6
Milk Composition

In examining the evidence concerning the influence of maternal nutrition on human milk composition, the subcommittee considered the broad spectrum of constituents of milk, the normal variation in their concentrations, and factors in addition to maternal nutrition that influence those variations. This discussion of the subcommittee's findings is not meant to be exhaustive. Rather, this chapter provides a framework for understanding how maternal nutrition can have an impact on the composition of human milk, as well as when and in what context nutritional factors are likely to be operational. Furthermore, it provides the information needed to estimate maternal nutrient requirements—the subject of Chapter 9—and provides a basis for considering some of the effects of maternal nutrition on the nursing infant's health (Chapter 7) and the effects of lactation on the mother's longer-term health and nutrient stores (Chapters 8 and 9).

CHARACTERISTICS OF HUMAN MILK

Human milk is a complex fluid that contains more than 200 recognized constituents (see Blanc, 1981). The number of recognized constituents has increased as analytic techniques have been improved. Milk consists of several compartments, including true solutions, colloids (casein micelles), membranes, membrane-bound globules, and live cells (Ruegg and Blanc, 1982). Its constituents can be broadly divided into categories; for example, aqueous and lipid fractions (see box) or nutritive and nonnutritive constituents. Many milk constituents serve dual roles (see later section ''Constituents of Human Milk with Other Biologic Functions"). Detailed discussions of human milk constituents



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Nutrition During Lactation 6 Milk Composition In examining the evidence concerning the influence of maternal nutrition on human milk composition, the subcommittee considered the broad spectrum of constituents of milk, the normal variation in their concentrations, and factors in addition to maternal nutrition that influence those variations. This discussion of the subcommittee's findings is not meant to be exhaustive. Rather, this chapter provides a framework for understanding how maternal nutrition can have an impact on the composition of human milk, as well as when and in what context nutritional factors are likely to be operational. Furthermore, it provides the information needed to estimate maternal nutrient requirements—the subject of Chapter 9—and provides a basis for considering some of the effects of maternal nutrition on the nursing infant's health (Chapter 7) and the effects of lactation on the mother's longer-term health and nutrient stores (Chapters 8 and 9). CHARACTERISTICS OF HUMAN MILK Human milk is a complex fluid that contains more than 200 recognized constituents (see Blanc, 1981). The number of recognized constituents has increased as analytic techniques have been improved. Milk consists of several compartments, including true solutions, colloids (casein micelles), membranes, membrane-bound globules, and live cells (Ruegg and Blanc, 1982). Its constituents can be broadly divided into categories; for example, aqueous and lipid fractions (see box) or nutritive and nonnutritive constituents. Many milk constituents serve dual roles (see later section ''Constituents of Human Milk with Other Biologic Functions"). Detailed discussions of human milk constituents

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Nutrition During Lactation Classes of Constituents in Human Milk Protein and Nonprotein Nitrogen Compounds Carbohydrates Proteins Lactose Caseins Oligosaccharides α-Lactalbumin Bifidus factors Lactoferrin Glycopeptides Secretory IgA and other immunoglobulins Lipids β-Lactoglobulin Triglycerides Lysozyme Fatty acids Enzymes Phospholipids Hormones Sterols and hydrocarbons Growth factors Fat-soluble vitamins Nonprotein Nitrogen Compounds A and carotene Urea D Creatine E Creatinine K Uric acid Minerals Glucosamine Macronutrient Elements α-Amino nitrogen Calcium Nucleic acids Phosphorus Nucleotides Magnesium Polyamines Potassium Water-Soluble Vitamins Sodium Thiamin Chlorine Riboflavin Sulfur Niacin Trace Elements Pantothenic acid Iodine Biotin Iron Folate Copper Vitamin B6 Zinc Vitamin B12 Manganese Vitamin C Selenium Inositol Chromium Choline Cobalt Cells   Leukocytes   Epithelial cells   and properties can be found in several recent review articles and books (e.g., Blanc, 1981; Carlson, 1985; Gaull et al., 1982; Goldman et al., 1987; Goldman and Goldblum, 1990; Hamosh and Goldman, 1986; Jensen, 1989; Jensen and Neville, 1985; Koldovskỳ, 1989; Lönnerdal, 1985a, 1986a; Picciano, 1984a, 1985; Ruegg and Blanc, 1982).

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Nutrition During Lactation METHODOLOGIC ISSUES Types of Variation The concentration of the individual constituents of mature human milk have been shown to vary considerably (see Table 6-1), even when they are collected and analyzed under controlled, defined conditions. The greatest variations have been observed from woman to woman, although variations are also found in different samples obtained from the same woman (Picciano, 1984b). Milk composition changes from the beginning of a feeding to the end, diurnally, from day to day, and with the onset and progression of lactation. Examples are given later in this section. Early investigators recognized the importance of sampling techniques in obtaining valid data on the composition of human milk and recommended collection of a total 24-hour specimen at different stages of lactation (Hytten, 1954a; Macy et al., 1945). Although such a recommendation represents the ideal approach, it is seldom feasible without interfering with the normal lactation process. No one sampling scheme can be endorsed universally for all milk constituents. Each scheme must be designed to accommodate the variation pattern of the constituents to be measured. Failure to do this will often result in an under- or overestimation of daily secretion rates, masking possible influences of maternal nutrition. Variation in the First Weeks Post Partum Changes in milk composition over the course of lactation are most marked during the first weeks of lactation (see examples in Figure 6-1). Colostrum is the fluid secreted by the mammary gland immediately following parturition. It differs from mature human milk in physical characteristics and composition. The intense yellow color of colostrum is indicative of the high concentration of carotenoids, including α-arotene, β-carotene, β-crytoxanthin, lutein, and xeaxanthin. The carotene content of colostrum is about 10-fold higher than that of mature milk (0.34 to 7.57 mg/liter compared with 0.1 to 0.3 mg/liter, respectively [Patton et al., 1990]). During the colostral period, which lasts 4 to 7 days, rapid changes occur in milk composition: concentrations of fat and lactose increase while those of protein and minerals decrease. The term transitional milk is sometimes used to describe the postcolostral period (7 to 21 days post partum), when changes in milk composition occur less rapidly than in the first few days following parturition. Mature human milk (ò21 days post partum) also exhibits variability, but to a much smaller extent than in early lactation. Data for selected nutrients (Appendix C) illustrate this point and indicate variations among studies arising from differences in analytic techniques and other experimental circumstances.

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Nutrition During Lactation TABLE 6-1 Estimates of the Concentrations of Nutrients in Mature Human Milk Nutrient Amount in Human Milka Nutrient Amount in Human Milka   g/liter ± SDbb   µg/liter ± SD Lactose 72.0 ± 2.5 Vitamin A, REd 670 ± 200 Protein 10.5 ± 2.0   (2,230 IUe) Fat 39.0 ± 4.0 Vitamin D 0.55 ± 0.10   mg/liter ± SD Vitamin K 2.1 ± 0.1 Calcium 280 ± 26 Folate 85 ± 37f Phosphorus 140 ± 22 Vitamin B12 0.97g,h Magnesium 35 ± 2 Biotin 4 ± 1 Sodium 180 ± 40 Iodine 110 ± 40 Potassium 525 ± 35 Selenium 20 ± 5 Chloride 420 ± 60 Manganese 6 ± 2 Iron 0.3 ± 0.1 Fluoride 16 ± 5 Zinc 1.2 ± 0.2 Chromium 50 ± 5 Copper 0.25 ± 0.03 Molybdenum NRi Vitamin E 2.3 ± 1.0     Vitamin C 40 ± 10     Thiamin 0.210 ± 0.035     Riboflavin 0.350 ± 0.025     Niacin 1.500 ± 0.200     Vitamin B6 93 ± 8c     Pantothenic acid 1.800 ± 0.200     a Data taken from the Committee on Nutrition (1985), unless otherwise indicated. The values are representative of amounts of nutrients present in human milk; some of them may differ slightly from those reported by investigators cited in the text. b SD = Standard deviation. c From Styslinger and Kirksey (1985), a study of unsupplemented women. d RE = Retinol equivalents. e IU = International units. f From Brown et al. (1986a). g From Sandberg et al. (1981). h Standard deviation not reported; range 0.33 to 3.20. i NR = Not reported. Variation with Length of Gestation There are substantial differences between the milk of mothers who deliver preterm and those who deliver at full term. The subcommittee has focused on lactating mothers of full-term infants; therefore, these differences are only briefly summarized here. During the first 3 to 4 days of lactation, preterm milk (the milk secreted by mothers who delivered prematurely) has higher protein, sodium, and chloride concentrations and lower lactose concentrations than milk secreted by mothers of full-term infants. While some investigators report higher fat concentrations in preterm milk (Anderson et al., 1981; Guerrini et al., 1981),

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Nutrition During Lactation FIGURE 6-1 Changes in the concentrations of lactose and whey proteins in human milk during the progression of lactation in four women during late pregnancy and the first 5 months of lactation. Values obtained for the right and left breast of each woman were averaged and used to calculate the mean plus or minus the standard error of the mean at each period. The zero on the horizontal axis indicated the time of delivery. From Kulski and Hartmann (1981) with permission.

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Nutrition During Lactation others do not (Bitman et al., 1983; Sann, 1981). Calcium, magnesium, and phosphorus concentrations are similar in preterm and full-term milk, as are concentrations of copper, iron, and zinc (Hamosh and Hamosh, 1987). During early lactation the milk produced by women who deliver prematurely undergoes the same changes in composition that occur after full-term pregnancies. The change occurs, however, over a longer period in mothers who deliver prematurely than in mothers of full-term infants (that is, 3 to 5 weeks compared with 3 to 5 days, respectively). The bioactive and immunologic properties of human milk also differ between preterm and full-term milk; this is discussed in detail elsewhere (Goldman, 1989b). Variation in Content of Macronutrients (Fat, Carbohydrate, and Protein) Lipids are among the most variable and difficult nutrients to measure accurately in human milk: among women, the total fat content of 24-hour milk samples may vary from less than 20 g/liter to more than 50 g/liter. However, Hytten (1954b) reports that the average fat content of milk secreted on the seventh day of lactation by any one woman was predictive of the average concentration in later lactation. Within one woman, the fat content of milk increases from the beginning to the end of a single nursing; it differs by as much as 20 g/liter in 24-hour collections on subsequent days, it differs from lactation to lactation in a nonconsistent manner, and it is influenced by the length of time between sample collection (the longest interval yielding the lowest fat values). These large variations complicate the measurement of total fat secreted by lactating women and, in turn, affect calculations of the energy value of milk, which are determined mainly by milk fat content. Among the macronutrients in human milk, lactose appears to be the least variable and thus the least influenced by improper sampling. The coefficient of variation (standard deviation divided by the mean) for human milk lactose content is 7.2% compared with 13% for the total nitrogen content (which is indicative of protein content) and 25% for the fat content in total 24-hour samples (Hytten, 1954c). Precision and Validity of Methods There are adequate methods for quantifying many human milk constituents. Unfortunately, methods designed to study bovine milk or other biologic fluids have been inappropriately applied in the analysis of human milk, thereby providing inaccurate and unreliable information, even in some recent studies. To obtain accurate results, one must apply proper sampling, extraction, handling, and storage procedures as well as a sensitive and selective detection system. A few examples of the many problems that must be addressed are presented below:

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Nutrition During Lactation Bioactive constituents. Enzymes and other bioactive constituents of human milk may alter the composition of expressed milk (Greenberg and Graves (1984), even at temperatures well below 0° C. (Berkow et al., 1984; Bitman et al., 1983). Bound forms. Several of the vitamins (such as vitamin D, folate, and pantothenic acid) are secreted bound to other compounds, and they must be released before they can be completely extracted or detected. For example, accurate measurement of the total content of pantothenic acid in human milk requires double enzyme hydrolysis (Song et al., 1984). Distribution in aqueous and lipid fractions. Vitamin D and its metabolites are secreted in the aqueous fraction of human milk and are attached to binding proteins (Hollis et al., 1982), but on standing they diffuse to the lipid fraction of milk. Thus, whether aqueous or lipid solvents are used should be determined by the handling procedure. Other sources of measurement errors. Commercial sources of reagents such as enzymes may be contaminated with vitamins and be responsible for falsely elevated levels in milk (Song et al., 1984). Many of the water-soluble vitamins are measured by microbiological assays. Care must be taken to ensure that the vitamin to be measured is stable under the extraction method employed and that the vitamin is converted to a form that can be utilized by the test organism. For example, the folate content of human milk is likely to be underestimated unless an antioxidant is used to prevent it from being oxidized, conjugase pretreatment is performed to cleave the long-chain forms of the vitamin, heat treatment is applied to release the folate from its binding proteins before microbiological analysis, and test organisms are selected that are able to use all the forms of folate in the samples (O'Connor et al., 1990a). The reproducibility and validity of techniques used in different studies could not always be ascertained by the subcommittee. Thus, the data on the nutrient content of human milk must be interpreted with caution. Large variations reported for many milk constituents may reflect improper sampling or analytic inaccuracies or both rather than true biologic variance. In addition to the methodologic concerns just described, there are problems of measurement and detection specific to nonnutrient constituents, as follows: The leukocytes in human milk are difficult to identify because their morphology is altered by the presence of many intracytoplasmic lipid bodies. Certain constituents, such as secretory immunoglobulin A (IgA), exist in a different physical form than they do in other tissues, such as blood, and therefore require discrete detection procedures. The titer of specific antibodies in human milk depends on whether the woman has recently been exposed to the relevant immunogen via the intestinal or respiratory tract.

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Nutrition During Lactation TABLE 6-2 Origins of Nutrients in Human Milka Origin Proteins Carbohydrates Lipids Vitamins Minerals Synthesis in mammary gland x x x o o Transfer from plasma to milk x x x x x a x indicates that the nutrient has this origin; o indicates that it does not. Nonspecific blocking factors in human milk may interfere with the detection of certain components by solid-phase immunoassays. Clearly, considerable effort is required to reliably detect and quantify many of the constituents in human milk and, therefore, to determine whether changes in maternal nutrition influence the content of such constituents in milk. There are other methodologic issues that are likely to hamper investigations of the influence of maternal nutrition on milk composition. Most recently, nutrient-nutrient interrelations have emerged as possible confounding variables. For example, a study of preterm infants indicates that zinc undernutrition could be responsible for low vitamin A levels in serum (Hustead et al., 1988). If this is also true for lactating women, supplemental vitamin A would have no effect on the vitamin A level in milk. Similarly, maternal iron deficiency in rats can cause an impairment of milk folic acid secretion that is not corrected with supplemental folic acid (O'Connor et al., 1990a). ORIGIN OF MILK CONSTITUENTS There are three sources of the milk constituents: some are synthesized in the mammary secretory cell from precursors in the plasma, some are produced by other cells in the mammary gland, and others are transferred directly from plasma to milk (see Table 6-2). All physiologic and biochemical phenomena that influence the composition of plasma may also affect the composition of milk. Milk composition can be modified further by hormones or other bioactive factors that are capable of influencing biosynthetic processes in the mammary gland. Metabolic changes and their relationships with milk production and composition have been well documented in studies in animals, especially cows, goats, and rats. The mixed origin of milk constituents is well illustrated by considering the lipid components of milk. Milk triglycerides (which account for 98% of the total lipid content) are synthesized in the mammary alveolar cell. Fatty acids may be derived from the plasma (transported there from either the intestine or fat deposits), or they may be synthesized from glucose within the mammary gland. The origins of the fatty acids can be distinguished: fatty acids synthesized within the mammary gland have chain lengths of 16 carbons or less; those derived

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Nutrition During Lactation from dietary sources (other than dairy products) and from adipose tissue tend to have longer carbon chains. The increase in prolactin level preceding and during lactation (Zinder et al., 1974) has two important effects on lipids. (1) Lipoprotein lipase activity in the mammary gland increases sharply (Hamosh et al., 1970). This enzyme hydrolyzes triglycerides and thus frees their fatty acids for transport into the cell, where they are reesterified. (2) Lipoprotein lipase activity in adipose tissue decreases (Hamosh et al., 1970). Both of these channel fat to the lactating mammary gland, where it is incorporated in the milk. MATERNAL NUTRITION AND THE COMPOSITION OF HUMAN MILK Three aspects of maternal nutrition could have an impact on human milk composition: current dietary intake, nutrient stores, and alterations in nutrient utilization as influenced by the hormonal milieu characteristic of lactation. Alterations in maternal nutrition that change the composition of human milk may have positive, neutral, or negative consequences to the nursing infant (see Chapter 7). When maternal nutrition is continuously compromised but the concentrations of nutrients in milk and the milk volume remain unchanged, the nutrients for milk synthesis are being furnished by maternal stores or body tissues. It has not been determined when this situation has a negative impact on the mother. Chapter 9 considers this in more detail. As explained in the preceding section, investigators must carefully control for stage of lactation in studies to determine the effects of maternal nutrition on milk composition. Other factors that must be considered in such studies include frequency of nursing, environmental conditions (e.g., the specificity of secreted antibodies in human milk after exposure to infectious agents), and length of gestation. Macronutrients: Protein, Fat, and Carbohydrate Protein Milk proteins are broadly classified as caseins and whey proteins. Caseins are phosphoproteins that occur only in milk. Molecules of casein associate in combination with calcium, phosphate, and magnesium ions in structures known as micelles. These micelles enable milk to carry a much larger quantity of calcium, phosphate, and magnesium than could be carried in a simple aqueous solution. The whey proteins, such as α-lactalbumin and lactoferrin, are synthesized in the mammary gland; other proteins (including serum albumin and several bioactive enzymes and protein hormones) are transported to the milk from plasma. In addition, dimeric IgA is produced by plasma cells in the mammary gland and is transported into the milk by specific receptors. Human

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Nutrition During Lactation milk also contains a variety of nonprotein nitrogen-containing compounds, including amino acids, peptides, N-acetyl sugars, urea, and nucleotides. Commonly used methods for measuring the protein content of human milk are nonspecific but often produce approximately the same results (Lönnerdal, 1985b). However, if the protein content of human milk is measured colorimetrically, an overestimation of approximately 25 to 40% is possible (Lönnerdal et al., 1987). Using amino acid analysis, Lönnerdal and coworkers (1976c) found that the protein content of mature human milk was approximately 8 to 9 g/liter. Similar values were found using nitrogen analysis of precipitated proteins, among diverse populations, i.e., disadvantaged Ethiopian women and privileged Swedish women (Lönnerdal et al., 1976a,b) and privileged U.S. women (Butte, 1984b). The nitrogen analysis method was used in a World Health Organization collaborative study, in which mature milk was found to contain 8.8, 8.3, 8.3, 7.6, and 12 g/liter in Hungary, Sweden, Guatemala, the Philippines, and Zaire, respectively (WHO, 1985). The reasons for the much higher results from Zaire are not clear. Methods based on amino acid analysis should yield results that reflect the sum of free and protein-bound amino acids. Nitrogen analyses of precipitated proteins exclude free amino acids and small peptides which may account for approximately 7 to 10% of the total amino acids found in human milk (Svanberg et al., 1977). There is no convincing evidence that diet or body composition influence the total concentration of milk protein, even in communities of undernourished women (Lönnerdal, 1986b); however, the interpretation of some studies is hampered by the use of total nitrogen as a proxy measure for the total amino acid content of milk (Deb and Cama, 1962) or by the short diet periods used in metabolic studies (Forsum and Lönnerdal, 1980). In a study of three well-nourished Swedish women, Forsum and Lönnerdal (1980) demonstrated that an increased maternal intake of protein (20% compared with 8% of energy from protein) increased total nitrogen, protein, and nonprotein nitrogen contents of mature human milk and 24-hour milk protein output. There have been reports of low concentrations of protein and altered free and total amino acid nitrogen profiles in milk of women from countries with limited food supplies: India (Deb and Cama, 1962), Pakistan (Lindblad and Rahimtoola, 1974), and Guatemala (Wurtman and Fernstrom, 1979). The nonprotein nitrogen content of human milk is higher than that in milk of other species; the importance of this to infant nutrition and health is unknown (Carlson, 1985). Taurine, an amino acid found only in animal products, is the second most abundant free amino acid in human milk (Rassin et al., 1978). Even the milk secreted by women who ingest no animal foods contains taurine concentrations of approximately 35 mg/dl—lower than concentrations in milk secreted by omnivores (54 mg/dl) but 30 times greater than levels in bovine

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Nutrition During Lactation milk (Rana and Sanders, 1986). Taurine functions in bile acid conjugation and may also function as an inhibitory neurotransmitter and as a membrane stabilizer. A broad spectrum of nucleotides occurs in human milk (Janas and Picciano, 1982), but the effects of maternal nutrition on the concentrations of these nucleotides have not yet been reported. Lipids The lipids in milk are contained within membrane-enclosed milk fat globules, the core of which consists of triglycerides—the major energy source in milk. The globule membrane is composed mainly of phospholipids, cholesterol, and proteins. Although there is no compelling evidence that changes in maternal fat intake influence the total quantity of milk fat, it has been shown repeatedly that the nature of the fat consumed by the mother will influence the fatty acid composition of milk (Jensen, 1989). For example, milk from four complete vegetarian women in Great Britain was found to contain five times as much C18:2 fatty acids as milk from four nonvegetarian women (31.9 and 6.9%, respectively) (Sanders et al., 1978). Finley et al. (1985) noted that, as lactation progressed, milk from both vegetarian and nonvegetarian women contained more fatty acids principally synthesized in the mammary gland (C8:0, C10:0, C12:0, C14:0) and less from the diet and adipose tissue. Chappell et al. (1985a) reported that the trans fatty acid content of human milk was directly related to maternal intake of partially hydrogenated fats and oils; in women experiencing postpartum weight loss, fat mobilized from adipose tissue also contributed trans fatty acids to human milk fat independently of current dietary intake. In the classic study of a single subject by Insull and colleagues (1959), both the total energy and fat contents of the diet were altered. Their results demonstrated that mammary lipid synthesis was influenced by energy balance as well as by the type and amount of fat in the diet. When the subject was fed excess energy as a low-fat, high-carbohydrate diet, the investigators found that 40 to 60% of the fatty acids in milk fat had carbon chain lengths of less than 16. On a very high fat diet (70% of kilocalories as corn oil) that was adequate in energy, the combined linoleic and linolenic acid content of the milk fatty acids increased from approximately 2 to 45%, and there was a corresponding drop in the content of shorter-chain saturated fatty acids. When a low-fat, calorie-restricted diet was fed, C16 or longer-chain saturated fatty acids predominated in the milk, indicating that stored body fat was utilized for milk fat synthesis. Effects of such changes on infant health have not been studied. Using stable isotope methodology, Hachey and colleagues (1987, 1989) confirmed the results of the study of Insull et al. (1959) showing that diet composition affects milk fat synthesis. Hachey et al. estimate that when the

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Nutrition During Lactation Bitman, J., D.L. Wood, N.R. Mehta, P. Hamosh, and M. Hamosh. 1983. Lipolysis of triglycerides in human milk at low temperatures: a note of caution. J. Pediatr. Gastroenterol. Nutr. 2:521-524. Blanc, B. 1981. Biochemical aspects of human milk—comparison with bovine milk. World Rev. Nutr. Diet. 36:1-89. Brines, R.D., and J.H. Brock. 1983. The effect of trypsin and chymotrypsin on the in vitro antimicrobial and iron-binding properties of lactoferrin in human milk and bovine colostrum. Biochim. Biophys. Acta 759:229-235. Brown, C.M., A.M. Smith, and M.F. Picciano. 1986a. Forms of human milk folacin and variation patterns. J. Pediatr. Gastroenterol. Nutr. 5:278-282. Brown, K.H., N.A. Akhtar, A.D. Robertson, and M.G. Ahmed. 1986b. Lactational capacity of marginally nourished mothers: relationships between maternal nutritional status and quantity and proximate composition of milk. Pediatrics 78:909-919. Bullen, J.J., H.J. Rogers, and E. Griffiths. 1978. Role of iron in bacterial infection. Curr. Top. Microbiol. Immunol. 80:1-35. Burgio, G.R., A. Lanzavecchia, A. Plebani, S. Jayakar, and A.G. Ugazio. 1980. Ontogeny of secretory immunity: levels of secretory IgA and natural antibodies in saliva. Pediatr. Res. 14:1111-1114. Butte, N.F., and D.H. Calloway. 1981. Evaluation of lactational performance of Navajo women. Am. J. Clin. Nutr. 34:2210-2215. Butte, N.F., R.M. Goldblum, L.M. Fehl, K. Loftin, E.O. Smith, C. Garza, and A.S. Goldman. 1984a. Daily ingestion of immunologic components in human milk during the first four months of life. Acta Paediatr. Scand. 73:296-301. Butte, N.F., C. Garza, J.E. Stuff, E.O. Smith, and B.L. Nichols. 1984b. Effect of maternal diet and body composition on lactational performance. Am. J. Clin. Nutr. 39:296-306. Carlson, S.E. 1985. Human milk nonprotein nitrogen: occurrence and possible functions . Adv. Pediatr. 32:43-70. Carpenter, G. 1980. Epidermal growth factor is a major growth-promoting agent in human milk. Science 210:198-199. Casey, C.E., M.R. Neifert, J.M. Seacat, and M.C. Neville. 1986. Nutrient intake by breastfed infants during the first five days after birth. Am. J. Dis. Child. 140:933-936. Casey, C.E., M.C. Neville, and K.M. Hambidge. 1989. Studies in human lactation: secretion of zinc, copper, and manganese in human milk. Am. J. Clin. Nutr. 49:773-785. Cavell, P.A., and E.M. Widdowson. 1964. Intakes and excretions of iron, copper, and zinc in the neonatal period. Arch. Dis. Child. 39:496-501. Cevreska, S., V.P. Kovacev, M. Stankovski, and E. Kamamaras. 1975. The presence of immunologically reactive insulin in milk of women during the first week of lactation and its relation to changes in plasma insulin concentrations. God. Zb. Med. Fak. Skopje. 21:35-41. Chappell, J.E., M.T. Clandinin, and C. Kearney-Volpe. 1985a. Trans fatty acids in human milk lipids: influence of maternal diet and weight loss . Am. J. Clin. Nutr. 42:49-56. Chappell, J.E., T. Francis, and M.T. Clandinin. 1985b. Vitamin A and E content of human milk at early stages of lactation. Early Hum. Dev. 11:157-167. Chappell, J.E., T. Francis, and M.T. Clandinin. 1986. Simultaneous high performance chromatography analysis of retinol esters and tocopherol isomers in human milk. Nutr. Res. 6:849-852.

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Nutrition During Lactation Chipman, D.M., and N. Sharon. 1969. Mechanism of lysozyme action. Science 165:454-465. Cleary, T.G., J.P. Chambers, and L.K. Pickering. 1983. Protection of suckling mice from the heat-stable enterotoxin of Escherichia coli by human milk. J. Infect. Dis. 148:1114-1119. Committee on Nutrition. 1985. Composition of human milk: normative data. Pp. 363-368 in Pediatric Nutrition Handbook, 2nd ed. American Academy of Pediatrics, Elk Grove Village, Ill. Crago, S.S., S.J. Prince, T.G. Pretlow, J.R. McGhee, and J. Mestecky. 1979. Human colostral cells. I. Separation and characterization. Clin. Exp. Immunol. 38:585-597. Cruz, J.R., B. Carlsson, and B. García. 1982. Studies in human milk. III. Secretory IgA quantity and antibody levels against Escherichiae coli in colostrum and milk from underprivileged and privileged mothers. Pediatr. Res. 16:272-276. Cumming, F.J., and M.H. Briggs. 1983. Changes in plasma vitamin A in lactating and nonlactating oral contraceptive users. Br. J. Obstet. Gynaecol. 90:73-77. Dallman, P.R. 1986. Iron deficiency in the weanling: a nutritional problem on the way to resolution. Acta Paediatr. Scand. Suppl. 323:59-67. Deb, A.K., and H.R. Cama. 1962. Studies on human lactation. Dietary nitrogen utilization during lactation, and distribution of nitrogen in mother's milk. Br. J. Nutr. 16:65-73. Debski, B., D.A. Finley, M.F. Picciano, B. Lönnerdal, and J.A. Milner. 1989. Selenium content and glutathione peroxidase activity of milk from vegetarian and nonvegetarian women. J. Nutr. 119:215-220. Delange, F. 1985. Physiopathology of iodine nutrition. Pp. 291-299 in R.K. Chandra, ed. Trace Elements in Nutrition of Children. Nestle Nutrition Workshop Series, Vol. 8. Raven Press, New York. Department of Health and Social Security. 1977. Composition of Mature Human Milk. Report on Health and Social Security. 12. Her Majesty's Stationery Office, London. Dewey, K.G., D.A. Finley, and B. Lönnerdal. 1984. Breast milk volume and composition during late lactation (7-20 months). J. Pediatr. Gastroenterol. Nutr. 3:713-720. Ekstrand, J., C.J. Spak, J. Falch, J. Afseth, and H. Ulvestad. 1984a. Distribution of fluoride to human breast milk: following intake of high doses of fluoride. Caries Res. 18:93-95. Ekstrand, J., L.I. Hardell, and C.J. Spak. 1984b. Fluoride balance studies on infants in a 1-ppm-water-fluoride area. Caries Res. 18:87-92. Ellis, L., M.F. Picciano, A.M. Smith, M. Hamosh, and N.R. Mehta. 1990. The impact of gestational length on human milk selenium concentration and glutathione peroxidase activity. Pediatr. Res. 27:32-50. Esala, S., E. Vuori, and A. Helle. 1982. Effect of maternal fluorine intake on breast milk fluorine content. Br. J. Nutr. 48:201-204. Feeley, R.M., R.R. Eitenmiller, J.B. Jones, Jr., and H. Barnhart. 1983. Copper, iron, and zinc contents of human milk at early stages of lactation. Am. J. Clin. Nutr. 37:443-448. Finley, D.A., B. Lönnerdal, K.G. Dewey, and L.E. Grivetti. 1985. Breast milk composition: fat content and fatty acid composition in vegetarians and nonvegetarians. Am. J. Clin. Nutr. 41:787-800. Forsum, E., and B. Lönnerdal. 1980. Effect of protein intake on protein and nitrogen composition of breast milk. Am. J. Clin. Nutr. 33:1809-1813. Fransson, G.B., and B. Lönnerdal. 1980. Iron in human milk. J. Pediatr. 96:380-384.

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