Maternal Micronutrient Malnutrition: Effects on Breast Milk and Infant Nutrition, and Priorities for Intervention

By Lindsay H. Alien, PhD, RD, Department of Nutrition, University of California, Davis, CA 95616, USA.

From a global perspective, lactating women are more likely to suffer from micronutrient deficiencies than from a shortage of dietary energy or protein. Also, micronutrient deficiencies are more likely to affect breastmilk composition, and the development and nutritional status of the infant. Dietary interventions or supplementation can increase the secretion of many of these nutrients in breast milk, and improve infant nutritional status. This brief review attempts to summarize current knowledge concerning the importance of maternal micronutrient status during lactation, and to suggest priorities for assessment and intervention with specific nutrients.

Table 1 summarizes how maternal deficiency of specific micronutrients affects their concentration in breast milk, reported subsequent effects on the nursing infant, and the effects of maternal supplementation on the concentration of the nutrient in breast milk and on infant function. In general, milk composition is most affected by the mother’s intake of water soluble vitamins, is less influenced by her consumption of fat soluble vitamins, and is relatively unaffected by maternal mineral intake or status. Where breast milk concentration is influenced by maternal intake of a nutrient, this is usually only true up to a level above which the concentration in milk approaches a plateau (1).

Table 1. The Influence of Maternal Micronutrient Deficiencies and Supplements During Lactation on Breast Milk and the Infant.

Nutrient	Effect maternal deficiency on milk content	Effect maternal deficiency on infant	Effect maternal supplementation on milk content	Effect maternal supplementation on infant	Ref #
Vitamins
Thiamin	ß	Beri-beri	Ý	ß infant beri-beri	1, p.126
Riboflavin	ß	High EGRAC	Ý	ß maternal & infant EGRAC	2
Vitamin B-6	ß	Neurological problems	Ý	ß neurological problems	3
Folate	Û/ß	?	Û	none but improves maternal status	4, p. 151
Vitamin B-12	ß	Increased urine MMA1 Neurological problems Developmental delays	Ý	ß infant’s plasma MMA	4, p.14
Ascorbic Acid	ß	?	Ý (small)	?	5
Vitamin A	ß	Low serum retinol	Ý	Ý serum retinol for months after single oral dose Ý infant stores	6, p. 517S
Vitamin D	ß	Ý risk rickets, but depends more on sunshine exposure	Ý	Ý serum 25(OH)D if dose >2,000 IU/day	6, p. 484S
Minerals
Calcium	Û?	ß bone mineral, but relative in utero vs postpartum influence unclear	Û?		4, p,237, 6, p. 477S
Iron	Û		Û
Zinc	Û		Ý/Û
Copper	Û
Iodine	ß	infant’s RDA probably still met; impact of in utero deficiency more important	Ý
Selenium	ß	plasma and RBC Se	Ý

¹ Methylmalonic acid

For some micronutrients, such as folate, a relatively severe maternal deficiency, or a very low intake, may be needed before their secretion in breast milk is adversely affected. In this case the mother’s nutritional status may decline further during lactation while breast milk concentration of the nutrient is relatively protected.

Prioritising Maternal Supplementation

In Table 2, micronutrients of concern have been divided into two priority categories based on their importance to the maternal-infant dyad during lactation, and the efficacy of interventions.

Table 2. Suggested Priorities for Maternal Micronutrient Supplementation During Lactation

PRIORITY I	PRIORITY II
Thiamin Riboflavin Vitamin B-6 Vitamin B-12 Vitamin A Iodine1 Selenium1	Folic acid Vitamin D Calcium Iron Copper Zinc

¹ In regions of endemic deficiency

Priority I

Micronutrients in this category include thiamin, riboflavin, vitamins B-6 and B-12, vitamin A, and probably iodine and selenium in endemically deficient populations. Detection, prevention and intervention of deficiencies in this category should receive top priority because:

1. they result in a lower concentration of the nutrients in breast milk,

2. they have documented adverse effects on the infant,

3. the concentration of these nutrients in breast milk and infant status can be readily improved by increasing maternal intake, and

4. for most of them, fetal storage is relatively low and breast milk is the major source for the infant.

In thiamin deficiency - which is now relatively uncommon because of fortification programmes - mothers with beri-beri produce breast milk low in the vitamin which results in infantile beri-beri within 3-4 weeks of birth. Maternal supplementation with the vitamin increases milk concentration rapidly and reduces the risk of infantile beri-beri.

Likewise, riboflavin-deficient mothers produce breast milk with a low riboflavin concentration. In The Gambia, the nursing infants of such mothers developed biochemical evidence of riboflavin deficiency (high erythrocyte glutathione reductase activity coefficients, EGRAC) which was normalized after a few days of maternal supplementation with a biscuit that provided about 1 mg riboflavin per day (2). Maternal EGRAC values fell within 3 weeks but did not normalize with this amount of supplement. Maternal supplementation should probably be continued throughout lactation because breast milk riboflavin concentrations fell and infant EGRAC values rose when the supplement was discontinued. Riboflavin deficiency occurs where diets are low in animal products, and is reported more frequently now that the more sensitive EGRAC method is being used for assessment.

The content of vitamin B-6 in maternal milk is strongly correlated with maternal intake. A study of Egyptian lactating women found one third of them to have suboptimal B-6 status based on low breast milk concentrations of the vitamin (3). Lower breast milk B-6 was associated with lower infant birth weight, changes in infant behaviour from birth through 6 months of age, and less maternal responsiveness to her infant. Supplementation of the mother with 2.5-4 mg/day pyridoxine hydrochloride will restore breast milk concentrations of B-6.

Maternal plasma vitamin B-12 concentrations are also strongly correlated with breast milk concentrations of the vitamin. Maternal vitamin B-12 status is important during both pregnancy and lactation. A low maternal intake or poor absorption of the vitamin in pregnancy may reduce fetal stores as well as breast milk concentrations (4, pp 167-180). In an infant born to a woman who was vitamin B-12 deficient during pregnancy, clinical signs of deficiency appear around 4 months after birth. However, if the infant is born to a vitamin B-12 replete mother but malabsorbs the vitamin from birth, it will not develop deficiency signs for 12-36 months. While maternal vitamin B-12 deficiency has received most attention in strict vegetarians, there have been recent reports of low breast milk B-12 concentrations from Mexico and Kenya, associated with maternal deficiency of the vitamin (4, pp. 167-180), and a higher prevalence of low plasma B-12 is being detected with modern radioassays. In developing countries it is possible that vitamin B-12 deficiency is a relatively common result of malabsorption subsequent to parasitic or bacterial gastrointestinal infections, exacerbated by a low intake of animal products. Because this vitamin deficiency can have serious effects on infant mental and physical development, the prevalence of this vitamin deficiency in the perinatal period deserves further attention.

When the breast milk vitamin A concentration exceeds 50 ug/dL it is rare to see clinical evidence of deficiency in the infant even after weaning, but when the milk contains 30 ug/dL, and especially <20 ug/dL, signs of deficiency in the infant are much more prevalent. Milk from vitamin A deficient mothers may not provide enough of the vitamin to build up infant liver stores and protect it from deficiency beyond six months of age (6, pp. 517S-524S). Supplementation of Indonesian mothers within 3 weeks postpartum kept breast milk retinol concentrations significantly higher for up to 8 months, providing substantial amounts of the vitamin to the infant and building infant stores. Supplementation of the mother with vitamin A during this period has been called “a window of opportunity” for improving the vitamin A stores of the infant (4, p. 195).

Theoretically, iodine fits in the Priority I category. In areas of endemic iodine deficiency more attention has been paid to ensuring that pregnant women are iodine sufficient. If they are given one or more oral doses during early pregnancy this should protect the fetus and increase breastmilk iodine concentrations. WHO does not have a specific recommendation for treating lactating women with iodine. The mammary gland actively sequesters iodine so that the infant will probably receive a high dose when the mother is supplemented. A systematic study is needed to determine the effect of providing lactating women with high doses of iodine, and the amount and frequency of dose that is optimal for the mother-infant dyad. One report showed an effect of iodized salt on breast milk iodine, but less effect of consuming other foods high in the nutrient.

The concentration of selenium in breast milk is related to the selenium intake of the mother. It is lower in regions of endemic selenium deficiency and, in late lactation, for women of high parity. Little is known about the impact of maternal deficiency during lactation on infant intake and function. Theoretically the need for maternal supplementation with this nutrient will depend on selenium intake which is in turn influenced locally by the selenium content of the soil. Selenomethionine supplements providing about 3 umol selenium per day increase the concentration of selenium in both maternal plasma and breast milk.

Ascorbic acid concentrations in breast milk are influenced by maternal intake and therefore vary substantially by season in some regions. Even where breast milk concentrations are low these are likely to supply the infant’s requirement for vitamin C so this nutrient is not listed in the first priority category. In addition, supplying an additional 35 mg per day to Gambian lactating women increased breast milk ascorbic acid by a relatively small amount (5).

Priority II

This category includes folate, vitamin D, calcium, iron, copper, and zinc. It contains nutrients with the following characteristics:

1. their concentration in breast milk is relatively protected during maternal deficiency,
2. breast milk concentrations are relatively unaffected by maternal supplementation,
3. the mother is especially vulnerable to further depletion during lactation,
4. and postnatal maternal supplementation is more likely to benefit the mother than her infant.

Lactation puts fairly heavy demands on maternal folate reserves (4, 151-166), and breast milk folate concentrations are maintained at the expense of maternal stores unless the mother is severely deficient. Likewise, supplementation of the mother with folate will not usually increase secretion of this nutrient in breast milk unless her deficiency is severe, but it will improve her folate status. Little is known about the prevalence of folate deficiency in lactating women, but it is probably not common.

Vitamin D supplements are unnecessary if the infant has adequate exposure to ultraviolet light (6, 484S-491S). Breast milk provides relatively little vitamin D and does not come close to providing the infant’s recommended intake, so that the infant relies on in utero storage of the vitamin and on sunlight exposure. Although breast milk concentrations correlate with maternal serum 25-hydroxyvitamin D concentrations, the amounts in breast milk do not correlate with infant vitamin D status unless the mother is supplemented with high doses (2,000 IU/d) of vitamin D. Doses of 1,000 IU/d increase neither breast milk nor infant plasma concentrations. Fully clothed infants need about 2 hours of sunshine exposure per week in order to synthesise enough of this vitamin. In regions of endemic rickets or marginal vitamin D deficiency, or where infants are tightly swaddled, priority should be given to supplementing the infant directly or increasing their sunlight exposure. Also, maternal vitamin D status can be improved by encouraging adequate exposure to sunlight before birth, which will promote fetal storage of the vitamin. There is some evidence that women who consume low calcium diets and who are deficient in vitamin D might not be able to increase their efficiency of calcium absorption in the usual way, i.e. by increasing their production of vitamin D metabolites. This in turn may cause breast milk calcium secretion to be lower.

Breast milk calcium concentration is independent of current dietary intake. There are some reports that the breast milk concentration of this nutrient is lower in populations where calcium intakes are low, but little is known about the relationship between maternal calcium status and infant development (6, 477S-483S; 4, pp. 237-250). When dietary calcium is adequate women seem to adjust to the additional demands for calcium during lactation by mobilising bone in the first few months, and replacing it later. Providing calcium supplements to the lactating woman with a low dietary intake of the nutrient is likely to benefit her calcium status more than that of her infant, although this has not been adequately investigated.

Neither maternal iron nor copper deficiency affects the secretion of these trace elements in breast milk, nor does supplementation of the mother. Iron supplementation should be directed to the pregnant woman, to anemic lactating women in order to replenish iron stores, and to breastfed infants after 4-6 months of age. Infants with low birthweights are at special risk of iron deficiency. Copper deficiency is relatively uncommon in adult women, or in breastfed infants unless there is persistent diarrhoea.

The zinc content of breast milk in developing countries does not appear to be different from that of women in wealthier countries, and both higher and lower concentrations have been reported. In two studies, maternal consumption of zinc supplements slightly reduced the usual decline in breast milk zinc that occurs during lactation. Thus, supplementation of the lactating woman with zinc is unlikely to benefit her infant substantially.

Policy Implications

Much remains to be learned about the importance of maternal micronutrient status and intake for the nutritional status and development of infants in developing countries. From this review it is evident that breastfed infants of women in developing countries are at risk for several micronutrient deficiencies. In most cases they will not be severe enough to produce obvious clinical symptoms of deficiency, but could result in low infant stores and perhaps more subtle developmental delays and behaviour changes. One fundamental question that remains to be answered is whether mothers consuming poor quality diets that are low in animal products, in most vitamins, and usually in calcium, can produce breast milk that is adequate to support the normal growth, nutrient stores and development of infants. While the endemic infant growth-faltering in developing countries is generally attributed to early feeding with non-breast milk foods or to infections, the potential for maternal supplementation during lactation to improve infant growth and status has not been studied systematically.

More work is needed to determine the optimal quantity of nutrients needed to replenish maternal stores and restore breast milk concentrations. We need more information on whether dietary interventions are as effective as providing supplements. Obviously an improvement in maternal diet is the optimal, long-term solution to preventing micronutrient deficiencies during both pregnancy and lactation. However, while increasing intake to meet the recommended dietary requirement may be sufficient to restore milk concentrations of some water soluble vitamins, higher intakes than are possible through dietary means are probably needed in the case of vitamins A and D. In The Gambia providing 35 mg of vitamin C per day in a biscuit had little effect on the amount of the vitamin in breast milk, and supplying the majority of the maternal riboflavin requirement in a supplemental biscuit failed to lower maternal EGRAC values to normal.

There are several reasons why further attention should be paid to improving the micronutrient status of lactating women. One is that both the mother and her infant will benefit from supplementation. Another is that supplementation of the lactating woman rather than the infant is safer, and can supply the infant with the most bioavailable form of the nutrient even when maternal dosing is intermittent. In the case of vitamin A, where fetal storage of the vitamin is low and the risk of maternal toxicity is high, a few high dose supplements to the lactating woman will maintain vitamin concentrations in breast milk for several months. It may also be possible to use breast milk to monitor maternal nutritional status (e.g. in the case of vitamins A and D), or usual maternal intake (for water soluble vitamins except folate) of micronutrients. Potential complications include diurnal, day-to-day and seasonal fluctuations in nutrient concentrations as well as inter-individual differences in the normal amounts of micronutrients in milk; and changes with duration of lactation and during gradual weaning.

In this review we have suggested which micronutrients should receive priority for attention for the assessment, treatment and counselling of the lactating woman. The prevalence of these deficiencies needs to be further documented in specific regions and as a result of specific dietary patterns. Wherever the opportunity arises, the effect of dietary and supplement interventions on maternal and infant outcomes should be evaluated systematically in order to increase our knowledge in this area.

References

1. Institute of Medicine (1991) Nutrition During Lactation. National Academy Press, Washington, D.C.

2. Bates, C.J., Prentice, A.M., Paul, A.A., Sutcliffe, B.A., Watkinson, M. & Whitehead, R.G. (1981). Riboflavin Status in Gambian Pregnant and Lactating Women and its Implications for Recommended Dietary Allowances. American Journal of Clinical Nutrition, 34, 928-935.

3. McCullough, A.L., Kirksey, A., Wachs, T.D., McGabe, G.P., Bassily, N.S., Bishry, Z., Galal, O.M., Harrison, G.G., Jerome, N.W. (1990). Vitamin B-6 status of Egyptian Mothers: Relation to Infant Behavior and Maternal-Infant Interactions. American Journal of Clinical Nutrition, 51, 1067-1074.

4. Nutrient Regulation during Pregnancy, Lactation and Infant Growth. (1994) (Allen, L.H., King, J.C., Lonnerdal, B., eds). Plenum, NY.

5. Bates, C.J., Prentice, A.M., Prentice, A., Paul, A.A., Whitehead, R.G. (1982). Seasonal Variations in Ascorbic Acid Status and Breast Milk Ascorbic Acid Levels in Rural Gambian Women in Relation to Dietary Intake. Transactions of the Royal Society of Tropical Medicine and Hygiene, 76, 341-347.

6. Recent Developments in Maternal Nutrition and Their Implications for Practitioners. (1993). Allen, L.H. ed. American Journal of Clinical Nutrition, 59(2S), 437S-545S.