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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.