9
Meeting Maternal Nutrient Needs During Lactation

In this chapter, the subcommittee synthesizes information presented in earlier chapters, especially that concerning maternal nutritional status, milk volume and composition, infant nutrition, and health effects of lactation on the mother later in life. It then examines estimated nutrient needs in relation to realistic dietary patterns for lactating women.

WHAT ARE THE NUTRITIONAL DEMANDS OF LACTATION

Nutrient Secretion in Milk

Nutrient needs during lactation depend primarily on the volume and composition of milk produced and on the mother's initial nutrient needs and nutritional status. Among women exclusively breastfeeding their infants, the energy demands of lactation exceed prepregnancy demands by approximately 640 kcal/day during the first 6 months post partum compared with 300 kcal/day during the last two trimesters of pregnancy (NRC, 1989). In contrast, the demand for some nutrients, such as iron, is considerably less during lactation than during pregnancy.

Table 9-1 provides the estimated daily output of various nutrients in human milk compared with the increments in nutrient intakes for lactating women as specified in the Recommended Dietary Allowances (RDAs) (NRC, 1989). Each nutrient output is given as a range, reflecting milk volumes from 600 to 1,000 ml/day and the average concentration of each nutrient in human milk, as described in Chapter 6 (Table 6-1). Because there is variability in the milk



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Nutrition During Lactation 9 Meeting Maternal Nutrient Needs During Lactation In this chapter, the subcommittee synthesizes information presented in earlier chapters, especially that concerning maternal nutritional status, milk volume and composition, infant nutrition, and health effects of lactation on the mother later in life. It then examines estimated nutrient needs in relation to realistic dietary patterns for lactating women. WHAT ARE THE NUTRITIONAL DEMANDS OF LACTATION Nutrient Secretion in Milk Nutrient needs during lactation depend primarily on the volume and composition of milk produced and on the mother's initial nutrient needs and nutritional status. Among women exclusively breastfeeding their infants, the energy demands of lactation exceed prepregnancy demands by approximately 640 kcal/day during the first 6 months post partum compared with 300 kcal/day during the last two trimesters of pregnancy (NRC, 1989). In contrast, the demand for some nutrients, such as iron, is considerably less during lactation than during pregnancy. Table 9-1 provides the estimated daily output of various nutrients in human milk compared with the increments in nutrient intakes for lactating women as specified in the Recommended Dietary Allowances (RDAs) (NRC, 1989). Each nutrient output is given as a range, reflecting milk volumes from 600 to 1,000 ml/day and the average concentration of each nutrient in human milk, as described in Chapter 6 (Table 6-1). Because there is variability in the milk

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Nutrition During Lactation concentrations of some nutrients, both between women and in the same woman at different stages of lactation, the estimates in Table 9-1 are provided primarily as an illustration of the relative levels of secretion in milk. They reflect the nutrient output by women exclusively breastfeeding a single infant; therefore, they are underestimates for those women breastfeeding twins or triplets and overestimates for those whose infants are given substantial amounts of other milks or solid foods. Previous editions of Recommended Dietary Allowances (e.g., NRC, 1980) presented RDAs for lactating women as increments to be added to the RDAs for nonpregnant, nonlactating women. In contrast, the 1989 RDAs for lactating women are presented as absolute amounts. This provides convenient numbers that apply to all lactating women regardless of age and reflects the limited precision of the published data. The absolute values in the 1989 RDAs represent the RDAs for nonpregnant, nonlactating women aged 25 to 50 plus increments, which are shown in Table 9-1. For many nutrients, it is evident that the RDA increments were designed to exceed the estimated daily output during lactation. The RDAs for lactating women are the same for mothers of all ages, but some of the RDAs for nonpregnant, nonlactating women differ for women of different age groups. The difference is most notable for vitamin D and calcium. For those two nutrients, no increment for lactation is included for women younger than 25. Their prepregnancy RDAs are considerably higher than those of the older group (10 µg compared with 5 µg for vitamin D, and 1,200 mg with 800 mg for calcium), and they are identical to the older women's RDAs for these nutrients during lactation. Daily outputs of energy, vitamin A, vitamin B12, iron, and iodine in milk tend to exceed the recommended increments. The allowance for energy is based on the assumption that lactating women can draw on fat stores deposited during pregnancy to help support milk production. Thus, gradual weight loss is expected during lactation. For women who are underweight or whose weight gain during pregnancy was low, a 650-kcal/day increase in energy intake during the first 6 months of lactation is recommended. Total energy needs during lactation depend greatly on the level of physical activity, as described in Chapter 5. In estimating output for several nutrients, the subcommittee used values for milk concentrations that were higher than from those used in deriving the RDAs. These are identified in Table 9-1, along with other comments regarding the rationale for the RDA increments for lactation. Long-Term Nutrient Output During Lactation In addition to examining the daily output of nutrients in milk, it is useful to estimate the overall nutrient outputs resulting from various durations of lactation. Obviously, these estimates depend on the timing and degree to which

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Nutrition During Lactation TABLE 9-1 Estimated Secretion of Nutrients in Mature Human Milk Compared with Increments in Recommended Dietary Allowances (RDAs) for Lactating Women A. Energy, Protein, and Fat-Soluble Vitamins Measure Energy, kcal Protein, g Vitamin A, µg REa Vitamin D, µg Vitamin E, mg of α-TEb Vitamin K, µg Estimated secretion in milkc Increment in RDAsd,e for the following periods of lactation: 420–9700 6.3–10.5 400–670 0.3–0.6 1.4–2.3 1.3–2.1 0–6 mo 500 15 500 5 4 0 6–12 mo 500 12 400 5 3 0 Comments Estimated 80% efficiency in conversion to milk energy Estimated 70% efficiency in conversion to milk protein None Increment advised in part to maintain calcium balance Estimated 75% absorption No increment listed because intakes usually exceed RDA

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Nutrition During Lactation B. Water-Soluble Vitamins Measure Vitamin C, mg Thiamin, mg Riboflavin, mg Niacin, mg of NEf Vitamin B6, mg Folate, µg Vitamin B12, µg Estimated secretion in milkc Increment in RDAsd,e for the following periods of lactation: 24–40 0.13–0.21 0.21–0.35 0.9–1.5 0.06–0.09 50–83 0.6–1.0 0–6 mo 35 0.5 0.5 5 0.5 100 0.6 6–12 mo 30 0.5 0.4 5 0.5 80 0.6 Comments Estimated 85% absorption Increment higher than secretion due to increased energy needs Estimated 70% utilization for milk production Increment higher than secretion due to increased energy needs The milk concentration used by the subcommittee is for unsupplemented women Estimated 50% absorption; RDA based on 50 rather than 83 µg/liter RDA based on 0.6 rather than 1.0 µg/liter

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Nutrition During Lactation C. Minerals Measure Calcium, mg Phosphorus, mg Magnesium, mg Iron, mg Zinc, mg Iodine, µg Selenium, µg Estimated secretion in milkc 0.3–0.5h Increment in  RDAsd, e for the following periods of lactation: 168–280 84–140 21–35 0.18–0.30 0.9–1.5g 66–110 12–20 0–6 mo 400 400 75 0 7 50 20 6–12 mo 400 400 60 0 4 50 20 Comments None Based on a desired ratio of 1 to 1 for calcium to phosphorus intake Estimated 50% absorption Secretion during lactation is less than menstrual loss Estimated 20% absorption Based on need of infant, not maternal loss in milk Estimated 80% absorption a RE = Retinol equivalents. b α-TE = α-Tocopherol equivalents. c At volumes of 600–1,000 ml/day, based on milk composition shown in Table 6-1. d From NRC (1989). e Women aged 25 to 50. f NE = Niacin equivalents. g 0 to 6 months; see Chapter 6. h 6 to 12 months; see Chapter 6.

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Nutrition During Lactation human milk is replaced with other foods over the period of weaning. If the mother ingests lower amounts of a nutrient than she requires to meet her own needs and to cover nutrients secreted in the milk, she can draw upon body stores. To illustrate the possible impact of inadequate intake on the mother, Table 9-2 lists the estimated total body content of protein, calcium, and folate; the average amounts of iron and vitamin A stored by women; and the estimated outputs during partial or exclusive breastfeeding for various durations. Energy output in milk is not listed: changes in maternal body stores cannot be easily computed since energy-supplying nutrients could originate in either fat or lean tissue. As shown in Table 9-2, protein output in milk during 6 months of exclusive breastfeeding totals approximately 1,500 g (1.5 kg). For a 60-kg woman with 25% body fat, lean body mass is 45 kg, or about 11 kg of protein. Assuming that the efficiency of conversion of body protein to milk protein approximately equals the conversion of dietary protein to milk protein (˜70% [NRC, 1989]), a woman consuming only the RDA for protein for a nonpregnant, nonlactating woman would need to mobilize about 19% of her lean tissue to support 6 months of milk production. In the absence of adequate calcium intake, calcium output in milk represents 2 to 8% of total body calcium, as described in Chapter 8. Although iron losses in milk during 6 months of exclusive breastfeeding are equivalent to approximately 14% of the average woman's iron stores, this is only about half of what is ordinarily lost through menstruation (NRC, 1989). Thus, unless there was excessive blood loss at delivery, the total demand for iron during lactation is reduced while the woman is still amenorrheic compared with the demand when the woman is nonpregnant and nonlactating. When menstruation resumes, the combined demands of milk production and menstruation could draw heavily on iron reserves if dietary iron intake is low. Vitamin A reserves vary greatly among women and may be precariously low in women whose habitual intake of the vitamin is marginal. In the U.S. population, on average, women are expected to have vitamin A stores of approximately 200 mg (NRC, 1989)—more than the total output of many women over usual periods of lactation (see Table 9-2). However, for a woman with much smaller stores whose diet barely meets her own vitamin A requirement, the loss of the vitamin in milk could theoretically deplete vitamin A stores within a few months. Since folate tends to be excreted in the urine if intake exceeds demand, body stores of folate are not large. Thus, with limited dietary sources of folate, reserves would be depleted after only a few months of lactation. The estimates discussed above are meaningful only in the context of dietary information. For example, total protein output in milk during 6 months of exclusive breastfeeding is high compared with total body protein, but this is not of great concern in the United States, where protein intake is usually

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Nutrition During Lactation TABLE 9-2 Estimated Long-Term Demand of Lactation for Selected Nutrients   Nutrient Output Source of Demand Protein, g (% of total body contenta) Calcium, g (% of total body contenta) Iron, mg (% of storesa) Vitamin A, mg (% of storesa) Folate, mg (% of storesa) Estimated body contentb,c 11,250 1,035 300 209 6–7 Partial breastfeeding for 6 mo 756 (10) 20 (2) 22 (7) 48 (23) 6 (˜100) Exclusive breastfeeding for 6 mo 1,512 (19) 40 (4) 43 (14) 96 (46) 12 (˜100) Exclusive breastfeeding for 6 mo, plus partial breastfeeding for 6 mo 2,268 (29) 60 (6) 65 (22) 144 (69) 18 (>100) Exclusive breastfeeding for 6 mo, plus partial breastfeeding for 12 mo 3,024 (38) 80 (8) 87 (29) 192 (92) 24 (>100) a Based on average milk composition values from Table 6-1 and a volume of 800 ml/day for exclusive breastfeeding and 400 ml/day for partial breastfeeding, assuming that none of the demand is met by the maternal diet. b For a 60-kg (132-lb) woman, based on values provided by the NRC (1989). c Percentage of total body content or stores not applicable.

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Nutrition During Lactation generous. Calcium output during lactation may be of greater concern for reasons discussed in Chapter 8. CAN NUTRIENT NEEDS DURING LACTATION BE MET BY USUAL DIETARY INTAKE ALONE Predicted Average Intakes by U.S. Women During Lactation One approach recommended for estimating the likelihood of nutrient deficiencies is to compare the distribution of intakes of each nutrient with the hypothetical distribution of requirements in a given population (NRC, 1986). If this method could be used, it would avoid the use of arbitrary cutoff values to define deficient intakes. As noted in Chapter 4, however, data on the usual dietary intakes of lactating women are not sufficient for this method to be applied, and the data that are available were generally obtained from relatively affluent groups, who are unlikely to be representative of the population as a whole. For these reasons, and because energy needs are highly variable and energy intake is difficult to quantify, the subcommittee opted to evaluate the likelihood of nutrient shortfalls during lactation based on the nutrient density (nutrient intake per 1,000 kcal) of the average woman's diet in the United States. Total energy intakes by women are generally underestimated surveys; the nutrient density approach avoids this potential bias. However, the calculated nutrient densities could also be biased if underreporting is greater for certain foods than for others. No data are available to evaluate this possibility. Table 9-3 provides nutrient densities for protein, minerals, and vitamins as determined from nationally representative samples of U.S. women aged 19 to 50 and the total nutrient intakes that would be predicted from those densities at three different levels of energy intake (nutrient density × kcal of energy = total intake). The three levels of energy intake chosen for the calculations are 2,700 kcal (the estimated energy needs for lactation listed in Recommended Dietary Allowances [NRC, 1989]), 2,200 kcal (a value closer to the average reported intakes of lactating women, as described in Chapter 4), and 1,800 kcal (a level that might occur if a lactating woman were actively restricting food intake in order to lose weight). Intakes of specific nutrients at these three levels of energy intake can be compared with the RDAs for lactation, also listed in Table 9-3. Comparisons of Estimated and Recommended Intakes Several patterns become apparent when comparing estimated intakes with the RDAs shown in Table 9-3. At an intake of 2,700 kcal, average predicted intakes are below the RDAs for only two nutrients: calcium and zinc. At an intake of 2,200 kcal, however, predicted intakes of calcium, magnesium,

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Nutrition During Lactation TABLE 9-3 Estimated Mean Nutrient Intakes by U.S. Women at Three Energy Levels Compared with the Recommended Dietary Allowances (RDAs) for Lactation A. Protein and Fat-Soluble Vitamins Measure Protein, g Vitamin A, µg of REa Vitamin D, µg Vitamin E, mg of α-TEb Vitamin K, µg Average nutrient density of diets of U.S. women aged 19 to 50 yrd (nutrient content per 1,000 kcal) 40 805 NRc 5 NR Nutrient intake assuming average nutrient  density at: 2,700 kcal 108 2,174 NAe 14 NA 2,200 kcal 88 1,771 NA 11 NA 1,800 kcal 72 1,449 NA 9 NA RDA for lactationf 0–6 mo 65 1,300 10 12 65 6–12 mo 62 1,200 10 11 65

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Nutrition During Lactation B. Water-Soluble Vitamins Measure Vitamin C, mg Thiamin, mg Riboflavin, mg Niacin, mg of NE Vitamin B6, mg Folate, µg Vitamin B12, µg Average nutrient density of diets of U.S. women aged 19 to 50 yrd (nutrient content per 1,000 kcal) 56 0.7 0.9 11.2 0.8 13.7 2.9 Nutrient intake assuming average nutrient    density at: 2,700 kcal 151 1.9 2.4 30.2 2.2 370 7.8 2,200 kcal 123 1.5 2.0 24.6 1.8 301 6.4 1,800 kcal 101 1.3 1.6 20.2 1.4 247 5.2 RDA for lactationf 0–6 mo 95 1.6 1.8 20 2.1 280 2.6 6–12 mo 90 1.6 1.7 20 2.1 260 2.6

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Nutrition During Lactation C. Minerals Measure Calcium, mg Phosphorus, mg Magnesium, mg Iron, mg Zinc, mg Iodine, µg Selenium, µg Average nutrient density of diets of U.S. women aged 19 to 50 yrd (nutrient content per 1,000 kcal) 397 645 143 7.0 5.8 145g 3.5g Nutrient intake assuming average nutrient    density at: 2,700 kcal 1,072 1,742 386 18.9 15.7 392 95 2,200 kcal 873 1,419 315 15.4 12.8 319 77 1,800 kcal 715 1,161 257 12.6 10.4 261 63 RDA for lactationf 0–6 mo 1,200 1,200 355 15 19 200 75 6–12 mo 1,200 1,200 340 15 16 200 75 a RE = Retinol equivalents. b α-TE = α-Tocopherol equivalents. c NR = Not reported. d From Continuing Survey of Food Intake by Individuals, Wave I, USDA (1987). e NA = Not applicable. f Assumes 2,700 kcal of energy per day, from NRC (1989). g Estimated from the Total Diet Study, Pennington et al. (1989).

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Nutrition During Lactation expected to increase until age 25. As discussed in Chapter 6, a low calcium intake will not affect the concentration of calcium in human milk, but its effect on the mother's long-term bone density is uncertain, especially if the duration of breastfeeding is long. The evidence reviewed in Chapter 8 does not indicate a higher prevalence of osteoporosis in women who breastfed their children, but there is little information on the bone health of breastfeeding women with low calcium intakes. Lactating women in Nepal with low calcium intakes maintained milk calcium levels similar to those of U.S. women, but levels of urinary hydroxyproline were more than twice as high, indicating greater bone resorption (Moser et al., 1988). There is some evidence from animal studies that calcium absorption is enhanced during lactation (Halloran and DeLuca, 1980), but the degree to which this can compensate for low intakes is unclear. Although it is evident that calcium status is only one of many possible factors in the etiology of osteoporosis, dietary guidance for lactating women should include recommendations for good sources of calcium. Zinc There is no generally accepted indicator to use for evaluating the adequacy of zinc intakes. The RDA increment for zinc during lactation is 4 to 13 times higher than the estimated zinc secretion in milk to allow for poor absorption of dietary zinc (estimated at 20% for nonpregnant, nonlactating adults). However, stable isotope studies of seven lactating women in Brazil whose zinc intake averaged only 8.4 mg/day indicate that zinc absorption may be as high as 59 to 84% (Jackson et al., 1988). The difference between the RDA increment and estimated zinc secretion is especially large during the second 6 months of lactation, when zinc concentrations in milk decline substantially, regardless of the woman's zinc intake (Krebs et al., 1985). Low intakes are not generally reflected in low zinc concentrations in milk, and no major health risks have been associated with zinc intakes lower than the RDA. However, maternal zinc status might be jeopardized by low intake: zinc levels in plasma were found to be lower among lactating women than among nonlactating controls in Nigeria (Mbofund and Atinmo, 1985) but not in the United States (Moser and Reynolds, 1983), despite relatively low zinc intakes in both studies. Given the importance of adequate zinc status to immune function and other outcomes, further research on maternal zinc status during lactation is warranted. Magnesium Magnesium is the only other mineral for which intake by lactating women may often be marginal, when compared with the RDA. Again, however, the increment recommended during lactation is two to three times the estimated daily secretion in milk, to account for an estimated absorption of 50% (NRC,

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Nutrition During Lactation 1989). The effect of lactation on magnesium absorption is not known. Despite the relatively large difference between recommended and actual magnesium intakes, the only evidence of maternal magnesium deficiency during lactation appears in two anecdotal reports of extraordinary cases: in a wet nurse whose milk output was estimated to be 1,700 ml/day for 3 months (Greenwald et al., 1963) and in a woman who secreted three times the normal level of magnesium in her milk (Kamble and Ookalkar, 1989). Women in Ghana who breastfed for up to 12 months post partum had levels of serum magnesium lower than those of nonlactating controls (Fenuku and Earl-Quarcoo, 1978), but in lactating U.S. women whose mean magnesium intake was 248 mg/day, neither plasma magnesium nor erythrocyte magnesium differed from values for nonlactating women (Moser et al., 1983). Magnesium intake from diet or supplements has not been associated with maternal plasma or erythrocyte magnesium (Moser et al., 1983), nor is it likely to influence magnesium concentrations in milk (see Chapter 6). The long-term impact of low magnesium intake on the mother's well-being has not been studied. Vitamin B6 The vitamins most likely to occur in low levels (relative to the RDAs) in the diets of lactating women are B6, E, thiamin, and folate. Vitamin B6 levels in milk are strongly influenced by dietary intake: levels in the milk of women supplemented with 2.5 mg/day are twice as high as those of unsupplemented women (192 compared with 93 µg/liter) (Styslinger and Kirksey, 1985), but the RDA increment for lactation appears generous even if based on the vitamin B6 content of the milk of supplemented women. On the other hand, protein intakes by lactating women in the United States are high (average predicted intakes range from 111 to 166% of the RDA; Table 9-3); thus, the RDA increment allows for the increase in vitamin B6 requirement that accompanies increases in protein intake. Low vitamin B6 intakes during lactation may adversely affect both the infant and the mother, although evidence of overt deficiencies is rare in the United States. Kirksey and Roepke (1981) reported three cases of breastfed infants with central nervous system disorders, which they attributed to vitamin B6 deficiency. The mothers of all three infants had been long-term (4- to 12-year) users of oral contraceptives prior to pregnancy at a time when the estrogen content of such preparations was much higher than it is currently; these mothers were considered to have inadequate vitamin B6 status. Levels of plasma pyridoxal 5-phosphate (PLP) tend to be lower in breastfed infants than in formula-fed infants, and there is a correlation between vitamin B6 levels in human milk and infant plasma PLP (Andon et al., 1989; McCoy et al., 1985). However, none of the infants in two studies of unsupplemented lactating women in the United States (N = 6 in Styslinger and Kirksey [1985] and N =

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Nutrition During Lactation 30 in Andon et al. [1989]) had any clinical symptoms of vitamin B6 deficiency. Women in the study by Andon and colleagues generally had adequate vitamin B6 status; none had used oral contraceptives in the preceding 5 years. Chang and Kirksey (1990) measured maternal plasma PLP and milk vitamin B6 levels in 47 lactating women who received daily pyridoxine supplements containing 2.5, 4.0, 7.5, or 10 mg. Combined with the women's usual diets, the 4.0-mg supplements resulted in maternal PLP concentrations reportedly similar to those of nonlactating women (although no data for nonlactating women were provided) and in milk vitamin B6 concentrations that were nearly as high as those of the women receiving the higher-dose supplements. The influence of maternal supplementation on infant vitamin B6 status was not evaluated. In an earlier study (Borschel et al., 1986), two of five breastfed infants whose mothers were supplemented with 2.5 mg of vitamin B6 per day had plasma PLP levels of less than 25 nmol/liter (6.18 ng/ml), which the authors described as relatively low. However, Reynolds and colleagues (1990) have questioned whether plasma PLP is an adequate index of vitamin B6 status, especially in infants, and suggest that some individuals may have low PLP values without any clinical evidence of vitamin B6 deficiency. Taken all together, and without indices of vitamin B6 status other than plasma PLP, the above studies do not provide sufficient evidence to warrant routine vitamin B6 supplementation of lactating women. Vitamin E Although average predicted vitamin E intakes may fall somewhat below the RDA, this is generally not cause for concern for two reasons. First, the allowance for vitamin E is based primarily on estimates of customary intakes from food sources in the United States, rather than on minimum requirements. Second, the calculated nutrient density of vitamin E shown in Table 9-3 may be an underestimate, since there may be selective underreporting of fat intake (and thus vitamin E) in the surveys on which the calculation is based. Although maternal vitamin E intake can influence the levels of this vitamin in milk, there is no evidence of vitamin E deficiency in individuals with normal fat absorption (NRC, 1989). Thiamin The RDA increment for thiamin during lactation is considerably higher than thiamin losses in milk—in part because the need for thiamin depends on energy intake, which is expected to be higher during lactation. The predicted average thiamin intakes shown in Table 9-3 are less than the RDA only at lower than recommended energy intakes, suggesting that low thiamin intake is seldom a problem. Low maternal thiamin intake can result in low thiamin levels in milk, however. Therefore, in the judgment of the subcommittee, intakes of at

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Nutrition During Lactation least 1.3 mg/day (the RDA for nonpregnant, nonlactating women of 1.1 mg/day plus an increment for milk secretion of 0.2 mg/day [Table 9-1]) are desirable among women consuming 2,200 kcal/day or less. Folate Predicted average folate intakes fall below the RDA only when energy intake is less than 2,000 kcal/day. However, the margin of safety between the folate output in milk and the RDA is quite narrow (Table 9-1). The RDA is based on an average folate concentration of 50 µg/liter in human milk, but a well-conducted study using an accurate method (Brown et al., 1986) suggests that average concentrations are approximately 85 µg/liter. This higher value was used as the basis for estimating the daily secretion of folate in Table 9-1. If absorption of folate from a mixed diet is estimated to be 50%, the desired increment would be about 140 µg of folate per day. AT this level, folate needs during lactation would be approximately 320 µg/day (the sum of 180 µg/day for nonpregnant, nonlactating women plus 140 µg/day for lactation). At an energy intake of 2,200 kcal/day, the average predicted maternal folate intake is lower than this amount—301 µg/day (Table 9-3). Approximately 10% of the U.S. population is believed to have low folate stores (LSRO, 1984), and poor folate status of women post partum is not uncommon (Butte et al., 1981; Martinez, 1980; Qvist et al., 1986). In a study of 91 middle-class lactating women in Norway who did not receive supplemental folate, Ek (1983) observed that folate levels in the red blood cells of women breastfeeding for more than 6 months declined 30% during the first 2 months, and increased thereafter, slightly exceeding levels observed at parturition. The folate levels in their milk did not reflect these changes, and there were no signs of folate deficiency in the mothers. The folate levels in red blood cells of women who breastfed for less than 1 month changed very little during the first 12 months post partum. This and other studies (Metz, 1970; Tamura et al., 1980) indicate that maternal reserves of folate may be depleted to maintain folate levels in milk. If dietary intake and maternal reserves of folate have been chronically low, milk folate levels will increase in response to increased folate intake (see Chapter 6). Thus, adequate folate intake is important to protect the health of both the mother and the infant. Nutrient Concerns for Selected Groups of Lactating Women The discussion above focuses on nutrients likely to be consumed by lactating women in the United States in amounts lower than the RDAs. Within certain age, income, and ethnic groups, however, the diet may be characterized by nutrient densities higher or lower than the averages shown in Table 9-3. Intake data from national surveys are available by age, race (white, black, and other) (e.g., USDA, 1987), and income (above and below the poverty level)

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Nutrition During Lactation (e.g., NCHS, 1983; USDA, 1988). Such data may be useful in identifying potential nutrient inadequacies in selected groups. Following are four examples of groups whose diets, on average, have nutrient densities lower than the values shown in Table 9-3. An energy intake of 2,200 kcal was assumed when calculating recommended nutrient densities. Diets of adolescents (aged 15 to 17) typically contain less iron (an average of 5.7 mg/1,000 kcal) (NCHS, 1983) than recommended during lactation (6.8 mg/1,000 kcal). Diets of adolescents with family incomes below the poverty level have a low vitamin A content (1,500 IU/1,000 kcal) (NCHS, 1983) compared with a desired density of 1,950 IU/1,000 kcal. On average, the diets of black women contain about 30% less calcium, 20% less magnesium, and 20% less vitamin A than average diets consumed by white women (USDA, 1987). Diets of low-income adult women are characterized by lower densities of calcium and vitamin A than are typical of diets of women above the poverty level (NCHS, 1983). Thus, special care should be taken to ensure that breastfeeding women in such groups have access to a nutrient-dense diet. Women with restricted eating patterns will have undesirably low intakes of certain nutrients. This applies to those whose total food and energy intake is low (unless nutrient density is unusually high) and to those who avoid foods that are major sources of nutrients, such as calcium-rich dairy products, vitamin D-fortified milk, animal foods (for vitamin B12), or fruits and vegetables (for folate and vitamin C). In some cultural groups, beliefs regarding foods that should not be consumed by lactating women may affect dietary patterns (Baumslag, 1986), but the influence of restrictive food beliefs on nutrient intake is not well documented. FOOD GUIDANCE FOR LACTATING WOMEN Numerous food guides for lactating women have been developed by various state and national agencies concerned with maternal nutrition. There is considerable variability in the dietary recommendations provided in these guides, as illustrated by the number of daily servings they recommend from each of the food groups (Table 9-4). For example, the recommended amount of protein-rich foods ranges from 4 to 12 oz/day, suggested servings of milk vary from three to six per day, and servings from the bread and cereals group range from four to eight per day. Some of the guides specify subcategories of fruits and vegetables, such as ''vitamin C-rich," "dark green leafy," and "other," whereas other guides lump all fruits and vegetables together and specify three to six servings. The foods selected from within each food group can strongly influence the

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Nutrition During Lactation TABLE 9-4 Recommended Numbers of Servingsa During Lactation, by Publication     Milk, Dairy Fruits and Vegetables Reference Protein Intake by Adults of All Ages Intake by Teens Breads, Cereals All Fruits and Vegetables All Fruits All Vegetables Vitamin C Rich Dark Green, Leafy or Vitamin A Rich Starchy Vegetables Other Vegetables Unsaturated Fat DHHS, 1980 8–12 5 NRb 4 NRc NRc NRc 1 1 NR 1 NR USDA, 1988a 4–6 4 NR 4 4 NRc NRc NRc NRc NR NRc NR Virginia Department of Health, 1981 6–9 3–4d NR 4 NRc NRc NRc 1 1 NR 2 NR American Red Cross, 1984 6–7 3 4 >8 NRc 3–4 3–5c NRc NRc NR NRc NR Michigan Department of Public Health, 1984 6 4 6 6 6f NRc NRc 2 1 NR NRc NR USDA, 1984 6–7 3 4 >8 NRc 2–4 3–5 NRc 1 1 1 NR Bouden, 1985 8–12 5 NR 4 3 NRc NRc NRc NRc NR NRc NR Alabama Department of Public Health, 1987 4–6 4–6 6 >6 >5 NRc NRc NRc NRc NR NRc NR California Department of Health Services, 1990 7 3 NR 7 3g NRc NRc 1 1 NR NRc 3 a Protein servings refers to ounces of meat, poultry, or fish or the equivalent amount of protein from other sources. Serving sizes for other food groupings differed somewhat among the publications but were generally as follows: milk, 1 cup or the equivalent in calcium content; breads and cereals, 1 piece or 30 g (1 oz) dry; fruits and vegetables, 1 piece or 1/2 cup; unsaturated fat, 1 teaspoon or the equivalent amount of fat from selected sources. b NR = No recommendation. c See related columns in the row. d Take five to six servings frequently. e Include all types regularly. f Include at least one raw fruit or vegetable. g Exclusive of other fruits and vegetables specified in this row.

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Nutrition During Lactation nutrient density of the total diet. Guides that specify many servings from some food groups may be difficult to follow if they depart greatly from typical eating patterns of the U.S. population. Although most food guides were developed to help individuals make food selections that would approach the RDAs, following them does not guarantee that the RDAs will be met. Only one of the food guides—the Daily Food Guide for Women (California Department of Health Services, 1990)—has been accompanied by an analysis demonstrating that following the guide will lead to nutrient intakes close to the RDAs (Newman and Lee, in press). In providing food guidance, foods that are important sources of the nutrients most likely to be in short supply should be identified. A selection of important food sources of the key nutrients identified in this chapter is listed below. Many more foods contain smaller but still important amounts of these nutrients. Calcium: milk; cheese; yogurt; fish with edible bones; tofu processed with calcium sulfate; bok choy; broccoli; kale; collard, mustard, and turnip greens; breads made with milk. Zinc: meat, poultry, seafood, eggs, seeds, legumes, yogurt, whole grains (bioavailability from this source is variable). Magnesium: nuts, seeds, legumes, whole grains, green vegetables, scallops, and oysters (in general, this mineral is widely distributed in food rather than concentrated in a small number of foods). Vitamin B6: bananas, poultry, meat, fish, potatoes, sweet potatoes, spinach, prunes, watermelon, some legumes, fortified cereals, and nuts. Thiamin: pork, fish, whole grains, organ meats, legumes, corn, peas, seeds, nuts, fortified cereal grain (widely distributed in foods). Folate: leafy vegetables, fruit, liver, green beans, fortified cereals, legumes, and whole-grain cereals. CONCLUSIONS The total amounts of nutrients that the lactating mother secretes in her milk are directly related to the extent and duration of lactation. Lactating women who meet the RDA for energy are likely to meet the RDA for all nutrients except calcium and zinc if the nutrient density of their diets is close to the average for young U.S. women. If nutrient intake is lower than the total demand for both maternal maintenance needs and milk production (because of low energy intake, low nutrient density of the diet, or both), the mother's body will mobilize available nutrients from body tissues during lactation. The level of nutrient intake needed to prevent net mobilization is not known for individual women, but because the RDAs include a generous safety margin, it is likely to be below the RDA. At energy intakes less than 2,700 kcal/day, the nutrients for which intake is most likely to be low, relative to need, include calcium, magnesium, zinc, vitamin B6, and folate.

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Nutrition During Lactation TABLE 9-5 Suggested Measures for Improving Nutrient Intake of Women with Restrictive Eating Patterns Type of Restrictive Eating Pattern Corrective Measures Excessive restriction of food intake, i.e., ingestion of <1,800 kcal of energy per day, which ordinarily leads to unsatisfactory intake of nutrients compared with the amounts needed by lactating women Encourage increased intake of nutrient-rich foods to achieve an energy intake of at least 1,800 kcal/day; if the mother insists on curbing food intake sharply, promote substitution of foods rich in vitamins, minerals, and protein for those lower in nutritive value; in individual cases, it may be advisable to recommend a balanced multivitamin-mineral supplement; discourage use of liquid weight loss diets and appetite suppressants Complete vegetarianism, i.e., avoidance of all animal foods, including meat, fish, dairy products, and eggs Advise intake of a regular source of vitamin B12, such as special vitamin B12-containing plant food products or a 2.6-µg vitamin B12 supplement daily Avoidance of milk, cheese, or other calcium-rich dairy products Encourage increased intake of other culturally appropriate dietary calcium sources, such as collard greens for blacks from the southeastern United States; provide information on the appropriate use of low-lactose dairy products if milk is being avoided because of lactose intolerance; if correction by diet cannot be achieved, it may be advisable to recommend 600 mg of elemental calcium per day taken with meals Avoidance of vitamin D-fortified foods, such as fortified milk or cereal, combined with limited exposure to ultraviolet light Recommend 10 µg of supplemental vitamin D per day To help them maintain satisfactory nutritional status, lactating women should be given sound nutrition information and encouraged to follow eating patterns that include frequent consumption of nutrient-rich foods, especially those that supply the minerals and vitamins listed above. Women who continue to breastfeed after return of their menses may benefit by increased consumption of iron-rich foods. Continued consumption of nutrient-rich diets after lactation may help to replenish body reserves of nutrients utilized during pregnancy and lactation. Selected groups of lactating women may need special attention to avoid nutritional problems in either themselves or their infants. These include groups with restricted eating patterns (such as complete vegetarians, women who diet to lose weight, and those who avoid dairy products), adolescents, and low-income women.

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Nutrition During Lactation RECOMMENDATIONS FOR CLINICAL PRACTICE Encourage lactating women to follow dietary guidelines that promote a generous intake of nutrients from fruits and vegetables, whole-grain breads and cereals; calcium-rich dairy products; and protein-rich foods such as meats, fish, and legumes (see also Table 9-5). The evidence does not warrant recommending routine vitamin-mineral supplementation of lactating women. If dietary evaluation suggests that one or more nutrients may be provided in lower than recommended amounts by the diet of an individual woman, promote selection and consumption of more food choices that are rich in these nutrients. For women whose eating patterns lead to a very low intake of one or more nutrients, provide individualized diet counseling (preferred) or recommend nutrient supplementation as described in Table 9-5. REFERENCES Alabama Department of Public Health. 1987. Foods for the Nursing Mother: Food Plan for the Nursing Mother. WIC Program, Alabama Department of Public Health, Montgomery, Ala. American Red Cross. 1984. Better Eating for Better Health: Participant's Guide. What Should I Feed My Baby? American Red Cross, Washington, D.C. 15 pp. Andon, M.B., R.D. Reynolds, P.B. Moser-Veillon, and M.P. Howard. 1989. Dietary intake of total and glycosylated vitamin B-6 and the vitamin B-6 nutritional status of unsupplemented lactating women and their infants. Am. J. Clin. Nutr. 50:1050-1058. Baumslag, N. 1986. Breastfeeding: Cultural practices and variations. Pp. 621-642 in Human Lactation 2. Hamosh, M. and A.S. Goldman, eds. Plenum Press, New York. Borschel, M.W., A. Kirksey, and R.E. Hannemann. 1986. Effects of vitamin B-6 intake on nutriture and growth of young infants. Am. J. Clin. Nutr. 43:7-25. Bouden, E.S. 1985. Health Practices to Improve Pregnancy Outcomes: A Guide for the Primary Care Practitioner. Pennsylvania Department of Health, Harrisburg, Pa. 237 pp. Brown, C.M., A.M. Smith, and M.F. Picciano. 1986. Forms of human milk folacin and variation patterns. J. Pediatr. Gastroenterol. Nutr. 5:278-282. Butte, N.F., D.H. Calloway, and J.L. Van Duzen. 1981. Nutritional assessment of pregnant and lactating Navajo women. Am. J. Clin. Nutr. 34:2216-2228. California Department of Health Services, Maternal and Child Health Branch and WIC Supplemental Foods Branch. 1990. Dietary guidelines and daily food guide. Pp. 59-92 in Nutrition During Pregnancy and Postpartum Period: A Manual for Health Care Professionals. Department of Health Services, Sacramento, Calif. Chang, S., and A. Kirksey. 1990. Pyridoxine supplementation of lactating mothers: relation to maternal nutrition status and vitamin B-6 concentrations in milk. Am. J. Clin. Nutr. 51:826-831. DHHS (Department of Health and Human Services). 1980. Breast-Feeding, DHHS Publ. No. (HSA) 80-5109. Health Services Administration, Public Health Service, U.S. Department of Health and Human Services, Rockville, Md. 22 pp.

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Nutrition During Lactation Ek, J. 1983. Plasma, red cell, and breast milk folacin concentrations in lactating women. Am. J. Clin. Nutr. 38:929-935. Fenuku, R.I., and S.N. Earl-Quarcoo. 1978. Serum calcium, magnesium and inorganic phosphate during lactation. Trop. Geogr. Med. 30:495-498. Greenwald, J.H., A. Dubin, and L. Cardon. 1963. Hypo-magnesium tetany due to excessive lactation. Am. J. Med. 35:854-860. Halloran, B.P., and H.F. DeLuca. 1980. Calcium transport in small intestine during pregnancy and lactation. Am. J. Physiol. 239:E64-E68. Jackson, M.J., R. Giugliano, L.G. Giugliano, E.F. Oliveira, R. Shrimpton, and I.G. Swainbank. 1988. Stable isotope metabolic studies of zinc nutrition in slumdwelling lactating women in the Amazon valley. Br. J. Nutr. 59:193-203. Kamble, T.K., and D.S. Ookalkar. 1989. Lactational hypomagnesaemia. Lancet 2:155-156. Kirksey, A., and J.L.B. Roepke. 1981. Vitamin B6 nutriture of mothers of three breastfed neonates with central nervous system disorders. Fed. Proc., Fed. Am. Soc. Exp. Biol. 40:864. Krebs, N.F., K.M. Hambidge, M.A. Jacobs, and J.O. Rasbach. 1985. The effects of dietary zinc supplement during lactation on longitudinal changes in maternal zinc status and milk zinc concentrations. Am. J. Clin. Nutr. 41:560-570. LSRO (Life Sciences Research Office). 1984. Assessment of the Folate Nutritional Status of the U.S. Population Based on Data Collected in the Second National Health and Nutrition Examination Survey, 1976-1980. Federation of American Societies for Experimental Biology, Bethesda, Md. 96 pp. Martinez, O.B. 1980. Red cell folate values of a group of non pregnant mothers. Can. J. Public Health 71:163-169. Mbofung, C.M.F., and T. Atinmo. 1985. Zinc, copper and iron concentrations in the plasma and diets of lactating Nigerian women. Br. J. Nutr. 53:427-439. McCoy, E., K. Strynadka, and K. Brunet. 1985. Vitamin B6 intake and whole blood levels of breast and formula fed infants: serial whole blood vitamin B6 levels in premature infants. Curr. Top. Nutr. Dis. 13:79-96. Metz, J. 1970. Folate deficiency conditioned by lactation. Am. J. Clin. Nutr. 23:843-847. Michigan Department of Public Health. 1984. Breastfeeding: A Special Gift. H-828. Bureau of Health Promotion and Disease Prevention, Michigan Department of Public Health, Lansing, Mich. 36 pp. Moser, P.B., and R.D. Reynolds. 1983. Dietary zinc intake and zinc concentrations of plasma, erythrocytes, and breast milk in antepartum and postpartum lactating and nonlactating women: a longitudinal study. Am. J. Clin. Nutr. 38:101-108. Moser, P.B., C.F. Issa, and R.D. Reynolds. 1983. Dietary magnesium intake and the concentration of magnesium in plasma and erythrocytes of postpartum women. J. Am. Coll. Nutr. 4:387-396. Moser, P.B., R.D. Reynolds, S. Acharya, M.P. Howard, M.B. Andon, and L.A. Lewis. 1988. Copper, iron, zinc, and selenium dietary intake and status of Nepalese lactating women and their breastfed infants. Am. J. Clin. Nutr. 47:729-734. NCHS (National Center for Health Statistics). 1983. Dietary Intake Source Data: United States, 1976-80. Vital and Health Statistics, Series 11, No. 231. DHHS Publ. No. (PHS) 83-1681. National Center for Health Statistics, Public Health Service, U.S. Department of Health and Human Services, Hyattsville, Md. 483 pp. Newman, V., and D. Lee. In press, 1991. Developing a Daily Food Guide for Women. J. Nutr. Educ. 23(2).

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Nutrition During Lactation NRC (National Research Council). 1980. Recommended Dietary Allowances, 9th ed. Report of the Committee on Dietary Allowances, Food and Nutrition Board, Division of Biological Sciences, Assembly of Life Sciences. National Academy Press, Washington, D.C. 185 pp. NRC (National Research Council). 1986. Nutrient Adequacy: Assessment Using Food Consumption Surveys. Report of the Subcommittee on Criteria for Dietary Evaluation, Coordinating Committee on Evaluation of Food Consumption Surveys, Food and Nutrition Board, Commission on Life Sciences . National Academy Press, Washington, D.C. 146 pp. NRC (National Research Council). 1989. Recommended Dietary Allowances, 10th ed. Report of the Subcommittee on the Tenth Edition of the RDAs, Food and Nutrition Board, Commission on Life Sciences. National Academy Press, Washington, D.C. 284 pp. Pennington, J.A.T., B.E. Young, and D.B. Wilson. 1989. Nutritional elements in U.S. diets: results from the Total Diet Study, 1982 to 1986. J. Am. Diet. Assoc. 89:659-664. Qvist, I., M. Abdulla, M. Jägerstad, and S. Svensson. 1986. Iron, zinc and folate status during pregnancy and two months after delivery. Acta Obstet. Gynecol. Scand. 65:15-22. Reynolds, R.D., M.B. Andon, and P.B. Moser-Veillon. 1990. Reply to M.W. Borschel and A. Kirksey (letter). Am. J. Clin. Nutr. 51:1116-1117. Styslinger, L., and A. Kirksey. 1985. Effects of different levels of vitamin B6 supplementation on vitamin B6 concentrations in human milk and vitamin B6 intakes of breastfed infants. Am. J. Clin. Nutr. 41:21-31. Tamura, T., Y. Yoshimura, and T. Arakawa. 1980. Human milk folate and folate status in lactating mothers and their infants. Am. J. Clin. Nutr. 33:193-197. USDA (U.S. Department of Agriculture). 1984. Promoting Breastfeeding: A Guide for Health Professionals Working in the WIC and CSF Programs. FNS-247. Food and Nutrition Service, U.S. Department of Agriculture, Alexandria, Va. 51 pp. USDA (U. S. Department of Agriculture). 1987. Nationwide Food Consumption Survey. Continuing Survey of Food Intakes by Individuals. Women 19-50 Years and Their Children 1-5 Years, 1 Day, 1986. Report No. 86-1. Nutrition Monitoring Division, Human Nutrition Information Service, U.S. Department of Agriculture, Hyattsville, Md. 98 pp. USDA (U.S. Department of Agriculture). 1988a. How WIC Helps: Eating for You and Your Baby. Program Aid No. 1198. Food and Nutrition Service, U.S. Department of Agriculture, Alexandria, Va. 6 pp. USDA (U.S. Department of Agriculture). 1988b. Nationwide Food Consumption Survey. Continuing Survey of Food Intakes by Individuals. Low-Income Women 19-50 Years and Their Children 1-5 Years, 4 Days, 1985. Report No. 85-5. Nutrition Monitoring Division, Human Nutrition Information Service, U.S. Department of Agriculture, Hyattsville, Md. 220 pp. Virginia Department of Health. 1981. Breastfeeding: The Best Feeding for Your Baby. WIC Program, Bureau of Nutrition, Virginia Department of Health, Richmond, Va. 7 pp.