data bank set up from Tunis birth records. Equal numbers of infants from 5 social classes rep- resented for each age group alcohol use Social class not verifiable Bayley MDI and PDI scores, body length and weight, disease preva- ance, allergies Confounders: No. of siblings; maternal educa- tion, smoking, alcohol use MDI mean advantages for breastfed over mixed and artificial com bined, according to sex, SES, and age: +3.86 (t = 3.02; p < .01) for males, high SES, 10 mo +5.85 (t = 2.04; p < .05) for females, high SES, 10 mo +4.97 (t = 2.82; p < .01) for females, low SES, 12 mo +5.93 (t = 2.77; p < .05) for males, high SES, 12 mo +3.50 (t = 1.92; p < .10) for males, high SES, 14 mo None of the confounding variables were found to influence MDI scores
Florey et al., 1995 [9] Follow-up correlational study examining the influence of feed- ing method on motor and mental development at 18 mo Feeding data obtained ffom hospital forms and records of nurses' home visits in the first 2 mo Bayley MDI and PDI administered to 582 children at 18 mo Subjects classified by feeding method: breasted (n = 228); bottle fed n = 354) Population-based sample of 846 firstboni single- tons delivered in a hospitalinDundee, Scotland   Bayley MDI and PDI scores at 18 mo Mean MDI scores: breastfed, 110.2; bottle-fed, 102.5 No group mean differences were found for PDI scores

TABLE 2. Studies of the effect of breastfeeding on development in children

Study Study design Sample Exclusion criteria Outcome variables Significant results
Hoefer and Hardy 1929 [12] Prospective, longitudinal, correlational study of growth Subjects classified by dura- tion of exclusive breast- Durabon feeding: artificially fed (mo) (n = 38); S3 mo (n = 78); 4-9 mo (n = 77); 10-20 mo fed (n = 190) 383 children 7-13 yr of age No data on feeding method IQ, EQ, PQ scores (tests not specified); age talking Mean scores for tests according to duration of exclusive breastfeeding:
Duration (mo) n IQ EQ PQ Age talking (mo)
Artificially feed 38 102.3 106.5 122.0 15.2
<=3 78 101.9 109.6 125.3 13.7
4-9 77 107.6 112.1 128.3 13.3
10-20 190 100.6 105.5 121.5 14.5
Rogan & Gladen, 1993 [7] Follow-up to study described rn table 1 Cognitive development measured at 3, 4, and 5 yr   See table 1 McCarthy Scale scores at 3, 4, and 5 yr 3rd-grade report card grades in English and math Results on aH scales showed a trend for higher scores in the breastfeeding groups at all ages Mean score advantages ranged from +2.8 to +4.8 pornts for very long breastfed vs short breastfed or bottle-fed No significant differences between groups in 3rd-grade report cards
Fergusson et al., 1982 [13] Prospective, longitudinal, correlational follow-up study Cognitive development measured at 3, 5, and 7 yr Subjects classified by months of breastfeeding: bottle-fed (0 mo breastfeeding); breastfed <4 mo; breastfed >4 mo Birth cohort of children partici- patina in a New Zealand devel- opmental study . Missing data on feeding method IQ test scores: age 3, Pea- body Picture Vocab- ulary Test; age 5, Stanford-Binet; age 7, Wechsler IQ LC test scores: ages 3 and 5, Reynell Develop- mental Language Scales; age 7, Illinois >4 Test of Psycholinguistic Abilities Confounders: Maternal intelligence, education and child- rearing knowledge, SES; children's gesta- tional age at birth and birthweight Mean advantages for breastfed vs bottle-fed groups on IQ and LC tests, controlling for confounders:
Age (yr) Breastfeeding duration (mo) Advantages
IQ LC
3 <4 +1.25 +3.15
>4 +2.42 +2.71
F=3.87; p<.05
5 <4 +2.53 +2.18
>4 +2.39 +1.97
F=7.49; p<.001
7 <4 +1.94 +2.02
>4 +2.31 +.203
F=4.65; p<.01
Rodgers, 1978 [11] Longitudinal, correlational study Data from achievement tests obtained at 8 and 15 yr Mothers interviewed every 2 yr from child's birth to age 18 Subjects classified by feeding method: breastfed only (n = I,291); bottle-fed only (n = 1,133). Other subjects classified by age (months) at which they were charged from breast- to bottle- feeding 5,362 infants born in 1 week of March 1946, selected to represent all singletons born that week Missing data on feeding method Age 8: performance on school-administered picture intelligence tests and reading tests Age 15: performance on sentence completion, nonverbal ability, and math tests All scores were standard- ized on the survey population to give a mean of 50 and an SD of 10 Confounders: intelligence Parental interest in school, SES, maternal ability and paternal education, family size, birth order Mean score advantage for breastfed only group vs bottle-fed only group on sentence completion test at age 15 was +3.5 (F = 4.89; p < .001) Regression analyses showed all listed con founders significantly predicted perfor mance on sentence completion test Predicted mean score advantage for breastfed only group vs bottle-fed only group, con founders held constant:
Age Test Advantage F P
8 Picture intelligence +1.76 12.78 <.001
15 Non-verbal ability +1.76 12.51 <.001
15 Math +1.55 11.50 <.001
15 Sentence completion +1.73 13.82 <.001

None of the studies reported significant differences among any of their feeding groups during the first 11 months of life. The earliest differences were observed at 12 months. For example, Morrow-Tlucak et al. [5] reported that at 12 months the mean Mental Development Index (MDI) of exclusively bottle-fed infants was 10 points lower than that of the babies who were breastfed for at least four months (p < .05) (table 1).

After the first year of life, bottle-fed babies consistently obtained lower MDI scores than the respective comparison groups with the longest periods of breastfeeding. The intergroup differences ranged from 3.5 [8] to 13.9 [5] MDI points. However, there are inconsistencies in the data. For example, on the one hand, Temboury et al. [6] reported that infants breastfed for more than three months had higher MDI scores than bottle-fed babies (table 1). On the other hand, breastfeeding from 5 to 19 weeks did not give an advantage over bottle-feeding in the Rogan and Gladen [7] study (table 1).

Developmental scales generally lack the sensitivity to detect subtle delays in mental development during the first year of life (see, for example, ref. 10). It is therefore not surprising that the MDI scores of the bottle-fed and breastfed babies in the studies cited above first appeared after 12 months of age. Of importance here is that the MDI obtained during the second year of life is generally a modest predictor of later intelligence [11]. Pearson correlations between MDI scores and later intelligence quotient (IQ) scores are generally less than 0.50. Consequently, the developmental significance of the observed MDI differences is questionable. A conservative conclusion is that, during the second year, the behavioural repertoire of the breastfed baby is broader than that of the bottle-fed baby.

 

Children (table 2)

In addition to a study published in 1929 [12], we found three studies [7,13,14] that reported the comparisons of scores from intelligence and school achievement tests in childhood of breast- and bottlefed subjects. As with the studies of infants and toddlers, these studies do not constitute a homogeneous set. There are differences in the ages at the time of testing, in the tests administered, and in the number and nature of the confounders accounted for. In one study [7] the last assessment occurred at 5 years of age, and in another [14] the subjects were tested up to 15 years of age. The tests also differed. For example, Rogan and Gladen [7] used the McCarthy Scales for the assessment of preschoolers, whereas Fergusson et al. [13] used the Peabody Picture Vocabulary Test for preschoolers, the Stanford-Binet Scale for five-year-olds, and the Wechsler Scale for seven-year-olds. Rodgers [14] used a picture intelligence test and tests of specific cognitive abilities (e.g., mathematics).

The studies of children generally included large samples, ranging from 383 [12] to more than 5,000 [14], and found relatively narrow numerical differences between groups to be statistically significant. An evaluation of the importance of this issue, however, must consider the consistency of the findings across studies. The results form a distinct pattern. Independently of age and the tests used, subjects who were breastfed generally had higher IQs and achievement scores than those who were bottle-fed. For example, a study in Great Britain compared the performance of 1,291 exclusively breastfed (duration not specified) and 1,133 exclusively bottle-fed subjects in tests of sentence completion at 15 years of age [14] (table 2). The breastfed subjects obtained consistently higher scores than the bottlefed subjects.

 

Problems of studies of direct effects

There are two salient features in the studies of both infants and toddlers and of children. One is the weakness of the correlational design, which precludes conclusive inferences. The other is the consistency across studies in different populations and social contexts of the cognitive advantage of breastfed over bottle-fed subjects. Although the second feature cannot compensate for the weakness of the first, it strengthens the scientific merit of the original hypothesis.

The search for direct effects of breastfeeding on mental development has closely followed the prescription of the main-effect model in the biomedical literature. This model posits that exposure to a particular influential factor or event during critical early periods of brain growth results in structural changes that, in turn, determine the presence of a particular developmental outcome. At issue here is that this model is rarely indicated today in research on developmental psychobiology, because more often than not it has not worked (see, for example, Sameroff and Chandler [15]). Theoreticians argue that the influences on development are multiple and interactive, and that one single determinant seldom causes the type of effects attributed to breastfeeding [16]. In the particular area of developmental risk, it has been shown that it is generally the number of risk factors to which an organism is exposed, rather than the nature of the factors, that influences cognition [17, 18].

In conclusion, shortcomings of design have prevented a fair test of the hypothesis that breastfeeding confers developmental advantages to infants. However, the consistency in the results strengthens the scientific merit of the hypothesis and indicates future experimental research, with the admonition that the magnitude of the effects is not likely to be large. Future research should be rooted in basic contemporary premises of human development, which underscore the influence of interactions between developmental determinants.

 

Bonding

In addition to providing nourishment for the infant, the act of breastfeeding been associated with the establishment and promotion of the mother-child relationship. It has been proposed that the physiological changes that occur during breastfeeding may be related to the occurrence of emotional changes in the mother [19]. That is, it is suggested that breastfeeding may enhance a mother's feelings of connectedness with her baby, which, in turn, positively influences the developing mother-child bond. However, the data to support this notion are weak, at best. In fact, the concept of bonding has been described as "scientific fiction" [20].

Preventive effects

The potential preventive effects of breastfeeding may be divided into primary effects, by which breastfeeding would prevent a nutritional deficiency known to have adverse effects on mental development, and secondary effects, by which breastfeeding would protect the development of cognitive function from the adverse effects of an early necrologic disorder.

Primary prevention (table 3)

Although there are no published studies addressing this issue head-on, sufficient relevant information exists to document the role of breastfeeding as a primary preventive factor. Iron deficiency is associated with developmental delays among infants and toddlers [21]. In addition, although there are discrepancies in the data, well-controlled clinical trials have shown that the developmental delays of babies with iron-deficiency anaemia are reversed following iron repletion therapy [22].

The iron in breastmilk is of low concentration but is highly bioavailable, so that breastfed infants are significantly less likely to become iron-deficient during the first six months of life than bottle-fed infants, especially infants fed cow's milk [23]. Thus, if breastmilk prevents anaemia, it also prevents the developmental delays associated with anaemia.

Further support for this argument is found in a randomized, controlled trial recently conducted in Canada on the preventive effect of iron-fortified formula [24] (table 3). Two groups of infants up to two months of age were randomly assigned to receive Enfalac with 12.8 or 1.1 mg elemental iron per liter. Subsequently, the Bayley Scales of Infant Development tests were administered to the subjects at 6, 9, 12, and 15 months of age. The treatment-by-time interactive term of an analysis of variance accounted for a significant portion of the variance of the Psychomotor Development Index (PDI). In particular, there were significant differences in the expected direction between groups at 9 and 12 months. Fortified formula prevented the delays in psychomotor development observed in those who received low-iron formula. No differences were observed in the MDI. Since the MDI is a poor indicator of mental development during the first 12 months, the absence of differences in MDI is not surprising.

In conclusion, when infants are artificially fed without iron fortification, breastfeeding is likely to operate as a shield against developmental delays associated with irondeficiency anaemia. This is particularly true in lowbirthweight infants, who are at high risk for iron-deficiency anaemia [25]. However, exclusive breastfeeding after six months of age is not likely to have this effect against irondeficiency anaemia [26].

Long-chain polyunsaturated fatty acids (LCPUFA) are components of neural tissue, and recent research on their effects on selective neural function in laboratory animals and humans provides strongly suggestive evidence of the potential contributions of breastmilk to cerebral function [27, 28]. Briefly, LCPUFA, particularly arachidonic and doeosahexaenoic acids, play important roles in the development of the retina and cerebrum, and deficiencies of these in laboratory animals and low-birthweight infants may cause selective dysfunctions in visual function and learning [1, 27].

In utero, effective transfer from the mother across the placenta satisfies the need for LC-PUFA in the foetus. Later, maternal milk, a rich source of doeosahexaenoic acid, meets the needs of the young infant [29]. Generally, however, the contents of docosahexacnoic acid in formula are insufficient for newborns or young infants, as demonstrated by the low plasma levels of docosahexaenoic acid in formula-fed infants and by visual function differences between breastfed and formula-fed infants [2931]. In one study, pre term (four months adjusted age) and full-term infants who were fed human milk performed significantly better than formula-fed infants in tests of visual evoked potentials and of preferential looking acuity. Further, at 36 months the breastfed term infants also performed better than the formulafed term infants in dot stereo acuity and lettermatching ability tests [1].

TABLE 3. Studies of the primary preventive effects of breastfeeding

Study Study design Sample Exclusion criteria Outcome variables Significant results
Moffatt et al., 1994 [24] Prospective, longitudinal, randomized clinical trial comparing the effects of iron-fortified and regular formula on the cognitive and motor development of Age (mo) infants 112 subjects received iron fortified and 113 regular formula for 15 mo Cognitive and motor devel opment measured at 6, 9, 12, and 15 mo 225 bottle-fed infants 0-2 mo old born in hospitals in the area of Winnipeg, Canada   Bayley MDI and PDI scores at 6, 9,12, and 15 mo No significant differences between groups in MDI scores Mean score advantage for iron-fortified formula vs regular formula group in PDI scores:
Age (mo) Advantage
6 +0.6
9 +4.0
12 +6.3
15 +2.8
p = .02 (group x time interaction)
Agostoni et al., 1995 [31] Prospective, quasi-experi- mental study comparing the effect of breastmilk, LC-PUFA-enriched for- mula, and standard for- mula on neurodevelop- mental scores at 4 mo Infants whose mothers chose to breastfeed were ran- domly assigned to receive LC-PUFA-enriched for- mula or standard formula Neurodevelopmental re- sponses measured with the Brunet-Lezine psycho motor development test at 4 mo Blood fatty acid content measured at 4 mo 90 infants born in a clinic in Milan, Italy, during 1 yr Classification of sub- jects: exclusively breastfed (n = 30); LC-PUFA formula (n = 29), standard formula (n = 31) Gestational age <37 wk Apgar score <7 Any perinatal dis- order or disease Scores on the Brunet- Lezine psychomotor test, which assesses gross and fine motor function, social reactions, and language Brunet-Lezine scores significantly higher in the exclusively breasfed and LC-PUFA formula groups than in the standard formula group (p < .05)
Group Mean score
exclusively breastfed 102.2
LC-PUFA formula 105.3
standard formula 96.5
Blood fatty acid levels significantly higher in the exclusively breastfed and LC-PUFA formula groups than in the standard formula group

A recent study [32] compared the developmental test performances of three groups of subjects receiving human milk, conventional formula (with LC-PUFA precursors), or an experimental formula supplemented with pre-formed LC-PUFA (table 3). All eligible subjects were between 37 and 42 weeks gestational age, were free of any type of diagnosable disorder, and had five-minute Apgar scores of 7 or better. Mothers of 30 of the subjects chose to breastfeed their babies. The remaining subjects were randomly assigned to receive either the conventional formula (n = 31) or the experimental formula (n = 29).

A psychomotor developmental test (BrunetLezine) was administered to 86 of the subjects at age four months (two subjects in the conventional formula group and two subjects in the experimental formula group could not be tested). The BrunetLezine Test assesses gross and fine motor function, social responses, and language. A developmental quotient score is obtained from scores on the subscales. The mean score on the Brunet-Lezine Test for all subjects was 101 (SD = 11) and the range was 80-136, similar to the standardized values reported by the authors of the test. Infants receiving the LC-PUFA-enriched formula or human milk scored significantly higher (105.3 and 102.2, respectively) on the Brunet-Lezine Test than the subjects receiving the conventional formula (96.5). There were no differences among the three groups in parental and socio-economic variables. Blood analyses for a subgroup of infants revealed that fatty acid levels were higher for the infants receiving the LC-PUFA-enriched formula or human milk than for the infants receiving conventional formula.

Although these and other similar studies [33] help our understanding of the relations among breastmilk, LC-PUFA, and cerebral function, they do not speak directly to the question of the contribution of breastmilk to the growth of intelligence. Neither theory nor empirical data suggest that visual acuity, visual evoked potential, or letter discrimination during the first months of life are precursors of the development of central information processing or of abilities that constitute the cornerstones of intelligence. Further, although the Brunet-Lezine Test, the Bayley Scale of Mental Development, and other developmental scales are useful tools to describe the behavioural repertoire of four-month-old infants, in most cases developmental scale scores obtained at that early age do not predict later developmental scale performance even at the end of the first year of life. Developmental scales administered in early life do not measure cognition.

Secondary prevention (table 4)

At issue here is the potential protective effect of breastfeeding against the sequelae of prematurity or an early neurologic disorder. Lucas and collaborators [34-36] have published a series of articles on the short- and long-term effects of breastfeeding and formula-feeding on the performance on developmental and IQ tests by children born prematurely with very low birthweights (1,850 g). The basic design is that of a prospective, randomized trial in five centres to assess the effects of diet on neurodevelopment (table 4). A limitation of these studies is that the definition of the samples is very limited, and the articles do not discriminate between the subjects who participated in the different studies. Further, the direction of the hypothesis tested in each study is not clearly indicated.

A study published in 1989 [34] compared the development of pre-term infants admitted to the neonatal units in Cambridge, Ipswich, or King's Lynn, England, from 1982 to 1984, who were randomly assigned at birth to either donated banked breast milk (REM) or pre-term formula (PTF) (2 g protein, 0.335 MJ; 35 mg phosphorus; 70 mg calcium; 45 mg sodium, 100 ml) as the sole diet. The mothers in this trial (trial I) had chosen not to provide their own milk to their offspring. In trial II, comparisons were also made among the offspring of women who elected to express their own milk to feed their children. These children were also randomly assigned to either BBM or PTF to supplement their intake from maternal milk. The diets were discontinued when the children were discharged from the neonatal unit or when their body weight was at least 2,000 g. Comparisons were made at nine months of age on their performance in the screening inventory of Knobloch et al. [37], which includes five developmental areas (adaptive, gross motor, fine motor, language, and personalsocial). This assessment tool is a screening inventory rather than a developmental scale, and is not generally recognized as a test of intellectual development, as suggested (p. 320) by the authors. A neurologic examination (Amiel-Tison and Grenier) was also administered to the children, who were classified as normal, equivocal, or impaired.

When the data from both trials were pooled at nine months of age, the subjects who had received PTF, either as the sole diet or as a supplement, had significantly higher scores in the adaptive, fine motor, language, and personal-social areas than those who had received BBM. Further, in trial II those subjects who had received PTF had a higher developmental quotient than those who had received BBM, as well as higher scores in the adaptive, language, and personal-social subscales .A finer analysis showed that among those who had received some milk from their own mothers, those who had received more than 50% of their total intake from BBM were at the highest disadvantage. Moreover, the covariation between diet and development was stronger among those classified as small for gestational age (below the 10th percentile).

Continue

Discussion of paper by Pollitt and Kariger

 

Dr. Colombo

An expert from the Institute on Brain Research in Frankfurt, who specialized in the growth and development of the brain in children, was sitting here a few months ago, and I asked him, "How long do these developments last?" I was expecting him to say for two or three years, but he said until puberty. Certainly, if there are clear differences, he said that they may show up at 12 months; but if we have to wait a long time, so many confounding factors intervene that the analysis may fail to give clear answers. As a layman, I can see that this would be a problem for the analysis. Now, I wish to give the floor to more respected colleagues. Thank you.

Dr. Lawrence

I am intrigued by the comment you made at the end that an area of enormous potential was assessing the role of breastfeeding in the formation of secure attachment in early childhood. Do you think of that as a maternal behaviour or an infant behaviour or both, and, if so, what is the mechanism that you postulate? This is particularly interesting in light of the question you asked me yesterday about the weakness of the evidence of maternal behaviour.

Dr. Pollitt

Infant attachment to the caretaker (biological or surrogate mother) is first observed at six to eight months, and it generally stems from the continuous social and emotional interactions between both members of the dyed. It is theoretically plausible that interactions leading to attachment are induced and sustained by behaviours or behavioural cues of both the infant (for example, smiling) and the caretaker (for example, scent of the nipple). Breastfeeding would provide a medium for the presence of particular behavioural interactions (for example, sucking and milk release) that would help the development of secure attachment between the infant and the caretaker.

Dr. Lawrence

Do you see this attachment in the breastfed infant as being singularly different from that of the bottlefed infant?

Dr. Pollitt

I do not know, but I suspect this is the case because bottle-feeding and breastfeeding represent different behavioural systems, including similar and distinct behaviours of both parties. For example, the organization of sucking behaviour occurs earlier in the breastfed infant than in the bottle-fed infant, and the scent of the mother's nipple is different from the scent of a nipple on a bottle. Further, whereas the composition of maternal milk changes during feeding, this does not happen in artificial feeding. These differences between bottle-feeding and breastfeeding might be independent of the social and emotional development of the child. Nevertheless, the nature of the behaviours supports the proposition that there is scientific and programmatic merit in testing the hypothesis in the field.

Dr. Garza

I'd like to explore your comment that even if we accept the validity of the present findings, with all of their limitations, the differences between breastfed and bottle-fed babies are rather modest. If we think of them as half a standard deviation, I agree with your assessment for those ranked around the mean. That is, I don't know whether half a standard deviation in either direction would have much functional significance. If, however, those differences are homogeneously distributed, they could theoretically have an enormous adverse impact on the number of functionally impaired people. Or the converse might be true: you would almost double the number of gifted people. Is there any reason to suspect that improvement would not be distributed homogeneously? Or is this such a theoretical construct that it has no merits?

Dr. Pollitt

The question refers to two separate but related issues. One is whether the alleged effects of breastfeeding are equally distributed along the entire distribution of scores, whatever cognitive measures are used. I do not have an answer, and I doubt whether at present there are relevant data to address this question. The second issue is the behavioural significance of the effects of breastfeeding on cognition. Even though the effects reported were relatively modest, they could still have significant developmental importance if they were found in different cognitive areas. Behaviourally, small benefits over a wide range of cognitive domains (for example, short- and long-term memory, attention, concept formation, and vocabulary) may be more advantageous than large benefits over a single domain (for example, short-term memory).

Dr. Garza

In relation to the comment made by Dr. Colombo, it may be useful for you to comment on the rather extraordinary finding from Guatemala that a limited intervention during gestation and the first 3 years of life was still of functional significance 15 years later, despite the fact that nothing had been done to sustain the intervention.

Dr. Pollitt

The study involved four rural communities. Pregnant and lactating women and children up to the age of seven years participated in this study from 1969 to 1976. Two of these communities received a high-energy (180 kcal x 180 ml) and high-protein (11.5 g x 180 ml) supplement called atole, and the remaining communities received a low-energy supplement (one-third of that in atole). A 1988 follow-up showed that those in the first group performed significantly better than those in the second group in a wide range of cognitive tests (for example, arithmetic, reading comprehension, and vocabulary). The data necessary to explain the mechanisms behind these effects are unavailable. It seems likely, however, that two different sets of mechanisms were involved. One is that atole made a difference in the development of particular areas in the brain or in the neurotransmitter systems that facilitated cognitive function. The other involves the benefits of atole on physical growth, neuromotor maturation, activity level, and interactions with the social and physical environment. These advantages pooled together could have increased the educational opportunities of the children and fostered cognitive development.

Dr. Woolridge

I have two questions. The first regards the two slides on alcohol and marijuana use. If I understand them correctly, they both refer to breastfeeding mothers. Are there data from those studies to show what sort of effect you would get for non-breastfeeding mothers? One may assume that use of alcohol and marijuana may affect other aspects of the mother-child relationship. The effect could lead to lower development in the children of users. For my second question, I wanted some clarification on the issue of preterm births. I think I read in the reviews by Villar and Belizthat the proportion of low-birthweight babies who are pre-term is smaller in developing than in developed countries because there are so many intrauterine-growthretarded babies. Because the figures for pre-term births are expressed proportionately does not necessarily mean that the incidence of pre-term births is lower in less developed countries.

Dr. Pollitt

I agree with what was said regarding the prevalence of lowbirthweight babies in developed countries and have nothing to add. I also agree with the speaker that mothers who bottle-feed their infants and use alcohol and marijuana might hinder the development of their offspring through different channels.

Dr. Victora

When we are looking at contaminants in breastmilk, we must realize that the alternatives to breastmilk can have contaminants, too, although they may be of different types. In New Zealand recently, the soya bean milk formula was found to have oestrogens, and the babies' intake was equivalent to about 12 pills per day, which is quite significant. I was wondering what is the effect of low-lead exposure on IQ, because we are trying to get lead out of petrol and similar things because of its effects on children.

Dr. Pollitt

There is no consensus on the cut-off point that should be used to define elevated lead levels in the blood. Recently, the cut-off point in the United States was lowered to 10 g/dl (0.48 mol/L). Nevertheless, the World Health Organization still uses the former cut-off point. Studies on the effects of elevated lead levels on cognition in children are limited by problems of research design. The use of experimental protocols is precluded because of obvious ethical concerns. Further, strong criticisms have been made of the validity and reliability of the data collected. In my view, there is still no evidence to support the contention that cerebral function is at risk with blood lead levels less than 25 parts per million.

Dr. Garza

What level of lead exposure would be needed to effect a change of one-half of a standard deviation in IQ?

Dr. Pollitt

I do not know.

Dr. Hartmann

How is it possible to differentiate between the effects of marijuana or alcohol on the infant through the maternal milk and the direct effects during gestation when the mother was also using alcohol or marijuana?

Dr. Pollitt

The published studies do not discriminate between the effects on the offspring of the mothers' consumption of drugs (alcohol or marijuana) before and during lactation. The authors, however, caution the reader against drawing unwarranted conclusions.

The cultural context of breastfeeding and breastfeeding policy

Penny Van Esterik

 

Abstract

Breastfeeding is not instinctive behaviour but is dependent on learning and is, therefore, influenced by social and cultural factors. Thus, the social sciences as well as the biological sciences should be engaged in explanatory research about breastfeeding To rebuild breastfeeding cultures to protect, support, and promote breastfeeding a biocultural model of breastfeeding and child care that takes a broader view of culture must be developed: a view that attends more to differences than similarities, that provides more detailed contingencies of context, that is more sensitive to the forces that constrain women's lives, and that can be more directly linked to policy-making. This article explores the interdisciplinary nature of breastfeeding research and suggests some areas where anthropological theory and method could be put to better use to ask new research and policy questions about breastfeeding

 

Introduction

Breastfeeding is the epitome of a biocultural phenomenon in which the processes of biology and culture are inextricably linked [1]. It is not instinctive behaviour but is dependent on learning; it is, therefore, influenced by social and cultural factors. Because breastfeeding is at the intersection of biological and cultural processes, the social sciences as well as the biological sciences should be engaged in explanatory research about breastfeeding. This article explores the interdisciplinary nature of current breastfeeding research and examines cultural factors and cultural context as two different ways to approach the "cultural" in "biocultural." I suggest some areas where anthropological theory and method could be put to better use in breastfeeding promotion and conclude that breastfeeding policy can be influenced by social science research.

 

Interdisciplinary nature of breastfeeding research

The participants in this Workshop come from many different disciplines but share a commitment to research and policy to strengthen breastfeeding. To work profitably together, we must acknowledge disciplinary differences. These differences emerge out of hundreds of years of Western philosophy and logic that have kept the sciences, social sciences, and humanities apart-or, in the case of breastfeeding, brought them together on biomedical terms. Anthropology straddles these divisions and permits an easier integration of the biological and the cultural.

Interdisciplinary work is not easy, as the different epistemological assumptions of each discipline need to be acknowledged. The term "biocultural" stresses the relation between biology and culture and, hence, is important for our discussions of breastfeeding and society. Most research on breastfeeding however, examines either the cultural or the biological aspects. The few people who put the two together often write and speak as if the biology part provides unquestioned facts, and the culture part provides the less important, ephemeral context.

Medical anthropology has been found to be "a powerful tool for reassessing what is taken as natural and normal in connection with the human body" [2]. Science has determined generalities or laws about breastfeeding many of which have been reviewed at this Workshop. But generations of mothers who breastfeed their children have also formed some generalities about the process. Our task should be to bring these two kinds of generalities or laws into a specifiable relation with each other, not to dismiss one, or to reduce one to the other. Millard [3] notes that the "guidelines" that Mexican women have about infant feeding are principles; that is, they are statements of natural tendencies or laws, conceptualizations of ultimate causes, and guides to practice. These guidelines also have commonalities with scientific practice. Application of cultural principles involves logic and situational decision-making on the part of the mother. These principles are used in conjunction with other sets of principles, such as the humoral system, to decide how individual infants should be fed.

Some concepts hinder and others enhance communication across disciplinary boundaries. In the past, "culture" and "cultural factors" have been used in ways that have not always increased understanding of infant-feeding practices or encouraged interdisciplinary collaboration between anthropology and the health sciences. As a term such as culture crosses disciplinary boundaries, its meaning and significance often change.

Defining culture and stating that cultural factors are important for understanding infant-feeding decisions does not alter the fact that the concept is very difficult to use. Just as biologists have difficulty agreeing on a definition of life, theologians on a definition of God, and doctors on a definition of health, anthropologists seldom agree on a definition of culture. We are unlikely to be able to find narrowly defined or easily measured cultural variables or indices to capture the variations within or between different infantfeeding patterns. Continuing to search for these elusive cultural factors may result in culture being blamed for generating attitudes and beliefs that are seen by health planners as obstacles that must be overcome by education.

 

Cultural factors in biomedical models

What sociocultural factors have been singled out for integration into biomedical and epidemiologic models of infant feeding? Common factors include religion, marital relationship, family composition, residence pattern, and values. Qualitative data have been used successfully to support findings from epidemiologic and biomedical research, but qualitative data can also be used to raise new questions and examine relations that are not amenable to reductionist models. Questions about values, attachment, nurturance, and sexuality-all intimately connected with breastfeeding and society-require interpretation from social science paradigms.

There is in the literature on breastfeeding clear agreement that maternal attitudes towards breastfeeding and bottle-feeding are culturally conditioned and, indeed, influence infant-feeding decisions. The most widely accepted method in health and nutrition research is the construction of knowledge, attitude, and belief questions that can be administered by a single context questionnaire, where respondents are asked whether, or to what extent, they agree or disagree with a statement about infant feeding. Scores on these questions may then be related to a mother's actual infantfeeding decisions.

There are numerous problems with this approach. Infant feeding in general and breastfeeding in particular are very personal and emotionally charged subjects. For this reason, it is difficult to obtain reliable, valid information on mothers' attitudes, beliefs, and knowledge through survey methods. Because the interviewers often have had no previous contact with the respondents, it is difficult for them to evaluate how the interview setting affects mothers' responses.

Interviewers' biases may encourage mothers to predict what the interviewer wants to hear and answer accordingly. This problem is complicated by respondents' desire to be polite to strangers or their hesitancy to speak frankly to authority figures perceived to possess power. In addition, standardized knowledge and attitude statements about infant feeding often reflect verbal cliches or key images developed through health-education or breastfeeding promotion campaigns. The problem of phrasing culturally appropriate questions or statements without biasing the response is particularly difficult.

Serious conceptual problems also arise in relating knowledge, attitude, and belief to actual practice. The links between knowledge and belief, belief and attitude, and attitude and practice are both poorly understood and ambiguous. Not only can we not demonstrate a causal relationship between attitude and behaviour, but we often cannot even predict the direction or order of the relationship. Behaviour may well change before attitude changes, not after. For example, breastfeeding-promotion campaigns, based on linear reasoning linking knowledge to belief, attitude, and practice, often aim to increase correct knowledge about the importance of breastfeeding. It is therefore not surprising that breastfeeding-promotion campaigns based on improving knowledge, attitudes, and beliefs about the benefits of breastfeeding have not, by themselves, proved to be an effective means for changing infant-feeding patterns. The success of these methods depends on whether women's knowledge of breastfeeding was acquired through formal classes, observation, books, or women's stories. Learning the practical management of breastfeeding is quite distinct from trying to teach someone else to do it right.

Underlying much of the literature on the determinants of infant-feeding practices is a nagging, unanswered question. Can we, given our current research methods, distinguish between mothers who want to breastfeed yet cannot, and mothers who do not want to breastfeed and do not? Women belonging to both of these categories may fail to initiate breastfeeding or may breastfeed for only a short period of time. We assume that women in the the former group have the knowledge and attitudes to support breastfeeding but are unable to do so. They are constrained by something, such as inappropriate medical practices, excessive promotion of breastmilk substitutes, or lack of social support. We assume that women in the latter group do not want to breastfeed or will breastfeed for only a short time.

The difference between these two categories of women lies not only in their demographic characteristics but also in their heads-in the ideas, beliefs, and assumptions about infant feeding that make up the cognitive and affective dimensions of human behaviour. Studies of the determinants of infant-feeding practices often include these factors under the variables of maternal knowledge and attitudes or cultural factors. Studies that do not emphasize these factors acknowledge their possible importance.

This approach to knowledge and attitudes, based on social-psychological methods and theories, does not reflect the way anthropologists approach human behaviour. Nor does it do justice to the complexity and flexibility of human decision-making about infant feeding. For example, in the complex calculus of infant-feeding decisions, a woman may weigh such factors as preference for dresses zippered up the back, avoiding sexual intercourse, or thwarting her mother-in-law. Even an apparently straightforward interpretation of behaviour may generate erroneous assumptions about cultural attitudes. For example, the conclusion that the use of Western-style blouses indicates a desire for modesty and a negative attitude towards exposure of the breast may be unjustified. In areas of the world where it is believed that the evil eye can poison breastmilk, blouses may, in fact, be worn to protect the breasts and breastmilk from danger.

Moreover, people have the capacity to tolerate an amazing degree of inconsistency between what they say they "believe," what they do believe, and what they do. The capacity of mothers to tolerate inconsistency, to hold contradictory beliefs and attitudes about infant feeding, and to interpret options reinforces the need for means of data collection and analysis beyond traditional knowledge and attitude assessment. Whereas cultural factors are determinants in chains of cause and effect, cultural context is a much less circumscribed concept that permits other kinds of information, such as the political context or the gender context, to guide explanations. This broad background information is referred to here as the "cultural context" of infant-feeding decisions. This context may be thought of as an additional level of analysis that integrates social, cultural, and biological factors. Such an additional level of analysis is necessary for interpreting attitudinal data. Survey responses alone seldom provide the data necessary for such contextual interpretation. For example, the knowledge that women agree that breastfeeding makes breasts sag, without the accompanying knowledge of how sagging breasts relate to women's body image and selfimage, may easily result in misinterpretation of this information or distortion of its meaning. Body image, beliefs about breast size, and ideas of beauty are embedded in culturespecific systems of gender ideology.

 

Breastfeeding context

Breastfeeding as a process is culturally constructed: that is, in spite of its physiological base, the process itself, its meaning, and the way it is integrated into cultural systems varies globally. Until recently, we have had minimal information on the sociocultural context of breastfeeding from detailed, long-term ethnographic analysis. This evidence is now available, and it demonstrates that women's lives and child-care practices are changing rapidly.

One conceptual model emerging from these ethnographic data approaches cultural context as the interaction between style and structure. Style refers to the manner of expression characteristic of an individual, a period of time, and a place. The concept of infant-feeding style communicates fundamental cultural assumptions underlying infant-feeding decisions. It refers to the manner of feeding infants in particular communities and includes both the way to feed an infant and the values, attitudes, and beliefs associated with that behaviour. Infant-feeding style includes the style of interaction between mothers and infants, eating style (how does the infant-feeding pattern fit with the household meal pattern?), breastfeeding style (how is breastfeeding accomplished?), and feeding "in style," reflecting the fact that infant-infant feeding choices are part of dynamic, changing trends and fashions.

To understand differences in breastfeeding style, it may be useful to distinguish between breastfeeding as a process and breastmilk as a product. Process or product interpretations may be emphasized in different contexts [4].

Both personal and shared styles of infant feeding interact with organizational and institutional structures, such as health-care institutions and marketing systems. These structures are important in influencing mothers' infantfeeding choices. The interaction between style and structure should allow us to predict how infant-feeding choices might be affected by different policy options.

 

Rebuilding breastfeeding cultures

A meeting of WHO and UNICEF policy makers in 1990 resulted in the adoption by 30 governments of a global initiative, the Innocenti Declaration, on the Protection, Promotion, and Support of Breastfeeding [5]. This Declaration stated that for optimal breastfeeding,

all women should be enabled to practice exclusive breastfeeding, and all infants should be fed exclusively on breastmilk from birth to four to six months of age. Thereafter, children should continue to be breastfed, while receiving appropriate and adequate complementary foods, for up to two years of age or beyond.

In order to bring this about,

efforts should be made to increase women's confidence in their ability to breastfeed. Such empowerment involves the removal of constraints and influences that manipulate perceptions and behaviour towards breastfeeding, often by subtle and indirect means. This requires sensitivity, continued vigilance, and a responsive and comprehensive communications strategy involving all media and addressed to all levels of society. Furthermore, obstacles to breastfeeding within the health system, the workplace, and the community must be eliminated.

This carefully worded statement is a challenge to change many priorities of the modern world to rebuild breastfeeding cultures. The language stresses the empowerment of women to breastfeed, rather than their duty to breastfeed, a change that should bring more advocates for women's health to support breastfeeding policies.

To rebuild breastfeeding cultures that will protect, support, and promote breastfeeding, we must work from models of breastfeeding and child care that are more sensitive to gender and the forces that constrain women's lives. What is entailed in recreating breastfeeding cultures? In some parts of the world, changing assumptions about body image is a priority; ensuring women are adequately fed is of higher priority elsewhere. A great deal of political will to make changes benefiting women and children is crucial in all state and international institutions.

At some point, policy makers need numbers to evaluate and finance policies and programmes. But that does not mean that ethnographic observations and other cultural information are merely illustrative anecdotes. The linkage between cultural data and policy can be directly relevant to establishing priorities. Because ethnographic description is both holistic and richly contextualized, it is easy for policy makers to picture the real-life conditions of the families that their policies will affect. Some products of ethnographic fieldwork, such as community sketches and mothers' life histories, are available much faster than survey data, which require substantial processing.

Solutions to infant-feeding problems must come from the cultural context underlying infant-feeding decisions. The same "culture" that some policy makers view as an obstacle to development must ultimately provide solutions assembled from available options, ideas, and strategies already in the cultural repertoire. In this case, the task of the policy maker is to choose options and implementation strategies that are most compatible with the infant feeding style in different countries.

Knowledge of style without consideration of structural constraints or supports would, however, be unproductive. Structural constraints, such as the powerful influence of the health-care system, the marketing practices of transnational manufacturers of infant foods, and structural supports, such as vendors selling porridges or traditional midwives, must also be included in policy decisions to suggest new directions to improve infant-feeding practices.

Breastfeeding-promotion activities, mothersupport projects, and consumer-advocacy campaigns are often viewed in isolation from each other and from other programmes. Nevertheless, breastfeeding has been linked to related childsurvival campaigns, such as immunization, family planning, growth monitoring, and oral rehydration therapy. To encourage the changes envisioned by the Innocenti Declaration, breastfeeding advocates must seek new allies and closely examine the concerns such potential allies have with regard to past promotion of breastfeeding. A number of potential allies could be called on to offer support for breastfeeding initiatives.

Links have already been made between breastfeeding and child-spacing programmes. The World Bank's "A case for promoting breastfeeding in projects to limit fertility" [6] identifies three arguments that have been used against the promotion of breastfeeding for its contraceptive effect:

  • Breastfeeding does not need to be promoted in areas where it is still the norm.
  • Declines in breastfeeding are inevitable and will have negligible demographic impact if compensated by increases in the use of modern contraception.
  • Breastfeeding is not a reliable contraceptive for the individual woman.

The World Bank report challenges these arguments and demonstrates the advantages of breastfeeding for child spacing. It is, however, important to note that African women's groups in particular have warned against linking breastfeeding to family planning too closely and have argued for breastfeeding to be promoted for its own sake.

Fewer commonalities have been recognized with environmental groups. Lactation and breastfeeding had no place in the report of the World Commission on the Environment and Development entitled Our Common Future (unpublished report, Geneva, 1987), although the report's treatment of issues such as sustainable development, the international economy, population, human resources, food security, energy, and industry all could be related to infant-feeding choices. The environmental movement and advocates for sustainable development are potential allies for breastfeeding could be shown how breastfeeding furthers their interests and encouraged to link breastfeeding into their planning. But breastfeeding promotion that treats women as producers of natural resources is bound to fail.

The strongest supporters of breastfeeding should be women's groups. Breastfeeding is seldom considered an important issue to be discussed in national or regional women's organizations in developed or developing countries. For example, national women's organizations were not immediately supportive of Brazil's breastfeeding initiatives because they saw it as a means of isolating women in their homes. Similarly, women's groups in India protested against legislation to control the marketing of infant formula, calling the bill draconian, fearing it would damage women's careers and force them back to the kitchen.

According to a review of American maternity policies by Kamerman [7]:

Although the women's movement clearly has played an important role in improving the status of women, maternity and other family benefits have not been at the forefront of its agenda.... Heretofore, the women's movement has viewed family politics as either too traditional a focus for unenlightened women, or as too open to criticism as conservative.

In Scandinavian countries, efforts to support breastfeeding have been more strongly supported by the women's movement:

The new feminist movement in Norway has encouraged women's self-confidence and pride- both prerequisites for breastfeeding. Unlike similar movements, the Norwegian feminist movement has never seen a contradiction between women's liberation and breastfeeding [8].

The antagonism to breastfeeding that exists in many parts of the European and North American women's movements results in difficulties in establishing breastfeeding as a priority in international women's meetings. This antagonism or apathy will be particularly destructive to efforts to implement the Innocenti Declaration unless it is countered by clear recognition of breastfeeding as a woman's right. Thus, there is a need to reconsider breastfeeding in relation to human rights. Programmes that promote the child's right to breastmilk rather than the mother's right to breastfeed without consideration of maternity entitlements are likely to be damaging in the long run.

The issue of breastfeeding has been invisible in the women's movement, either because it is taken for granted in some parts of the world or because it is totally out of women's consciousness in other parts of the world. It is the responsibility of breastfeeding advocates to integrate their issues with other concerns of women. This process was begun at the Beijing Conference on Women in September 1995, where a number of measures protecting breastfeeding were included in the final action plan. Women's organizations need to be informed about how breastfeeding entitlements can complement their other policy objectives and then be mobilized to support breastfeeding policies. If feminist theorists and activists supported breastfeeding, they might well be able to reformulate a more global, holistic approach to gender, care, mothering, and empowerment.

 

Conclusions

Indigenous cultural knowledge about child feeding is critically important for successful breastfeeding research and programmes, but there are ways this knowledge can be better used. I suggest that anthropologists can be most useful to breastfeeding research if they resist the pressure to reify culture, or to provide checklists of cultural factors affecting infant feeding. No list would be adequate to the task, and the temptation to reduce culture to one or two factors within a biomedical framework may draw attention away from more important questions about power, class, or gender. Whenever we use the concept of culture, we should ensure that it is firmly situated in understandings of material conditions of life and fields of power. Anthropologists should develop innovative ways to communicate about other patterns of infant feeding without resorting to homogenizing generalizations and dangerous reifications that can be used to create or perpetuate stereotypes: "All Bangladeshi women reject colostrum," "All Mexican women wean abruptly," and so forth. We should strive to make visible the cultural systems in which we operate, examining assumptions about our own health-care systems and the tenets of biomedicine and not treating them as natural or as givers. Finally, we should resist the commoditization of culture by insisting on the necessary theoretical framing of the concept and locating it more directly within various social science disciplines. In this way, we can make room for metaphor as well as measurement in breastfeeding research, programmes, and policy.

 

References

1. Stuart-Macadam P. Dettwyler K, eds. Breastfeeding: biocultural perspectives. New York: Aldine De Grnyter, 1995.

2. Lindenbaum S. Lock M, eds. Knowledge, power and practice: the anthropology of medicine. Berkeley, Calif, USA: University of California Press, 1993.

3. Millard A, Graham MA. Weaning decisions by rural Mexican women. Working Paper on Women in International Development no. 73. East Lansing, Mich, USA: Michigan State University, 1984:1.

4. Van Esterik P. Commentary: an anthropological perspective on infant feeding in Oceania. In: Marshall LB, ed. Infant care and feeding in the South Pacific. New York: Gordon and Breach, 1985:357.

5. WHO/UNICEF meeting on Breastfeeding in the 1990s; a global initiative. Innocenti Declaration on the Protection, Promotion and Support of Breastfeeding, Florence, Italy, 1 August 1990. New York: UNICEF, 1990.

6. Berg A, Brems S. A case for promoting Breastfeeding in projects to limit fertility. Washington, DC: World Bank, 1989.

7. Kamerman S. Maternity policies and working women. New York: Columbia University Press, 1983.

8. Baumslag N. Breastfeeding: the passport to life. New York: UNICEF, 1989.

Discussion of paper by Van Esterik

 

Bishop McHugh

I'd like to make two comments. The first draft of the document to be used in Beijing for the International Women's Conference did not contain the word breastfeeding. Now, how can you write a document about women and empowerment of women and not even mention it? I understand that it has now been included.

Van Esterik

No. I was at the preparatory conference, and I welcome a chance to bring you up to date. The fascinating thing is that breastfeeding was there in the regional conferences in South-East Asia and Latin America and the Vienna Conference on Human Rights. Breastfeeding was very clear because the World Assistance for Breastfeeding Action (WABA) lobbied to make sure, and it went in under "women's health," "human rights," and "employment," so that if it was removed in one section, it would be there in another. When those drafts came to New York, every reference to breastteeding was removed. So we went to the preparatory conference for Beijing and we lobbied, and we know for sure that one reference is in under "structural adjustment," because one of our WABA members is the Swaziland representative, and she stayed up until midnight when they were finishing, and she got it in there. But all the most important places-"human rights," "women's health," and "infant health"-were bracketed, which means they will not be discussed until Beijing. That document was not out until the last day of the preparatory conference, and so we have a lot of work to do.

Bishop McHugh

I agree. But I also think it underscored part of my concern, and that is, it is part of a cultural context that eliminated it. When the documents came to New York, it was a different understanding of women that is perhaps local to ten square blocks of New York City that wrote the document and excluded that concept, because that's not part of their lexicon. The second comment I want to make is that you did not have to feel uncomfortable showing the Playboy pictures. In fact it's important to show them, because we in the United States face recurring court cases brought by women who have been excluded from restaurants or other places for breastteeding. They have to go to the courts to vindicate what seems to me ought to be a natural right. But you can walk into any drugstore, and what you have is mild compared with what you can get from the so-called girlie magazines.

Dr. Sommerfeldt

Just a very brief comment on the Women's Conference in Beijing. I had a call from someone from New York asking if the Demographic and Health Survey could give an estimate of the burden that breastfeeding imposes on women. I think the reason for this question was to support an argument that it was difficult to breastfeed and perhaps that women shouldn't do it. I said that, first, I didn't think it was a burden. Second, I said there was no way we could provide that kind of quantification, although all they had to do was pick up our report and take whatever information they wanted from it. I also said that if a woman didn't breastfeed and didn't use contraception and conceived again very soon, that would be a much greater burden on her than breastteeding. She never contacted me again. Maybe she got an answer from someone else. I don't know.

Dr. Van Esterik

We had a major problem. The Health Caucus was controlled by someone who was very close to multinational companies, and we had BINGOs (Business Interest NonGovernmental Organizations) in that caucus, not women's interests NGOs. One thing that made it very difficult was that they went around to some people we were lobbying and talked about how people who were promoting breastfeeding were just trying to make women feel guilty if they couldn't breastfeed. They kept asking other people for statistics about how many women couldn't breastfeed. I will leave you with a popular article, as well as an academic one, arguing that breastfeeding is a feminist issue. The first is designed specifically for radical North American and European women's groups that do not usually think about breastfeeding, and the second is to tell them why they should consider breastfeeding as a feminist issue.

Dr. Menken

I think we would be unrealistic if we said that breastfeeding was not a burden. It is a burden if women are hassled in the ways that we have been talking about. It's made a burden, and I think that's exactly the kind of point we are addressing. These are burdens caused by culture, and many of the issues we need to address are making it comfortable, promoting an atmosphere, just as many people live in an atmosphere where their attempts to breastfeed are frowned upon and discouraged. My first kid was born in Bethesda Medical Center. Let me tell you, the fight to breastfeed 29 years ago was really something. Not many people have the energy. They are fighting too many other battles. What we need to say is that under the right circumstances, it is not a burden; it's much better, and it's much easier, but I think we have to recognize that.

Dr. Perez

I was going to make this comment in a later session, but I believe that now is the moment. We are all interested in promoting breastfeeding, but we have to remember that the breast is one of the most important sexual symbols of a woman's body. More than that, it is not only a symbol, it is a very important organ that participates in the sexual union. The nipple is especially important in a woman's orgasm. Thus, if somebody proved that it is true that breastfeeding destroys this symbol, this organ, we would have a great enemy. If it is not true, we have to teach women that it's not true. I do not know if it is true or not, but we have to keep in mind that the breast is not only a place where women produce milk. It is a very important organ in the sexual relationship of couples.

Dr. Van Esterik

Most of the work that I have been doing this month at the Bellagio Study Center concentrates on the cultural construction of women's bodies. I'd like to argue that the breast is not universally a sexual symbol. It could be buttocks or legs or other body parts that are considered most attractive about a woman. But I agree with you in terms of having to consider breasts as sex objects. Hundreds of years of Cartesian dualisms, mind versus body, sexuality versus nurturance, maternity is over here and sexuality is over there. Breastfeeding advocates have a lot of work to do to show that this is not an either/or situation. It is both.

A woman was arrested in Ontario for obscene behaviour for taking her shirt off, and I was an expert witness. I spent two hours on the stand trying to argue that I could comment on ordinary breasts, not just lactating breasts. I argued that men's breasts and nipples are also sexually responsive and are also important in sexual foreplay, and women have to sit there and control themselves if a man takes his shirt off, and it's not considered obscene behaviour. Although there are differences, the differences must be culturally constructed, because you can go to beaches in parts of Europe and it's not shocking, as you mentioned the other day. But a woman breastfeeding on a nude beach that's what's shocking. Basically, we have to change the whole way we've been thinking for the last 500 years, so we have a lot of work to do.

Dr. Pollitt

I will play the devil's advocate. In a way, I don't think what Professor Hanson has presented is social construction, because there is no cultural constructivism in immunology or in many other biological aspects of breastfeeding I worry that if we emphasize the social behavioural component of breastfeeding too much, where is the seed for cultural constructivism? There may be a possibility of losing some strength in the argument of how important breastfeeding is from a biological perspective, and although I agree with you that one goes with the other, we must try to evaluate whether, by putting too much emphasis on cultural construct, we may lose some strength in the argument for the biological importance of breastfeeding.

Dr. Van Esterik

I think you have made the biological points pretty clearly over the last few days.

Dr. Garza

Well, it's brief, but it's important, I hope. Because we've constructed most of this discussion around changing behaviours, I'd like you to talk a little about how we protect the social constructs that exist, because we saw data earlier showing that 50% to 90% of women are breastfeeding. Thus, we seem to have a significant advantage in protecting a practice that does exist. How do we use the cultural constructs that have maintained this for the last 20 to 25 years?

Dr. Van Esterik

I don't have a clear answer. It is very important that we work with very local and specific understandings of infant feeding. We should pay much more attention to language and linguistic issues within communication campaigns to ensure we are using the words of the women we want to influence. In other words, we should put much more emphasis on the experiences of women themselves. I would hope that these experiences, in fact, will be parallel discourses. In other words, the scientific and the biological discourse will be much better understood if they are related to women's experiences, so that women's breastfeeding experiences will be much more prominent. I think these narratives are absolutely critical. I don't know how they would fit in with your research designs, but I don't see that they would do any harm as illustrating another way of thinking alongside the scientific papers on this topic.

The role of education in breastfeeding success

Veronica Valdand Janine Schooley

 

Abstract

Many of the factors that have contributed to the decline in breastfeeding around the world can be overcome by education and support. Examples of successful approaches to education at different levels (mother, health professional, institution) that impact breastfeeding are discussed. For example, because breastfeeding is a learned behaviour for both mother and baby, providing the mother with information, skills, and support for the breastfeeding process is integral to her ability to breastfeed successfully. In addition, because the health professional plays a pivotal role in the success or failure of breastfeeding it is essential I that education and training of health professionals be adequately addressed. By using an approach to healthprofessional education that builds on a highly trained core and spreads to all levels through a built-in multiplier effect, improvement of breastfeeding practices can be assured. In order to sustain these results, however, health-professional school curricula must include adequate information on the science of lactation and the clinical management of breastfeeding The experience of Chile's National Breastfeeding Programme is used to illustrate the power of education at each of these levels in influencing the success of breastfeeding and the feasibility of using education of both mothers and health professionals as a way of preserving this incredible natural resource.

 

Breastfeeding is a learned behaviour

Why does breastfeeding, something so biological, natural, and part of the essence of being a mammal, need to be taught and learned? Lactation occurs in every female after delivery as a biological response to hormones present in that period, and yet 38,000 infants die every day because they are not breastfed [1]. Clearly breastfeeding is a behaviour that needs to be learned for the survival of the species [2].

In nature, young females observe their elders caring for and breastfeeding their offspring. That experience will allow them to take care of their own when they reach reproductive age. A good example of the power of this experience is the case of a female gorilla named Dolly who had been raised at the San Diego Zoo. When she delivered her first offspring, she did not know what to do. She hugged the placenta and was afraid to touch the baby, whom she was not able to breastfeed. During her second pregnancy, the curators decided to teach her about mothering and breastfeeding. They showed her videos of mother gorillas in the wild nursing their infants and gave her a doll to teach her to be gentle in holding and nursing a baby. The teaching programme was a success, and she has been able to nurse and care for several other babies since then.

Something similar occurs with women in modern society [3]. With urbanization and the lack of extended families, most first-time mothers have not seen their mothers or relatives breastfeeding. Even worse, from everywhere around them they have been receiving the message that what is normal and modern is bottle-feeding. As young girls, they are given a doll and bottle to play with, and their mothers also probably bottle-fed. Formula companies advertise their products to the public, and for many women, this is their only source of information regarding infant feeding [4]. As more deliveries occur in hospitals, more women are influenced by hospital practices that often interfere with breastfeeding [1]. There, they do not receive the necessary support from the health-care team, because health professionals generally lack the knowledge and skills for good clinical management of breastfeeding [5]. In addition, an increasing number of women are working away from their homes and their infants.



FIG. 1. Percentage of tbe mothers exclusively breastfeeding at six months according to presence or absence of prenatal group education and parity

Therefore, the natural behaviour of breastfeeding is subverted by a variety of forces, as reflected in the often abysmal rates of prevalence and duration of exclusive breastfeeding.

 

Educating women about breastfeeding has a positive effect on breastfeeding performance

One way to minimize this interference with breastfeeding is through the education and support of mothers. Several studies show that providing breastfeeding education for women has a positive impact on the success of breastfeeding [6-11]. This impact has been underscored by results achieved at the Hospital of the Pontifical Catholic University of Chile, which showed a significant increase in exclusive breastfeeding at six months post-partum among women who received prenatal group education [12]. Eighty per cent of 59 women who received prenatal group education as part of a breastfeeding-promotion programme completed six months of exclusive breastfeeding versus 65% of the 363 who were part of the same study but did not receive prenatal group education (p < .003). This effect was even larger among primiparas, where only 57% of those who did not receive prenatal group education, versus 94% of those who did, were breastfeeding exclusively by the end of the sixth month (fig. 1).

These results were obtained in the context of a prospective study on the impact of a breastfeeding promotion programme on the duration of exclusive breastfeeding among lower-middle-class urban women. This study took place in the hospital and outpatient clinic of the Pontifical Catholic University in Santiago, Chile [13]. The study included a control group of 313 mother-infant pairs and an intervention group of 422 mother-infant pairs. Both groups were followed monthly for six months. Thirty-two per cent of the control group were able to complete six months of exclusive breastfeeding. This was, in fact, a relatively high prevalence, because only 2% of infants that age were exclusively breastfed according to a national survey carried out by the Ministry of Health in 1986. The higher prevalence in this population was due to the fact that the hospital of the Pontifical Catholic University has always promoted breastfeeding and had rooming-in, and medical and nursing students are taught that breastfeeding is important.

Before recruiting the study population, there was a need to develop a comprehensive programme designed to promote exclusive breastfeeding. The breastfeedingpromotion programme involved educating all health-care providers at the institution who take care of mothers and infants; changing policies that interfere with breastfeeding to make them more supportive of optimal breastfeeding practices, such as immediate contact between mothers and infants; delaying supplements or solid foods until the end of the sixth month if the infant is growing well; creating a Lactation Clinic to prevent and solve breastfeeding problems; providing breastfeeding education for women during the prenatal and postnatal periods, including how to breastfeed and how to prevent problems; and emphasizing the effect of exclusive breastfeeding on delaying the return of fertility and the use of the lactation amenorrhoea method for child spacing.



FIG. 2. Duration of exclusive breastfeeding before (control) and after (intervention) completion of a breastfeeding-promotion programme at the Pontifical Catholic University of Chile in 1993.



FIG. 3. Feeding status at six months among infants of working women

After the implementation of the breastfeedingpromotion programme, 67% of the study population completed six months of exclusive breastfeeding (fig. 2). The prevalence has even improved in the broader population cared for at the hospital of the Pontifical Catholic University after the institution of the Lactation Clinic and the use of the lactation amenorrhoea method by an increasing number of women. Education and support activities were developed for women who work outside the home. When mothers were taught how to hand-express and store their own milk and were offered monthly clinical follow-up, 47% of the working mothers were able to feed their infants exclusively with their milk for six months, and fewer than 6% of the 170 motherinfant pairs who were followed weaned before six months (fig. 3). None of the women in the control group (those not receiving education and support) who continued to work completed six months of exclusive breastfeeding. All of this happened in an institution where the personnel thought they were already promoting breastfeeding, but the results show that much more could be done. What made the difference?

 

Health-professional education is the cornerstone of improvement in breastfeeding practices

The difference was due to the intensive education of a core team of health professionals in the science of lactation and the clinical management of breastfeeding, and the resulting multiplier effect [14]. Before implementing the breastfeedingpromotion programme, a multidisciplinary team composed of a paediatrician and an obstetrician participated in Wellstart International's lactation management education programme. During their trip to San Diego for the course that would initiate their participation in the lactation management education programme, these professionals, like the hundreds of others throughout the world who have participated in the programme, asked themselves, "What can we learn that is new about breastfeeding and lactation during a whole month?" At the end of the four-week course, like all the others who have participated in the programme, they had acquired new knowledge and skills, shared experiences, and realized that lactation was such a broad topic that they had only just begun to learn. Wellstart's lactation management education programme is designed to develop core resources of expertise that can form the basis of teaching and promotion programmes at the institutional, national, and regional levels, using the following approach:

  • Education of educators. By recruiting teachers and decision makers who are in positions to influence institutional or national policy, the lactation management education programme has included a built-in multiplier or cascade effect that helps to ensure the continuation and expansion of the breastfeeding-related efforts to colleagues and families.
  • Provision of sound scientific foundation and clinical expertise. Preparing health-care professionals to teach others and gain the necessary respect and recognition from their peers requires a significant quantity and quality of current, scientifically sound information and the acquisition of associated clinical skills.
  • Selection of multidisciplinary teams. For breastfeeding promotion and support to be effective, families must receive coherent and consistent information from the entire health-care team. The lactation management education programme brings these disciplines together as working teams and models this approach within its own faculty.
  • In-country (or institutional) ownership of action plans. The programme focuses on providing participants with knowledge, skills, and resources and on assisting them to plan and carry out programmes of their own design, in their own countries.
  • Provision of teaching materials. Participant teams require tools to use and adapt for their own teaching and promotion efforts. Each team receives funds to pay for a selection of slides, videos, books, and a variety of teaching aids. These materials complement the syllabus, the textbooks, and a collection of over 1,000 relevant journal articles that become the basis of a lactation library for their institution.
  • Provision of follow-up. Field-based follow-up with an emphasis on institutionalization and sustainability is an essential component of the lactation management education programme. Once the participants have finished the four-week course, they become "associates" (not trainees, graduates, or alumni). This terminology reflects the ongoing, collegial nature of the relationship.
  • Factor X-the broader human experience. The term "factor X" is used to describe an intangible but essential ingredient of the lactation management education programme: the attention to detail and special treatment of participants, which helps lead to lifelong motivation, close relationships, and a sense of esprit de corps. There is an important intercultural exchange and sharing of experiences and memories that are necessary to balance the rigorous technical and programmatic curriculum.

The lactation management education programme has had an impact throughout the world, not so much because of what it has done, but because of the galvanizing effect its approach has had on others. By putting essential tools and resources into the hands of teachers and decision makers, the programme has served as a catalyst for a powerful multiplier effect in a number of countries. More than 550 associates from over 50 countries have participated in the lactation management education programme. In part because of their participation, National Breastfeeding Programmes are developing in more than 20 countries, National Training Centres in 13 countries, and Regional Training Centres in 5 countries. The impact is particularly great in countries where the UNICEF/WHO Baby-Friendly Hospital Initiative is under way, and many positive influences are at work. Chile provides an excellent example of the effect of health-professional education on breastfeeding. In October 1990 the results of the research project "The effect of a breastfeeding promotion program on the fertility of urban women in Santiago, Chile" [15] were presented in a three-day breastfeeding course for health professionals. The course was designed to offer participants basic knowledge on the anatomy and physiology of the mammary gland, clinical management of breastfeeding, updated benefits of breastmilk and breastfeeding, and the relation between fertility and breastfeeding, along with the results of the above-mentioned project and several others. Two years later, a questionnaire was sent to the participants to see if the course had had an impact on their actual practices and recommendations regarding breastfeeding. The results showed there were significant increases in clinical practices supporting breastfeeding, which included teaching the mothers and supervising breastfeeding techniques. The weaning recommendations given to mothers, including when to begin weaning foods and milk supplements and when to complete weaning, reflected a postponement of over two months compared with earlier practices (fig. 4) [16].

This course was also the beginning of a process of creating a critical mass of people with knowledge and interest in promoting and supporting breastfeeding throughout the country. By adopting many of the approaches used in the lactation management education programme, Chile developed its own cascade effect. In 1992, after the Innocenti Declaration and the World Summit for Children, the Chilean government created a National Breastfeeding Commission to develop a National Breastfeeding Programme. As part of that programme, the Baby-Friendly Hospital Initiative was launched in Chile with the support of UNICEF. The main emphasis and activities of the National Breastfeeding Programme, with the participation of the six Wellstart associates, have been educating health-professional teams on breastfeeding and developing teaching materials to help them disseminate that training. In 1992, 34 professionals, including teams from three hospitals, participated in the first Baby-Friendly Hospital Initiative Training for Trainers Workshop. These teams received teaching materials such as slides, videos, books, and syllabi to replicate the teaching at their institutions.. Since then two new workshops have been developed, attended by 142 new trainers who are now teaching the health teams in their own and neighbouring institutions.. By the end of 1994, more than 4,500 health workers had been trained throughout the country in replicated, 18-hour courses (fig. 5). Eleven hospitals have been designated as Baby-Friendly owing to their supportive practices for breastfeeding. In 1994 approximately 290,000 infants were born in Chile, with 52,000 of these births occurring in Baby-Friendly Hospitals.



FIG. 4. Recommended ages for initiating weaning, introducing cow's milk-based supplements, and completing weaning before professionals complete breastfeeding education course



FIG. 5. Numbers of health workers trained in Baby-Friendly Hospital Initiative workshops in Chile 1992-94

A national survey carried out at the end of 1993 showed that the prevalence of exclusive breastfeeding at six months had increased from 2% in 1985 to 25% in 1993 (fig. 6). In areas of the country where health workers in hospitals and community clinics have been trained, the percentage of exclusive breastfeeding at six months is more than 60%. These results show that there actually was a lack of knowledge among health workers on how to promote and support breastfeeding [17, 18], and that when they learn, they change their practices, which then have an impact on the prevalence and duration of breastfeeding in the community.



FIG. 6. Percentage of children and partially breastfed in Chile in 1993 according to age. Source: Ministry of Health National Breastfeeding Survey

The next step is to make this effort sustainable and costeffective. The only way to do this is to change what is taught at the university level and to include the scientific basis and clinical management of breastfeeding in the curricula of health-professional schools [19, 20]. This effort has already begun in many countries. A curriculum guide for medical, nursing, and nutrition training programmes has been developed by Wellstart and is beginning to be used in several universities in the United States, Latin America, and Africa. In Latin America two subregional workshops were hod for this purpose, one in Guatemala and another in Paraguay. A national pre-service curriculum workshop was held in the Pontifical Catholic University in Chile as the first activity of the National Breastfeeding Training Centre. The participants included representatives from schools of medicine, nursing, midwifery, nutrition, pharmacy, and dentistry from all the Chilean universities. In Africa a similar process is under way with the participation of 10 countries in east, central, and southern Africa.

Heal to-professional education is critical to making any kind of long-term-change in the way breastfeeding is promoted, supported, and protected. When health professionals are convinced that a breastfed child has the best start in life and really understand how breastfeeding works, they will send the right messages and give the needed support. Only then will the impact on the community be sustainable and something as natural as breastfeeding be preserved.

 

References

1. Jolly R. Breastfeeding and health care services. Int J Gynaecol Obetet 1990-,31(SUPPL 1):7-9.

2. Lawrence RA. Physiology of lactation. In: Breastfeeding: a guide for the medical profession. St. Louis, Mo, USA: Mosby-Year Book, 1994:59-89.

3. Lawrence RA. Breastfeeding in modern medicine. In: Breastfeeding a guide for the medical profession. St. Louis, Mo, USA: Mosby-Year Book, 1994:1-35.

4. Auerbach KG. The many ways of marketing artificial baby milk. l Hum Lactation 1992;8:61-2.

5. Freed GL, Clark SJ, Sorenson J, Lohr JA, Cefalo R. Curtis P. National assessment of physicians' breastfeeding knowledge, attitudes, training and experience. JAMA 1995;273:472-6.

6. Gupta A, Gupta R. Obstetric and infant feeding practices ID Punjab: effect of educational intervention. Indian Pediatr 1992; 29:333-5.

7. Hill P. Effects of education on breastfeeding success Matern Child Nurs J 1987;16:145-6.

8. Hoffman MN, Durcan NM, Disler PB. Breast-feeding in a socio-economically disadvantaged area of Cape Town. Part II. The introduction of an educational and support program. S Afr Med J 1984;66:66-7.

9. Kistin N. Benton D, Rao S. Sullivan M. Breastfeeding rams among black urban low-income women: effect of prenatal education. Pediatrics 1990;86:741-6.

10. Libbus MK. Lactation education practice and procedure: information and support offered to economically disadvantaged women. J Commun Health Nurs 1994; 11:1 -10.

11. Wiles LS. The effect of prenatal breastfeeding education on breastfeeding success and maternal perception of the infant. J Obstet Gynecol Neonat Nurs 1984;13: 253-7.

12. Pugin E, ValdV, Labbok MH, Perez A, Aravena R. Does prenatal breast-feeding skills group education increase the effectiveness of a comprehensive breastfeeding promotion program? J Hum Lactation 1996; 12:15-20.

13. ValdV, Perez A, Labbok MH, Pugin E, Zambrano 1, Catalan S. The impact of a hospital and clinic-based breastfeeding promotion program in a middle class urban environment. J Trop Pediatr 1993;39:142-50.

14. Naylor A. Professional education and training for trainers. Int J Obstet Gynecol 1990;41:25-7.

15. Perez A, ValdV. Santiago breastfeeding promotion program: preliminary results of an intervention study. Am J Obstet Gynecol 1991;165(suppl):203944.

16. ValdV, Pugin E, Labbok MH, Perez A, Catalan S. Aravena R. Adler BA. The effects on professional practices of a threeday course on breastfeeding. J Hum Lactation 1995;11:185-90.

17. Goldstein AO, Freed GL. Breast-feeding counseling practices of family practice residents. Fam Med 1993; 25:524-9.

18. Lawrence RA. Educating and training the medical profession. In: Breastfeeding: a guide for the medical profession. St. Louis, Mo, USA: Mosby-Year Book, 1994: 647-52.

19. Naylor AJ, Creer E, Woodward-Lopez G. Dixon S. Lactation management education for physicians. Semin Perinatol 1994;18:525-31.

20. Wellstart International and the University of California San Diego. Woodward-Lopez G. Creer E, eds. Curriculo pare el manejo de la lactancia: una guia pare el personal docente de las escuelas de medicine, enfermeria y nutrici1st Spanish ed. San Diego, Calif, USA: Wellstart International, 1995.

Discussion of paper by Valdés and Schooley

 

Professor Howie

I suggest that factor X is important, and it almost comes back to the sort of things that Dr. Van Esterik was talking about. It is the whole culture and atmosphere, and I was very impressed with that picture of the maternal support group. It was the warmth and the smile of the health professional in the middle of the group that really made an impression on me, and I don't know if the other people in the group felt the same thing. I felt that she was exuding a very large dose of factor X. The real challenge is how to get everybody exuding factor X. It has to do with smile and atmosphere and less to do with the mechanics of the videos and the material. I suspect that factor X is the key to the sort of things that you are achieving.

Dr. Vald/strong>

I think the important thing is that factor X is contagious. Once you learn the style, you can't make a traditional, boring course. Now, people get there and they are received maybe with candy, maybe with some touching things. That's the only place where working women come and charge their batteries. The doors are open, they sit, they chat. We have become sexual psychologists because all their concerns come to us and they are heard. I think that's the reason they come back to the programme. They follow us, and they believe us.

Dr. McNeilly

When Professor Howie and I set up the first breastfeeding study in Edinburgh, we were aiming to recruit 200 women. We assumed the average time of breastfeeding was four months, so there would not be a problem. We would finish the study in two years. We had to have a meeting after four months, because none of the 20 women who had entered the study at that point had even thought to stop breastfeeding. We couldn't understand why, but the reason was that the research nursing sister who was recruiting them, Mary Houston, talked to these women about problems with breastfeeding, children, anything. They kept going because they would save their problems up, and she would visit them every two weeks, and they would keep going until she arrived and pour out their hearts to her. She would fix it, and they would carry on. Now, having subsequently done a study on that, we found that the difference between the women who gave up and the women who carried on was not that they had fewer problems or anything like that; it was just that they had somebody whom they could rely on to discuss their problems with, and Mary Houston certainly had factor X. So, I think that from our point of view, we stopped at 45 women rather than 200 because factor X interfered with the programme.

Dr. Garza

I enjoyed the presentation. It obviously shows what one can do with a good system. But I was struck by the complexity of what is needed, because we have dismantled the family structure that used to support it, and in some ways there are parallels with formula. Whenever we try to replace a natural system with an artificial one, we keep discovering that many things are missing. I'm wondering what you are doing to get yourself out of business. Because that would be our ultimate success; that is, when we wouldn't need those very complex systems to replace a family structure.

Dr. Vald/strong>

I'm trying hard to get out of business. First, by including breastfeeding in the medical curriculum so we don't have to retrain professionals. I think the next step would be to include breastfeeding in the schools and change what children are taught in school. I have now gone to my children's school because I'm horrified at what they teach them. That would be another step. When you see that 60% of the mothers are breastfeeding, these children will have had the opportunity to have seen breastfeeding in action. So, I think we are reversing the situation.

Dr. Lawrence

A very nice presentation. I would add that before we change things completely, we have to go back to the school system. In New York State we have created, with the Department of Education, a curriculum for kindergarten through high school that is currently on trial in one part of the state. Our aim is to educate all children, not just girls, that breastfeeding is normal and to put it into the curriculum: not to have them take a course in breastfeeding, but to have it as part of the curriculum. The second piece is the education of the health-care professional, and that, too, needs to be part of the total curriculum and not something you can choose or not choose. We have tried a model programme doing that as well, in which our first-year medical students get something about the value of human milk in their nutrition course. They get the anatomy and physiology of the breast in their second-year course on women's health, and in the third year all of our students spend a week in the newborn nursery, seeing mothers, helping them breastfeed, and learning what the practical questions are. But, in response to Dr. Garza's comment, we have to weave it into the normal curriculum for everybody in their culture, plus the health-care professional.

Dr. Vald/strong>

I completely agree, and it is important that it be present in all of the schools to send the same message.

Dr. Perez

I discovered Veronica Valdin 1985, and because we had to start a research project, I asked her to go to Wellstart. She stayed there a little over a month. When she came back, the first thing she did was to give us a one-day workshop on breastfeeding. There were 18 obstetricians and gynaecologists from Catholic University's Department of Obstetrics and Gynaecology. Some of us have been in this department almost 40 years, several of us have a lot of experience, and some of us have some background in breastfeeding research. After the one-day workshop, we could not believe how much we had learned about very simple breastfeeding techniques. I'm sorry Dr. Valddidn't talk about how to teach a woman to breastfeed, because she knows a lot about that, and she is a genius about that very simple thing. We, with 40 years of practice, did not understand that, and she, after being in Wellstart, taught us in a fantastic way. I believe this first step of Dr. Valdin our university is a very important step in any breastfeeding programme, which is to teach the health team.

Dr. Vald/strong>

Thank you, Dr. Perez. It was quite a challenge, because we had to teach our teachers.

Summary of the workshop

 

Scientific experts in fields concerned with the health and well-being of children and their mothers recognize breastfeeding as the best way to nourish infants and to promote the post-partum and possibly the longer-term health of women. This consensus led the world community more than 20 years ago to recommend that infants be breastfed exclusively for four to six months, with continued breastfeeding for two years or longer.

 

Benefits to the infant

The benefits to the infant fall into three broad categories: nutritional, immunologic, and behavioural. Reviews of the world's scientific literature by the Working Group reaffirmed the strength of the conclusions regarding the nutritional and immunologic benefits and led to an acknowledgement of the potential for significant behavioural advantages.

Nutritional benefits

It is clear that the nutritional benefits to infants extend through the periods of exclusive and partial breastfeeding and possibly beyond the latter period. The high nutritional value of human milk conferred by the high bioavailability of its nutrients, the balance of specific nutrients, and other characteristics is of significant advantage to all infants. It is of most value, however, to infants of families with low economic resources. Human milk substitutes accessible to those infants generally are unsafe because of their inferior nutritional quality and frequent contamination with potentially fatal infectious agents.

The bacteriologic safety and high nutritional value of human milk argue strongly for maximizing the intake of human milk, especially among infants of the poor. This is especially important when other foods are added to the infant's diet. Added foods are of inferior quality, are often bacteriologically contaminated, and generally displace human milk, thereby raising the risk of infection and malnutrition in children living in unsafe environments. Although there are recent data that support the extension of exclusive breastfeeding beyond six months among some infants, the published data remain too limited to conclude that the period of exclusive breastfeeding should be extended universally beyond the current recommended period of four to six months. There is no controversy, however, regarding the important role of human milk in supplying essential nutrients to the child during the period of mixed feeding.

The major possible exceptions to the full adequacy of exclusive breastfeeding relate to vitamins K, D, and B12. Although there is some disagreement, most medical scientists continue to recommend vitamin K supplementation at birth for all infants, regardless of feeding mode, to prevent haemorrhagic problems in the newborn. Infants with limited exposure to sunlight, or those whose mothers had low vitamin D stores because of low vitamin D intake or limited sun exposure, should receive vitamin D supplements. Infants of strict vegetarians who do not eat eggs or milk products also run the risk of vitamin B12 deficiency and should be provided with an exogenous source of this essential nutrient.

Maternal malnutrition also may result in abnormally low levels of some nutrients in human milk. Generally, however, even women living under very harsh conditions will provide sufficient milk of adequate quality to breastfeed infants exclusively for four to six months. More importantly, circumstances that lead to maternal malnutrition almost uniformly result in malnutrition and serious infectious morbidity among non-breastfed infants. The mortality rates of non-breastfed infants in these circumstances are estimated to be 12 times higher than those of breastfed infants.

The contamination of human milk by xenobiotics may present safety concerns in some circumstances. Situations in which environmental pollutants, such as heavy metals and organohalides, may contaminate human milk should be evaluated carefully; however, attention must always be given to the benefits and risks presented by the exclusion of human milk and the use of its substitutes. In these circumstances exposure of the infant obviously begins in utero, thus making it more imperative to attend to the contamination of the environment.

The major biological xenobiotic of concern is the human immunodeficiency virus (HIV), which is responsible for the acquired immunodeficiency syndrome (AIDS). Although it is clear that human milk may carry HIV, controversy remains as to the conditions that determine the infectivity of HIV in human milk. There is no controversy, however, that the benefits of human milk are much greater than the risks presented by HIV in areas characterized by high rates of infant mortality and malnutrition.

Immunologic benefits

In addition to serving as the most reliable, safe, and nutritious food for infants, human milk provides unique immunologic benefits, which result in decreased rates of infection and other desirable outcomes. In the recent past, scientific evidence was limited to the likelihood that human milk conferred passive protection; that is, protection against infectious disease occurred because of the direct interaction between specific milk components and potential pathogens that threaten the infant. However, there was little evidence to support the hypothesis that human milk alters the development of the infant's immune system to provide active as well as passive protection. Data reviewed by the Working Group support the idea that both active and passive mechanisms likely account for the decreased infectious morbidity observed in infants in both economically developing and fully industrialized nations. Of particular interest were data from the United Kingdom demonstrating that breastfeeding for at least 13 weeks had protective effects against gastrointestinal and, to a lesser degree, respiratory infections that lasted beyond weaning.

Recent studies have demonstrated that breastfeeding enhances responses by the infant to infectious challenges. Enhanced responses were noted following the administration of parenteral vaccination with diphtheria and tetanus toxoids and Hib (Haemophilus influenzae type b)-protein conjugate, oral poliovirus, and "natural" infections with respiratory syncytial virus. The mechanisms responsible for these responses are the subject of intensive investigations. It is likely that both the high nutritional quality of human milk and its complex immune components (e.g., various growth factors, cytokines, and antiinflammatory factors) are responsible for the improved immune function of breastfed infants.

The combined nutritional and immunologic protective effects of human milk against diarrhoeal disease result in a reduced incidence and severity of the disease. As a consequence, breastfeeding protects strongly against diarrhoeal mortality, especially in young infants. Although partial breastfeeding is protective, maximal protection is achieved with exclusive breastfeeding. A reduction in the incidence of respiratory disease is less clearly established, but breastfeeding does appear to reduce the severity of respiratory illness, as reflected by hospitalization rates and mortality. There also is fairly consistent evidence that breastfeeding protects against otitis media, but the effect is less than that seen for diarrhoeal diseases. Evidence for protection against other infectious diseases is less clear, but nonetheless suggestive. Theoretical mathematical projections based on data obtained from the World Health Organization indicate that a 40% reduction in the prevalence of non-breastfeeding would result in a 50% reduction in respiratory deaths and a 66% reduction in diarrhoeal deaths worldwide in children 18 months old or younger.

Evidence also was reviewed which suggests that the immunologic benefits may last for a longer term. Investigators have reported that for years after breastfeeding has ceased, breastfed infants have a significantly lower risk than bottle-fed infants of developing type I diabetes, Crohn's disease, and Iymphomas in childhood.

Behavioural benefits

Behavioural benefits are more difficult to document. Although it is highly plausible that specific constituents of human milk enhance the infant's neural development and that suckling at the breast promotes desirable emotional ties between mother and infant, objective experimental evidence in support of the hypothesis that breastfeeding directly enhances the infant's behavioural development is limited. The usefulness of most published investigations is restricted by inadequate study designs, inappropriate evaluation tools available to or selected by the researchers, and an overly narrow focus on developmental outcomes, such as IQ scores and psychomotor indices. The narrowness of the focus excludes consideration of interactions between feeding mode and other potentially important modulators of behavioural development (such as reductions in morbidity) and disregards the processes that underlie development. Furthermore, very little attention has been given to the alternative possibility that breastfeeding may limit mental development through, for example, the transfer to the child of toxic substances in milk. This alternative is complicated by the confounding likelihood that the infant's exposure to toxicants is initiated during gestation, the period of maximal vulnerability.

Even when these caveats are acknowledged, previously breastfed children appear to have an advantage over bottlefed children in developmental scales, IQ tests, and assessments of other specific cognitive outcomes. Among the most provocative observations are the positive effects on IQ of feeding human milk to premature infants. Although the workshop participants acknowledged controversial aspects of those observations, the need to replicate such studies was recognized widely. The consistency of the evidence argues strongly for evaluations with more robust designs and evaluation tools. Such investigations should permit inferences regarding the nature, degree, and persistence of the potential effects of breastfeeding or human milk feeding on behavioural development and the assessment of the modulation of putative effects by social, economic, and other environmental factors.

 

Benefits to the mother

Maternal benefits also fall into three broad categories: reductions in fertility, health benefits of a non-behavioural nature, and positive behavioural outcomes. The Working Group examined the first and second categories in greater detail than the third.

Generally, lactation is expected to help women maintain a healthy body weight when sufficient quantities of adequate food are readily accessible and to enhance the physiological efficiency of nutrient utilization under nearly all conditions. The hormonal changes that accompany lactation are expected to influence maternal behaviour in ways that support breastfeeding and promote mothering behaviours. Investigators also have suggested that successful breastfeeding is important to maternal self-efficacy and possibly social empowerment. These expectations likely are most relevant when maternal nutritional and social needs are met.

The mother's responses to breastfeeding have been studied much less than those of the infant. A principal limitation is that lactation seldom has been studied in the context of the complete reproductive cycle, which includes the nulliparous period, pregnancy, lactation, and the nonlactating, non-pregnant state that precedes a subsequent pregnancy. The significance of this omission stems from the likelihood that biological strategies for maintaining maternal well-being through the life cycle rely on a healthy physiological preparation for reproduction and adequate pregnancy intervals for maternal repletion. Interactions among the contiguous and interdependent stages within reproductive cycles and the biological effects of the distinct socio-economic, demographic, and environmental conditions in industrializing, newly industrialized, and post-industrialized settings are expected to modulate maternal responses to lactation.

Health consequences

Insufficient data were available to the Working Group for an assessment of the effects of lactation on the prevention of maternal obesity and nutrient depletion. Although obesity is of most concern in fully industrialized and newly industrialized nations, it is, ironically, a growing problem among some developing countries with large numbers of undernourished women of reproductive age. Similarly, the paucity of data makes it difficult to assess the global impact of lactation on nutrient depletion of the mother and its potential consequences for maternal and infant health.

Issues related to longer-term health outcomes, that is, osteoporosis and breast cancer, were addressed more confidently. Concerns that lactating women may be at greater risk of osteoporosis because of loss of calcium in milk have not been supported by recent studies conducted largely in affluent countries. Current evidence supports a preventive effect of breastfeeding against pre-menopausal breast cancer, but no association has been found between breastfeeding and post-menopausal disease.

Fertility

Data reviewed by the Working Group reaffirmed the suppression of fertility by breastfeeding. The duration of the mother's infertility is directly dependent on her infant's suckling activity. Breastfeeding is most effective in decreasing fertility (and thereby facilitating longer, more desirable interpregnancy intervals) when infants are breastfed on demand and are provided no other sources of food or water. There also are data suggesting that the use of pacitiers may lessen the effects of breastfeeding on fertility by decreasing the infant's suckling activity.

The mean anovulatory period for non-breastfeeding women appears to be approximately 50 days. In breastfeeding women, anovulation may persist well into the second year post-partum. Infertility appears to be maintained by a suckling-induced disruption of the normal pulsatile pattern of luteinizing hormone (LH) release (essential for ovulation) and facilitated by an increased hypothalamic sensitivity to the negative feedback effects of oestradiol. The mechanisms responsible for these maternal responses to lactation have not been identified but are sufficiently reliable to have led a group of investigators to conclude that when women fully or nearly fully breastfeed and remain amenorrhoeic, breastfeeding provides more than 98% protection from pregnancy in the first six months post-partum. The programmatic implementation of this conclusion is known as the lactational amenorrhea method (LAM) of natural family planning.

Any biological or social factor that either promotes or interferes with the infant's suckling activity (such as a delay in the introduction of complementary foods or the inappropriate or premature introduction of supplementary or complementary infant foods) will, respectively, prolong or shorten the duration of infertility. Discussions on the control of milk synthesis were particularly relevant to these considerations. It is clear that milk synthesis is under autocrine (local) control. The frequency and degree to which the breast is emptied are the principal determinants of the quantity of milk that is produced. Generally, interference with the suckling activity of infants will be reinforced by a subsequent decrease in milk production. Under such conditions, feedback mechanisms will lead to progressive decreases in suckling, which, in turn, will disable mechanisms that disrupt pulsatile release of LH and eventually result in an earlier return of ovulation.

Demographic effects of breastfeeding

The Working Group examined the demographic effects of the impact of breastfeeding on fertility and infant mortality. It reviewed the impact of breastfeeding on one of the two principal proximate determinants of fertility, the rate of births. The other proximate determinant, the reproductive span (the interval between a woman's first ovulation and the time she either dies or becomes infertile), was not considered, because breastfeeding is not thought to influence it.

The effects of breastfeeding on the dynamics of birth intervals may be examined by dividing the birth interval into three parts: the post-partum period (the time between delivery and the resumption of both ovulation and sexual intercourse), the time between the end of the post-partum period and the next birth, and the period of the pregnancy associated with a live birth. Endocrine responses that make lactation possible prolong post-partum anovulation and amenorrhoea through mechanisms that have been reviewed briefly in the preceding section and regulate other reproductive functions (such as luteal function) through mechanisms that are understood less comprehensively. A semi-quantitative assessment of the impact of these effects on fertility suggests that a woman's lifetime fertility may be reduced as much as 50% by prolonged breastfeeding.

The demographic impact, however, also will be influenced by the effect of infant-feeding practices on child survival. Unlike the semi-quantitative assessments of the effects of the proximate determinants of fertility on population growth, the impact of the proximate determinants of child mortality on population growth has been more difficult to estimate. Six types of factors have been identified among the principal determinants of child mortality: maternal characteristics, environmental contamination, nutrient deficiency, injury, personal illness control, and the gestational age and development of the newborn. The first three are influenced greatly by breastfeeding.

The relations among breastfeeding, fertility, and child mortality are confounded by the socio-economic changes that often accompany changes in breastfeeding patterns. The socio-economic conditions that traditionally have led to decreases in the incidence and duration of breastfeeding tend, over the long term, to have a beneficial effect on the six factors listed above and to diversify and increase the use of contraceptive strategies for birth control. Nonetheless, if socio-economic changes are ignored and the positive impact of breastfeeding on fertility and child mortality on population growth is assessed, it appears that long-term breastfeeding (i.e., breastfeeding into the second year of the child's life) is likely to have only a limited effect on population growth. This, however, does not diminish the health benefits to both mother and infant anticipated from increased birth spacing and the nutritional and immunologic benefits discussed previously.

 

Current worldwide breastfeeding trends

The Working Group also reviewed data from demographic and health surveys conducted from 1990 to 1993. It is alarming that under-five mortality remains excessive by any measure in much of the world. For example, in 13 African countries for which data are available, mortality among children between one and four years of age ranged from 318 per 1,000 live births in Niger to 83 per 1,000 in Namibia. As in all regions, infant mortality in those 13 countries generally accounts for an increasing proportion of underfive mortality as the under-five mortality rate drops.

It is very likely that improved breastfeeding practices will have a significant impact on child mortality in nearly all economically developing countries. The term "breastfeeding practices" deserves emphasis, because the percentage of children born in the last five years who were ever breastfed ranged from 95% to 97% in the same 13 African countries for which mortality data are available. The percentages of children ever breastfed were similarly high (greater than 90%) in the Asian, South Pacific, and Latin American countries for which data are available.

In most developing countries that were surveyed, substantially more than 50% of all infants were breastfed up to 12 to 15 months of age, and more than 25% were breastfed up to 20 to 23 months. The median duration of breastfeeding among children born in the last three years ranged from 17 to 28 months in the African countries that were surveyed. No economically developing country in the regions surveyed had a mean duration of breastfeeding below six months, and in most countries the mean durations were substantially above that level. Yet, consistently across all countries surveyed, the mean duration of breastfeeding was from 5% to nearly 100% greater in rural than in urban areas. In most countries, a minority of infants were fed only human milk through four months of age, although rates varied widely among those countries surveyed. For example, 90% of Rwandan infants were reported to receive only human milk through four months of age. The rates in Tanzania, Kenya, Madagascar, and Namibia ranged from 17% to 47%, and the rates in Burkina Faso, Ghana, Malawi, Niger, Senegal, Nigeria, Zambia, and Cameroon ranged from 1% to 13%. Rates were similarly divergent in other regions of the world. The percentages of infants whose diets were restricted to only human milk and water were similarly divergent among countries but were substantially higher than the percentages of those receiving only human milk.

 

Sociocultural factors affecting breastfeeding

Breastfeeding is a learned, not an instinctive, behaviour. Desirable breastfeeding practices must be actively promoted and supported. Successful breastfeeding, therefore, is dependent upon social and cultural factors. Major shifts in breastfeeding practices in fully industrialized countries over the last 30 to 40 years and rural-urban differences in most economically developing countries provide the best evidence of the great influence of sociocultural factors on breastfeeding. The best predictors of breastfeeding practices in fully industrialized countries are sociocultural rather than biological. This also is increasingly true in the industrializing countries, especially in those that are urbanizing quickly. However, recognizing the importance of sociocultural factors in determining infantfeeding practices does not lessen the difficulty of understanding how specific sociocultural factors operate or may be measured adequately to explain variations within and between different infant-feeding patterns.

The sociocultural factors that have been examined most often are those that can be integrated easily into biomedical and epidemiologic models, such as religion, martial status, education, and kinship patern. These often are included in assessments of knowledge, attitudes, and beliefs. Yet because infant feeding, and breastfeeding in particular, represents a wide range of highly emotional issues, it is often difficult to obtain reliable and valid data from informants in most studies.

Other factors are less commonly studied, because they are more difficult to assess. For example, factors reflective of values, attachment, nurturance, and sexuality require interpretation from social science paradigms and are not as amenable to reductionist models. Nonetheless, all of these factors probably contribute significantly to the links among what people say they know, what they know, and what they practice.

As long-term, detailed ethnographic analyses have become increasingly available, a conceptual model has emerged that describes culture as an interaction between style and structure. Style refers to the manner of expression characteristic of an individual, a time, and a place. The application of this model is expected to increase understanding of the influence of sociocultural factors on breastfeeding. Infant-feeding styles communicate fundamental values, attitudes, and beliefs reflected in the interaction between mother and infant during feeding, in how breastfeeding is accomplished, and so forth. These styles of feeding are part of dynamic trends and fashions.

Styles in turn are in a dynamic interaction with defined organizational and institutional structures, such as those related to health care, the economy, and governments, each with its own potential influence on infant-feeding choices. An improved understanding of relevant styles and structures should enhance our ability to predict how infant-feeding choices will be affected by changes in sociocultural factors.

Despite these limitations, a comparison of the effects of biological and sociocultural factors on measures of breastfeeding success (for example, prevalence and duration) strongly suggests that breastfeeding is biologically robust but highly susceptible to positive and negative sociocultural influences. The principal basis for this conclusion is that breastfeeding is sustainable under the wide range of biological conditions characteristic of affluent women in economically developed countries and of poor women in harsh environments in less economically developed areas. This is not true when breastfeeding is considered under an analogously wide range of sociocultural conditions relevant to breastfeeding. Although it would be a mistake not to recognize the cost that this characteristic presents to poor women (that is, to their biological wellbeing), it is equally fallacious to conclude that adequate breastfeeding can be accomplished only when all biological needs are optimally met.

 

Resources needed to protect, support, and promote breastfeeding

The information reviewed by the Working Group did not allow a prioritization of resources needed to protect, support, and promote breastfeeding. It did allow the group, however, to identify resources that would enhance the likelihood of successful lactation in nearly all settings. The paucity of quantitative information available to assess the relative importance of resources needed in specific settings represents a major research gap. The resources identified by the group fell into three broad categories: time, space, and sociocultural/economic support.

The physiological and sociocultural information reviewed by the group documented clearly that breastfeeding requires time of the mother. The two principal sources and sinks of time are the family and, when the mother also is employed outside the home, her employer. Because milk production is sustained by physiological processes dependent upon the regular removal of milk, time constraints that result in decreased or inefficient suckling will have a negative impact on milk production and eventually on the sustainability of adequate milk production. Time constraints imposed by employers have marked negative impacts on breastfeeding success because of adverse effects on suckling. Employment policies that recognize the importance of maternal leaves, temporary parttime employment options that do not adversely affect longer-term full-time employment opportunities, and opportunities for breastfeeding in the workplace represent complementary strategies to help establish and sustain adequate lactation.

Space is required to breastfeed. Differing perceptions of physical modesty, hygiene, and other concepts dependent upon cultural norms and relevant to infant feeding and maternal well-being will make diverse demands on the characteristics of spaces best suited for the protection, support, and promotion of breastfeeding. These demands apply to family residences, places of employment, and various sites where communities congregate, such as places of worship, businesses, and entertainment.

Sociocultural and economic support fall into two subcategories, tangible and intangible support. Examples of the types of tangible support needed to obtain full benefits of breastfeeding are safe and adequate food for the mother and complementary infant foods for the period of mixed feeding when foods other than human milk are introduced to the infant's diet; fair labour compensation that recognizes the needs of families; and adequate housing and related services that protect, support, and promote the hygienic well-being of the family.

Examples of intangible support tended to centre around five social sectors: government, business, community, health professions, and educational and research institutions. Those which centre around government represent a wide range of issues. They extend from laws and policies that govern parental leaves to those that lead to differing urbanization trends. Parental leave policies are of obvious relevance; urbanization trends influence family support structures and employment patterns, which affect the protection, support, and promotion of breastfeeding.

Although the Working Group recognized the significant influence that the commercial sector plays in determining parental and family leave policies of specific countries, the negative impact of both overt and subtle inappropriate marketing practices by producers of infant foods received more focus. Strategies that have a negative impact on breastfeeding appear designed to decrease suckling at the breast, thereby causing decreased milk production, with increased dependence on human milk substitutes, and undermining maternal confidence in the ability to breastfeed and the general social support of breastfeeding. These strategies are implemented by such diverse activities as direct advertisement to the public and the now discredited distribution of human milk substitutes at little or no cost in health-care settings or directly to family residences. Other issues relevant to the commercial sector's employment policies and the impact of these policies on the time mothers have to breastfeed have been discussed previously.

The issue common to communities-at-large, health professions, and educational and research institutions is recognition of breastfeeding as the expected mode of feeding for all infants and, its corollary, the use of human milk substitutes only when specifically indicated. Although all agencies and institutions with interests in infant health recommend exclusive breastfeeding for at least the first four to six months, these recommendations are not commonly reflected in the practices of communities, health professionals, and educational and research institutions. Examples of the consequences of failing to make practices conform with recommendations are inappropriate management of lactation by health professionals who have received inadequate training, poor knowledge and attitudes of many young families relative to breastfeeding because of inattention to lactation in primary and secondary education, and a poor knowledge base for the improvement of lactation practices because of inadequate research support.

 

Conclusions and recommendations

The data reviewed by the Working Group provide a strong scientific base for the present recommendations. The present benefits of breastfeeding in all countries and the benefits that are projected when international recommendations are implemented more broadly are of great significance to individuals and organizations responsible for the implementation of scientific knowledge that is highly pertinent to infant and maternal health.

The Working Group urges the active protection, support, and promotion of breastfeeding by governments, communities, the commercial sector, educational and research institutions, voluntary organizations responsible for the promotion of maternal and infant health, and, in particular, health professionals and facilities. Especially relevant to this recommendation is the resilience of lactation in the face of harsh biological conditions and the fragility of breastfeeding in the face of inadequate sociocultural and economic support. These characteristics impose a special responsibility on all societies to safeguard the well-being of women by ensuring their access to a safe and adequate food supply throughout their life cycle and to provide adequate time, space, and sociocultural and economic support to women and their families to maximize the health of all children from infancy and the health of women throughout the reproductive cycle.

Books received

Basic calculations for chemical and biological analyses. Bassey J. S. Efiok. AOAC International, Gaitersburg, Md., USA, 1993. (ISBN 0-935584-51-X) 135 pages, paperback. US$45 (USA, Canada, Mexico), US$55 elsewhere.

This book is neither new nor explicitly nutrition-related, but it is exceedingly convenient and useful for the kind of calculation that every nutrition or food scientist is required to make from time to time. It contains the information necessary for calculating the amount, concentration, and preparation of reagents, buffers, spectroscopy, enzyme assays and activities, and radioactivity. Anyone still concerned in any way with calculations of laboratory data will find this inexpensive paperback invaluable.

 

Carcinogens and anticarcinogens in the human diet. A comparison of naturally occurring and synthetic substances. National Research Council. National Academy Press, Washington, D.C., 1996 (ISBN 0-30905391-9) 417 pages, paperback. US$44.95.

Plants contain chemicals that have medicinal stimulatory, hallucinatory, and narcotic effects, so it is not surprising that they also contain chemicals that are protective against or contributory to cancer. The US National Research Council committee responsible for this report was charged with examining the occurrence, toxicological data, dosage, mechanisms of action, and potential role of natural and synthetic carcinogens and anticarcinogens in food. Despite their enormous number in the food supply, the great majority of naturally occurring and synthetic chemicals in the diet are present at levels below those at which any significant adverse biological effects are likely. Moreover, a varied and balanced diet contributes significant protection. The committee concluded that natural components in the diet may prove to be of greater concern than synthetic components with respect to cancer risk. Even though human epidemiologic data indicate that diet contributes to a significant portion of cancer, it is extremely difficult to assess human cancer risk from individual natural or synthetic compounds, because the diet is such a complex mixture and interactions among components are largely unknown. The report documents and discusses these conclusions.

 

Trace elements in human nutrition and health. World Health Organization, Geneva, 1996. (ISBN 92-4-156173-4) 343 pages, paperback. SwF 85/ US$76.60; SwF 59.50 in developing countries.

This book provides authoritative recommendations concerning nutritional requirements and safe ranges of intake for 19 trace elements important to human health, based on a consensus of international experts. It combines the latest scientific knowledge about the consequences of specific dietary intakes with practical advice on how to identify the effects of deficiencies and excesses of trace elements. Recommendations for individual elements are presented in the form of safe ranges of intake for population groups and represent the limits of adequacy and safety for the mean intakes of whole populations. The final chapters provide detailed guidelines for the design and interpretation of research on trace elements for human consumption. These include analytical methodologies, dietary surveys, environmental supplies of trace elements, and the differences between population averages and individual intakes.

This book is essential for every nutrition library; it is unfortunate that it cannot be made available even more cheaply for developing countries. A French edition is in preparation.

 

Vitamin A and the immune function. Edited by Chris Kjolhede and William R. Beisel. Haworth Medical Press, New York, 1996. (ISBN 1-56024757-6) 156 pages, hardback. US$29.95.

This is the report of a 1993 symposium that dealt broadly with vitamin and immune function from basic biochemistry to applied epidemiology and clinical practice. It includes basic information on the metabolism and mechanisms of action of vitamin A, with special reference to infection and immunity, the effects of vitamin A on B-cell and T-cell function, and the complex relationship of vitamin A status, supplementation, and immunocompetence. A comprehensive historical overview by Dr. Beisel provides valuable background. In addition to its authoritative summary of current knowledge, the book will be useful for the design of future indepth investigations.

Note for contributors

The editors of the Food and Nutrition Bulletin welcome contributions of relevance to its concerns (see the statement of editorial policy on the inside of the front cover). Submission of an article does not guarantee publication-which depends on the judgement of the editors as to its relevance and quality. Contributors should review recent issues of the Bulletin for content and style.

Language. Contributions may be in English. French. Or Spanish. If French or Spanish is used. the author should submit an abstract in English if possible.

Format. Manuscripts should be typed. double-spaced. with ample margins. Only an original typed copy or a photocopy of equivalent quality should be submitted: photocopies on thin or shiny paper are not acceptable.

When a manuscript has been prepared on a word processor, it will he appreciated if a floppy disk. either 3 1/2 - inch or 5 1/4 - inch, can be included with the manuscript. with an indication of the disk format and the word-processing program used.

Length. Ordinarily contributions should not exceed 4,000 words.

Abstract. An abstract of not more that 150 words should he included with the manuscript. The abstract should state the purposes of the study or investigation. basic procedures (study subjects or experimental animals and observational and analytical methods). main findings (give specific data and their statistical significance if possible), and the principal conclusions. Emphasize new and important aspects of the study or observations. Do not cite references or use abbreviations or acronyms in the abstract.

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References. References should be listed at the end of the article, also double-spaced. Unpublished papers should not be listed in references. nor should papers submitted for publication hut not yet accepted.

Number references consecutively in the order in which they are first mentioned in the text. Identify references in the text and in tables and figure legends by arabic numerals enclosed in square brackets. References cited only in

tables or figure legends should be numbered in accordance with the first mention of the relevant table or figure in the text. Be sure references are complete.

Reference citations should follow the format illustrated below.

Journal reference

-standard journal article (list all authors):
1. Alvarez ML, Mikasic D, Ottenberger A, Salazar ME. Caractericas de familias urbanas con lactante desnutrido: un ansis crco. Arch Latinoam Nutr 1979;29:220-3().

-corporate author:
2. Committee on Enzymes of the Scandinavian Society for Clinical Chemistry and Clinical Physiology. Recommended method for the determination of gammaglutamyltransferase in blood. Scand J Clin Lab Invest 1976;36:1 19-25.

Book or other monograph reference

-personal author(s):
3. Brozek J. Malnutrition and human behavior: experimental, clinical and community studies. New York: Van Nostrand Reinhold, 1985.

-corporate author:
4. American Medical Association, Department of Drugs. AMA drug evaluations. 3rd cd. Littleton. Mass, USA: Publishing Sciences Group, 1977.

-editor, compiler, chairman as author:
5. Medioni J. Boesinger E. eds. Mnismes ologiques de l'evolution. Paris: Masson. 1977.

-chapter in book:
6. Barnett HG. Compatibility and compartmentalization in cultural change. In: Desai AR. ed. Essays on modernization of underdeveloped societies. Bombay: Thacker, 1971.

Identification. Contributors should give their full name and highest degree. the name of departments and institutions to which the work should he attributed, the name and address of the author responsible for correspondence about the manuscript, and sources of support for the work. If the material in the article has been previously presented or is planned to be published elsewhere-in the same or modified form-a note should be included giving the details.

Manuscript copies. The contributor should keep a duplicate copy of the manuscript. Manuscripts will not be returned unless specifically requested. Proofs will be sent to the authors only in exceptional circumstances.

Contributions should be addressed to:
The Editor
Food and Nutrition Bulletin
9 Bow Street
Cambridge, MA 02138, USA

Note à l'intention des auteurs

La rction du Food and Nutrition Bulletin recherche des articles traitant de sujets correspondant a ses themes (voir au vo de la couverture la politique toriale de cette revue). La remise d'un manuscrit ne signifie pas sa publication, qui dnd de l'opinion de la rction sur son intt et sa qualitLes auteurs sont invita se pencher sur les rnts nums du Bulletin pour prendre connaissance de son contenu et de son style.

Langues. Les manuscrits peuvent etre rgen anglais, en frans ou en espagnol, et dan ces deux derniers cas, I'auteur ajoutera. si possible, un rmn anglais.

Format. Les manuscrits doivent etre dactylographi en double interligne. avec une marge suffisante. Ne doit etre prntu'un exemplaire original dactylographiu une photocopie de qualitquivalente.

Lorsqu'un manuscrit a prrur un appareil de traitement de texte, un disque ou de 3.50 ou de 5.25 pouces devrait dans toute la mesure possible y etre joint en prsant son format et le programme utilis

Longueur. Les manuscrits ne dovient pas. ordinairement, dsser 4,000 mots.

Rmem>. Un rme 15() mots maximum doit accompagner le manuscrit. Il devra donner les buts de l'de ou des recherches, les procres de base (sujets de l'de ou animaux expmentaux et modes d'observation et d'analyse), les principaux rltats (fournir des donn spfiques et indiquer dans la mesure du possible leur importance statistique) ainsi que les principales conclusions. Veuillez mettre en relief les aspects nouveaux et importants de l'de ou des observations. Dans le rmne citez aucun ouvrage de rrence et n'utilisez ni abrations ni sigles.

Tableaux et figures. Ils doivent etre reportsur des feuillets sr Les tableaux doivent etre dactylographien double interligne. Veuillez soumettre uniquement des figures originales, des dessins a l'encre de Chine ou des photographies tir sur papier glacLes labels qui apparaissent sur les figures doivent etre dactylographiou gravou imprimde maniere professionnelle et non pas its a la main.

Photographies. En principe, les mataux photographiques doivent etre remis sous forme de ntifs noir et blanc ou d'euves noir et blanc sur papier brillant. Sauf demande expresse les photographies ne seront pas renvoy.

Unitde mesure. On utilisera de prrence le systeme mique. Si d'autres systs sont utilis l'ivalant mique doit etre indiqu

Rrences. Les rrences doivent apparae a la fin de l'article, en double interligne lement. Les documents non publine doivent pas figurer dans les rrences pas davantage que les documents prnta des fins de publication mais qui n'ont pas encore accept

Veuillez numter les rrences dans l'ordre ou elles sont mentionn dans le texte. Identifiez au moyen d'un chiffre arabe placntre crochets les rrences dan le texte, les tableaux et les lndes des figures. Les rrences cituniquement dans les tableaux ou les lndes des figures doivent etre numt en fonction de la premiere fois ou il est fait mention du tableau ou de la figure approprians le texte. Assurez-vous que les rrences sont completes.

Les rrences cit doivent suivre le format dit ci-dessous.

Journal

-article de journal type (mr tous les auteurs):
1. Alvarez ML, Mikasic D. Ottenberger A. Salazar ME. Caractericas de familias urbanas con lactante desnutrido: un ansis crco. Arch Latinoam Nutr 1979;29:220-3().

-auteur d'une soci:
2. Committee on Enzymes of the Scandinavian Society for Clinical Chemistry and Clinical Physiology. Recommended method for the determination of gammaglutamyltransferase in blood. Scand J Clin Lab Invest 1976:36:119-25.

Livre ou autre monographie

-auteur(s) a titre personnel:
3. Brozek J. Malnutrition and human bebavior: expmental, clinical and community studies. New York: Van Nostrand Reinhold, 1985..

-auteur d'une soci:
4. American Medical Association, Department of Drugs. AMA drug evaluations. 3e Littleton, Mass. (E.U.): Publishing Sciences Group, 1977.

-teur, compilateur, prdent en tant qu'auteur:
5. Medioni J, Boesinger E, . Mnismes ologiques de l'lution. Paris: Masson, 1977.

-chapitre d'un ouvrage:
6. Barnett HG. Compatibility and compartmentalization in cultural change. Dans: Desai AR. Essays on modernization of underdeveloped societies. Bombay: Thacker, 1971.

Identification. Les auteurs doivent indiquer leur nom complet et leur principal dipl le nom des drtements et des institutions auxquels le travail doit etre attribule nom et l'adresse de l'auteur charge la correspondance sur le manuscrit ainsi que les sources de financement du travail. Si l'article a d remis auparavant ou est retenu pour une autre publication-sous la meme forme ou sous une forme modifion l'indiquera de fa dill

Copies du manuscrit. L'auteur doit conserver un double. Les manuscrits ne seront pas retourna moins que leurs auteurs n'en fassent expressnt la demande. Les euves seront envoy aux auteurs dans des circonstances exceptionnelles seulement.

Les auteurs s'adresseront a:
The Editor
Food and Nutrition Bulletin
9 Bow Street
Cambridge, MA 02138, USA

Nota para posibles autores

Los editores del Food and Nutrition Bulletin agradecen el envio de contribuciones pertinentes al tema de la revista (vea la polca editorial de esta revista en el interior de la tapa anterior). La presentacie un articulo no es garantde su publicacila cual dependerel criterio de los editores en lo que respecta a su pertinencia y calidad. Se ruega a los que deseen colaborar que consulten los ns recientes de Food and Nutrition Bulletin para cerciorarse de su contenido y estilo.

Idioma. Las contribuciones podrremitirse en espanol, franco ingl En caso de utilizar espanol o franc el autor deberncluir. de ser posible, un resumen en ingl

Formato. Los manuscritos deberpresentarse mecanografiadas, a doble espacio, con menes amplios. Solamente se presentaroriginales mecanografiados o una fotocopia de los mismos de calidad equivalente. No se admitirfotocopias en papel fino o satinado.

Si ha preparado cl manuscrito con mina de tratamiento de textos, agradeceremos nos envjunto al manuscrito una copia del disco floppy bien en 31/2 pulgadas, bien en 51/2 pulgadas, indicando el formato del disco y el programa de tratamiento de textos que ha utilizado.

Longitud. Las contribuciones ordinarias no deberexceder las 4.000 palabras.

Ress. Se adjuntarl manuscrito un resumen que no exceda de 150 palabras. El resumen indicarl objetivo del estudio o investigacimdos bcos (individuos, animales seleccionados en experimentos y mdos de observaci ansis). descubriniientos principales (si fuera posible aportando datos especcos y su significado estadico), y las conclusiones principales. Se enfatizarlos aspectos nuevos e importantes del estudio u observaciones. En el resumen no se citarreferencias ni se usarabreviaturas ni siglas.

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Unidades de medida. Se utilizarreferentemente el sistema mico decimal. De utilizarse otras unidades, deberindicarse sus equivalentes en el sistema mico decimal.

Referencias. Al final del articulo deberconsignarse las referencias, tambien doble espacio. En las referencias no se consignardocumentos que no se hayan publicado. ni aquellos que hayan solicitado su publicaciero que no se han aceptado todav

Las referencias se numerarconsecutivamente en el orden en que aparecen en el texto. Las referencias en el texto, en los cuadros y en los epafes de figuras se identificarcon ns argos encerrados entre paresis rectangulares. Las referencias que se citan solamente en cuadros o epafes de figuras se numerarde acuerdo con la primera menciue se haga en el texto del cuadro o figura pertinente. Debe asegurarse que se dan todas las referencias.

Las citas hechas a referencias deben adjustarse al formato indicado a continuaci

Referencia a publicacieria

- artlo modelo de publicacieria (consignar todos los autores):
1. Alvarez ML, Mikasic D. Ottenberger A. Salazar ME. Caractericas de familias urbanas con lactante desnutrido: un ansis critico. Arch Latinoam Nutr 1979;29:220-30.

-autores corporativos.
2. Committee on Enzymes of the Scandinavian Society for Clinical Chemistry and Clinical Physiology. Recommended method for the determination of gammaglutamyltransferase in blood. Stand J Clin Lab Invest 1976;36:119-25.

Referencia a labro u otra rnonograf

-autor(es) personal(es):
3. Brozek J. Malnutrition and human behavior: experimental. clinical and community studies. Nueva York: Van Nostrand Reinhold, 1985.

-autor corporativo:
4. Ameritan Medical Association, Department of Drugs. AMA drug evaluations. 3ra. ediciLittleton, Mass.. EE.UU.: Publishing Sciences Group, 1977.

-editor, recopilador, presidente de consejo como autor:
5. Medioni J. Boesinger E, editores. Mnismes ologiques de l'lution. Paris: Masson. 1977.

-caplo de libro:
6. Barnett HG. Compatibility and compartmentalization in cultural changa. En: Desai AR, editor. Essays on modernization of underdeveloped societies. Bombay: Thacker, 1971.

Identificaciem>. Los autores deberconsignar su nombre completo y titulacialta. nombre del departamento e instituciones a las que se atribuirl trabajo, el nombre y la direcciel autor responsable de la correspondencia del manuscrito, y fuentes de sustentaciel trabajo. Si el material del articulo ha sido presentado previamente o se prevublicacin otra parte, en forma igual o modificada. se debergregar una nota con detalles sobre dicha publicaci

Copias de la contribuciem>. El contribuyente deberonservar una copia del material que env No se devolverlos manuscritos a no ser que se pida su devoluciLas correcciones de prueba se enviara los autores solamente en casos excepcionales.

Las contribuciones deberdirigirse a:
The Editor
Food and Nutrition Bulletin
9 Bow Street
Cambridge, MA 02138, USA

Title of interest

Food Habits in Later Life: A Cross Cultural Study
By Mark L. Wahlqvist et al.

This study provides scholars, policy experts, and general readers with solid data and analysis regarding dietary practices of diverse populations of elderly communities in Australia, China, Greece, Japan, the Philippines, and Sweden. The work also brings together crosscultural studies of food and health among elderly in other communities of Asia, Europe, and Central America.

The study makes an important contribution to the great need for descriptive research on the health status, lifestyle, and eating habits of the elderly in developed and developing countries. The study also makes available a mass of data needed to determine to what extent eating habits and lifestyle predict health status in the elderly.

UNUP-912
ISBN 92808-0912-1
US$65, CD-ROM

United Nations
University Press
53-70, Jingumae 5-chome, Shibuya-ku, Tokyo 150, Japan
Tel (03) 3499-2811, Fax (03) 3406-7345,
E-mail: Sales@hq unu ecu, Http://www unu edu