7
Infant Outcomes

Because the exclusively breastfed infant is entirely dependent upon the mother for nutrition, the subcommittee examined the evidence relating maternal nutrition to infant health. In addition to nutrients in human milk, it considered constituents that have important nonnutritive functions (see Chapter 6).

As discussed in Chapters 5 and 6, the adequacy of the maternal diet may affect the formation, composition, or secretion of milk. As nutritional demands of the infant increase, milk production becomes correspondingly greater (see Chapter 5). Thus, there is a complex interrelationship between maternal nutrition, volume and composition of the milk, and the vigor of the infant.

Since infant nutrition, growth, development, and health are interrelated, the effects of breastfeeding and maternal nutrition on each of these outcomes were reviewed. The health-related outcomes include resistance to infectious diseases, allergic disorders, and chronic diseases with an immunologic basis that develop later in childhood; the passage of infectious or toxic agents in milk to the recipient; and infant mortality. Because of the specific tasks assigned to the subcommittee, this review was limited to effects on full-term infants.

In reviewing the relevant literature, the subcommittee had to contend with several confounding factors that potentially alter the interpretation of the results. For example, sick infants may be unable to breastfeed because they are separated from their mothers or because they are unable to suckle adequately. In such circumstances, if the mother does not continue lactation by pumping, breastfeeding is difficult to resume if or when the child recovers. Thus, illness may cause the cessation of breastfeeding, rather than the absence of breastfeeding causing illness. In many cultures, there is a strong relationship



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Nutrition During Lactation 7 Infant Outcomes Because the exclusively breastfed infant is entirely dependent upon the mother for nutrition, the subcommittee examined the evidence relating maternal nutrition to infant health. In addition to nutrients in human milk, it considered constituents that have important nonnutritive functions (see Chapter 6). As discussed in Chapters 5 and 6, the adequacy of the maternal diet may affect the formation, composition, or secretion of milk. As nutritional demands of the infant increase, milk production becomes correspondingly greater (see Chapter 5). Thus, there is a complex interrelationship between maternal nutrition, volume and composition of the milk, and the vigor of the infant. Since infant nutrition, growth, development, and health are interrelated, the effects of breastfeeding and maternal nutrition on each of these outcomes were reviewed. The health-related outcomes include resistance to infectious diseases, allergic disorders, and chronic diseases with an immunologic basis that develop later in childhood; the passage of infectious or toxic agents in milk to the recipient; and infant mortality. Because of the specific tasks assigned to the subcommittee, this review was limited to effects on full-term infants. In reviewing the relevant literature, the subcommittee had to contend with several confounding factors that potentially alter the interpretation of the results. For example, sick infants may be unable to breastfeed because they are separated from their mothers or because they are unable to suckle adequately. In such circumstances, if the mother does not continue lactation by pumping, breastfeeding is difficult to resume if or when the child recovers. Thus, illness may cause the cessation of breastfeeding, rather than the absence of breastfeeding causing illness. In many cultures, there is a strong relationship

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Nutrition During Lactation between the type of infant feeding and the social status and functioning of the family. In the United States, breastfeeding rates increase with an increase in socioeconomic status. The favorable environment of these women and their infants is associated with a lower risk of many illnesses. In addition, since surveys indicate that the breastfeeding mother is less likely to smoke, her infant is at lower risk of respiratory problems from exposure to passive cigarette smoke. Further, the young infant in day care—often because the mother is working (and therefore less likely to breastfeed)—may be exposed to communicable diseases more often than the infant cared for exclusively at home. Thus, the lower risks of morbidity reported for breastfed infants may be in part due to factors other than breastfeeding. Other potential sources of bias are reviewed by Kramer (1987). INFANT NUTRITION: VITAMINS AND MINERALS Human milk serves as the nutritional standard for infants. Certain nutrients (vitamins A, D, K, B12, riboflavin, and folate; iron; copper; zinc; and fluoride) are reviewed in this section to illustrate the uniqueness of human milk and relationships, if any, of the infant's nutritional status to maternal nutrient stores and maternal diet. Other essential nutrients are of no less importance to the infant; information about them is presented in Chapter 6. Three major factors contribute to the nutritional status of the exclusively breastfed infant: nutrient stores, especially those accumulated in utero; the amount and bioavailability of nutrients supplied by human milk; and environmental and genetic factors that influence the efficiency of nutrient utilization. Nutrient stores at birth are determined by the rate of placental nutrient transfer and by the duration of gestation. The stores of many nutrients increase substantially during the last trimester of pregnancy and tend to be higher in infants with higher birth weight or greater gestational age. The infant's total nutrient intake is determined by nutrient concentrations in human milk and by the volume of milk consumed. The amount of nutrient absorbed by the infant is further influenced by the bioavailability of that nutrient in human milk. Providing the breastfed infant with supplemental foods has a complex effect on the total amount of nutrient absorbed. For example, infants consuming such foods as formula or infant cereal generally decrease their intake of human milk (see Chapter 5) and, thus, the nutrients and other specialized components it supplies. Thus, the intake of supplementary foods may add nutrients in a less bioavailable form, decrease the bioavailability of nutrients in human milk, and decrease the intake of other important factors in human milk. Growth, infections, and differences in the efficiency of nutrient utilization affect the infant's rate of nutrient utilization, which in turn can influence the infant's nutritional status. Birth weight is inversely associated with the rate of nutrient utilization. For example, infants who are small at birth usually

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Nutrition During Lactation experience catch-up growth during infancy. Disease or injury may adversely affect nutrient utilization either directly by increasing rates of catabolism or urinary and fecal losses or indirectly by sequestrating a nutrient in tissue compartments. Finally, other environmental influences, such as the degree of exposure to ultraviolet light (ordinarily from sunshine) in the case of the synthesis of vitamin D, may be important determinants of the nutritional status of the infant. Fat-Soluble Vitamins Vitamin D Plasma levels of 25-hydroxycholecalciferol (a vitamin D metabolite used as a measure of vitamin D status) in the mother are positively correlated with those in the neonate, providing evidence that maternal vitamin D status affects the infant's vitamin D stores (Hillman and Haddad, 1974; Hoogenboezem et al., 1989; Markestad, 1983; Markestad et al., 1983). Several investigators have found that plasma concentrations of 25-hydroxycholecalciferol in the neonate are within the normal range for adults (10 to 40 ng/ml) (Markestad, 1983; Roberts et al., 1981), whereas Ala-Houhala (1985) reported that 25-hydroxycholecalciferol plasma levels in Finnish neonates were abnormally low in winter (mean, <10 ng/ml) compared with the range of values found in summer (12 to 18 ng/ml, p < .001). These studies suggest that infants born to mothers with inadequate vitamin D status are highly dependent on a regular supply of vitamin D through diet, supplements, or exposure to ultraviolet light. Plasma 25-hydroxycholecalciferol levels in unsupplemented breastfed infants have been compared with those of formula-fed infants or breastfed infants receiving approximately 10 µg of supplemental vitamin D per day. In six reports, plasma 25-hydroxycholecalciferol levels were substantially lower in unsupplemented breastfed infants (Ala-Houhala, 1985; Chan et al., 1982; Greer et al., 1982; Lichtenstein et al., 1986; Markestad, 1983; Roberts et al., 1981). Four studies (Ala-Houhala, 1985; Greer et al., 1982; Hoogenboezem et al., 1989; Markestad, 1983) have shown plasma levels of this compound at or below the lower limits of normal (≤10 ng/ml) (Nutrition Foundation, 1984) in the unsupplemented groups. Ala-Houhala (1985) reported that in the winter months, 10 of 18 unsupplemented breastfed infants had plasma levels of less than 5 ng/ml, which may lead to rickets (Nutrition Foundation, 1984). Despite reports of rickets in breastfed infants (Arnaud et al., 1976; O'Connor, 1977; Ozsoylu, 1977) and the low vitamin D content of human milk, breastfeeding has long been considered to be protective against rickets (Belton, 1986; Lakdawala and Widdowson, 1977). Breastfed infants require approximately 30 minutes of exposure to sunlight per week if wearing only a diaper, or 2 hours per week if fully clothed without a hat, to maintain normal serum 25-hydroxycholecalciferol levels (Specker et

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Nutrition During Lactation al., 1985). Darkly pigmented infants require a greater exposure to sunshine to initiate the synthesis of vitamin D in the skin (Clemens et al., 1982). In a study by Greer and colleagues (1982), which included randomization of breastfed infants to a placebo or to a daily supplement of 10 µg of vitamin D, the bone mineral content of the placebo group was significantly lower in the first few months after birth but slightly higher than that of the supplemented group by the end of the first year. In summary, exclusive breastfeeding results in normal infant bone mineral content when maternal vitamin D status is adequate and the infant is regularly exposed to sunlight. If the infant or mother is not exposed regularly to sunlight, or if the mother's intake of vitamin D is low, supplements for the infant may be indicated (5 to 7.5 µg/day). Vitamin A Although vitamin A concentrations in human milk are dependent on the mother's vitamin A status, vitamin A deficiency is rare among breastfed infants, even in parts of the world with endemic vitamin A deficiency (Sommer, 1982). Even after breastfeeding is discontinued, it appears to confer a protective effect (Sommer, 1982; West et al., 1986), presumably because some of the vitamin A provided by human milk is stored in the liver. Infants who consume human milk that provides 100 to 151 µg of retinol equivalents per day grow well and do not show signs of vitamin A deficiency. In the United States, human milk provides approximately twice this amount (FAO, 1988; NRC, 1989). These U.S. concentrations are used as the international standard for adequate vitamin A intakes in infancy (FAO, 1988; NRC, 1989). In the United States, there is no indication to routinely supplement either the infant or the mother with vitamin A. Vitamin K Vitamin K is essential for the formation of several proteins required for blood clotting. This vitamin has two major forms: vitamin K1 (phylloquinone), synthesized by plants, and vitamin K2 (menaquinone), synthesized by bacteria. Most of the vitamin K in human milk is phylloquinone; the extent to which infants absorb menaquinone produced by gut microflora is not known. Vitamin K stores at birth are extremely low. Therefore, newborns are immediately dependent on an external source of the vitamin, but the amount provided by human milk is low—approximately 2 µg/liter (Committee on Nutrition, 1985; NRC, 1989). Bacteria that colonize the intestinal tracts of breastfed infants produce less menaquinone than do those in formula-fed infants. A deficiency of the vitamin produces a syndrome in infants called hemorrhagic disease of the newborn. This vitamin K-dependent disease has two different clinical forms. The classic early-onset form occurs at age 2 to 10

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Nutrition During Lactation days in 1 of 200 to 400 unsupplemented newborns. The late-onset form occurs around 1 month of age in 1 of 1,000 to 2,000 unsupplemented newborns. Late-onset hemorrhagic disease of the newborn is a devastating, often fatal disease (Gleason and Kerr, 1989). Both forms occur more often in unsupplemented breastfed than formula-fed infants. Although maternal supplementation with vitamin K in the last weeks of pregnancy (Owen et al., 1967) or unusually high milk intakes (>500 ml) during the first 3 days of postnatal life (Motohara et al., 1989) may reduce the risk of hemorrhagic disease of the newborn, the most dependable method of preventing this serious disorder is to inject the infant with 0.5 to 1.0 mg of vitamin K at birth or to give an oral 1.0- to 2.0-mg dose, as recommended by the American Academy of Pediatrics (Committee on Nutrition, 1985) and required by many states. Water-Soluble Vitamins Vitamin B12 Full-term infants of adequately nourished women are born with a total body vitamin B12 content of 30 to 40 µg (FAO, 1988). Assuming that 0.10 µg/day is required during infancy (FAO, 1988), these stores would supply an infant's needs for approximately 8 months. The 0.4 µg of vitamin B12 per day usually provided by human milk to the exclusively breastfed infant provides for ample accumulation of stores (FAO, 1988; NRC, 1989). Vitamin B12 concentrations in milk, and thus the infant's intake of this vitamin, are dependent on the mother's B12 intake and stores. Breastfed infants born to women who eat little or no animal foods are at risk for developing vitamin B12 deficiency. In a study of six vitamin B12-deficient, exclusively breastfed infants in India, vitamin B12 concentrations in their mother's milk ranged from 0.03 to 0.07 µg/liter (Jadhav et al., 1962). Vitamin B12 deficiency has also been found in breastfed infants of complete vegetarian mothers in industrialized countries (Close, 1983; Davis et al., 1981; Gambon et al., 1986; Higgenbottom et al., 1978; Rendle-Short et al., 1979; Sklar, 1986). Urinary methylmalonic acid (UMMA) concentrations of the breastfed infants of omnivorous mothers were significantly lower (p = .05) than those of infants of complete vegetarians; maternal serum B12 concentrations were negatively associated with maternal UMMA (p = .003) and infant UMMA (p < .001) levels (Specker et al., 1988). In general, the deficiency syndrome is usually not clinically apparent until the latter half of infancy. An important finding is that breastfed infants may develop clinical signs of vitamin B12 deficiency before their mothers do (Lampkin and Saunders, 1969; McPhee et al., 1988). For infants of mothers eating a mixed diet that includes animal foods, human milk is a generous source of vitamin B12; it provides for the infant's needs

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Nutrition During Lactation throughout the first year of life. For mothers who are complete vegetarians, it is desirable to find an acceptable food source or supplement of vitamin B12 that will meet their needs and those of the nursing infant. Folate The full-term infant is born with adequate folate stores, even when maternal folate is suboptimal (Salmenperä et al., 1986b). The bioavailability of folate in human milk is high: to maintain equivalent folate status in formula-fed infants, approximately 50% more folate is required from formula than from human milk (Ek and Magnus, 1982). Serum and red cell folate levels are adequate in breastfed infants; indeed, they are several-fold greater than adult reference levels (Ek and Magnus, 1979; Salmenperä et al., 1986b; Smith et al., 1985). This is reported for infants exclusively breastfed for up to 1 year (Salmenperä et al., 1986b). Maternal folate levels in serum and milk do not appear to be correlated; however, there are strong associations between maternal and infant serum folate levels at 6 weeks and at 3 months after birth (Smith et al., 1983) and at 4 and 9 months after birth (Salmenperä et al., 1986b). Those associations suggest that folate stores accumulated in utero are more important determinants of folate status during infancy than are levels of folate in milk. Riboflavin Biochemical data concerning the riboflavin status of infants are difficult to interpret. Hovi and colleagues (1979) reported a transient increase in the activation coefficient of erythrocyte glutathione reductase (EGR) in full-term healthy breastfed newborns—a finding that suggests riboflavin deficiency. The increase became even greater when the infants had received phototherapy for treatment of hyperbilirubinemia (Gromisch et al., 1977; Hovi et al., 1979; Tan et al., 1978); however, this was not accompanied by clinical signs of riboflavin deficiency. The increase in the activation coefficient did not occur with daily maternal riboflavin supplements of 0.5 mg/kg of body weight, but neither was this increase evident after 2 weeks in the infants of unsupplemented women (Nail et al., 1980). The riboflavin concentration in human milk is dependent on maternal riboflavin status (Bates et al., 1982). High EGR activation coefficients have been reported for breastfed infants who receive only 0.13 to 0.21 mg of riboflavin per day from human milk (Bates et al., 1982). The average intake of riboflavin in exclusively breastfed infants in the United States is estimated to be 0.26 mg/day. Using several criteria, including riboflavin levels in urine and blood, Snyderman and coworkers (1949) found that riboflavin intakes of 0.3 to 0.4 mg/day provide adequate riboflavin status. Among infants undergoing phototherapy, comparable intakes of riboflavin maintain normal EGR activation coefficients (Tan et al., 1978). No

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Nutrition During Lactation longitudinal studies of representative populations have been conducted in developed countries to determine the adequacy of riboflavin status among breastfed infants. No reports of riboflavin deficiency among exclusively breastfed infants in the United States were encountered in the review of the literature by the subcommittee. Minerals Iron Iron deficiency and iron deficiency anemia remain important problems in the United States and the rest of the world. The estimated worldwide prevalence of anemia in children from birth to age 4 years is 43%. There are remarkable differences in the prevalence rates of iron deficiency anemia in economically developed regions (~12%) and developing areas (~51%) of the world (FAO, 1988). In the United States, children aged 1 to 2 years have a higher prevalence of iron deficiency (9.3%) than do people in other age groups (DHHS, 1988). Although inadequate iron intakes are not the sole cause of anemia in infants and children, diets low in iron play a major etiologic role. A heavy demand is placed on the iron reserves of breastfed infants: the estimated daily physiologic requirement is 0.7 mg for growth and 0.2 mg to replace basal losses (Dallman, 1986). Human milk provides from 0.15 to 0.68 mg of iron per day. Approximately 50% of iron is absorbed from human milk compared with 7% from iron-fortified formula and 4% from infant cereals (Dallman, 1986). The iron concentration in milk is not influenced by the mother's iron status (Dallman, 1986; Murray et al., 1978; Siimes et al., 1984). Body stores of iron and ferritin levels increase during the first 3 months of postnatal life and then drop during the fourth to sixth months (Duncan et al., 1985; Garry et al., 1981; Saarinen et al., 1977). Despite those changes, iron deficiency is uncommon in breastfed infants during their first 6 months (Duncan et al., 1985; Garry et al., 1981; Owen et al., 1981; Picciano and Deering, 1980; Saarinen and Siimes, 1979a; Saarinen et al., 1977). Woodruff and colleagues (1977) suggest that partially breastfed infants younger than 6 months are at risk of iron deficiency: they found a hemoglobin level lower than 11.0 g/dl in 1 of 12 breastfed infants and a transferrin saturation of less than 16% in 4 of them. Mothers in that study were instructed to feed supplementary foods to the infants at age 3 months; foods high in iron content were offered in limited amounts. Supplementary foods lead to decreased intake of human milk and possibly impair the absorption of iron from human milk (Oski and Landaw, 1980). Two studies of a total of 43 infants indicated that there is a risk of iron deficiency by age 9 months if human milk is the infant's only food (Pastel et al., 1981; Siimes et al., 1984). Therefore, foods with bioavailable iron,

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Nutrition During Lactation iron-fortified foods, or an iron supplement should be given beginning at age 6 months (or earlier, if supplementary foods are introduced before that time). Copper Full-term infants have relatively large copper stores at birth (Brückmann and Zondek, 1939; Widdowson et al., 1972). The relationship between maternal copper status and concentration in human milk is weak (Munch-Peterson, 1950; Salmenperä et al., 1986a; Vuori et al., 1980). Serum copper levels were higher among the older infants in a cross-sectional study of breastfed infants ranging from newborns through age 12 months (Ohtake, 1977). Salmenperä and coworkers (1986a) found that ceruloplasmin as well as serum copper consistently rose during 12 months of exclusive breastfeeding, despite the low copper intakes characteristic of breastfed infants. The daily intakes from months 4 to 9 ranged from 0.03 to 0.26 mg/day—less than the Food and Nutrition Board's estimated safe and adequate daily dietary intake of 0.4 to 0.6 mg/day for infants aged 0 to 6 months (NRC, 1989). Neither the subcommittee nor Mason (1979) could find case reports of copper deficiency of exclusively breastfed infants. Thus, the evidence suggests that the bioavailability of copper in human milk is high and that the copper status of breastfed infants is adequate during the first year of life. Zinc Human milk has been regarded as a good source of zinc (Lönnerdal et al., 1984); this form of zinc is highly bioavailable (Sandström et al., 1983). The zinc concentration in human milk does not appear to be influenced by the mother's diet (Lönnerdal et al., 1981), but the evidence is not consistent (see Chapter 6). Plasma zinc levels in breastfed infants are similar to those of adults and of infants fed zinc-fortified formula (Hambidge et al., 1979), and they are substantially greater than those of infants fed formula not fortified with zinc (Hambidge et al., 1979; Vigi et al., 1984). Erythrocyte and hair zinc levels also are similar in breastfed infants and infants fed formula fortified with zinc (Hatano et al., 1985; MacDonald et al., 1982). The full-term breastfed infant who is born with usual liver zinc stores is at very low risk of zinc deficiency. Fluoride Although fluoride is not considered to be an essential nutrient, it is beneficial to humans in the prevention of dental caries (NRC, 1989). Fluoride supplementation during infancy helps prevent caries in deciduous teeth; however, caries is a multifactorial disease, and breastfeeding may affect the prevalence of caries in ways other than by the provision of fluoride. The subcommittee found

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Nutrition During Lactation no studies that directly assessed the relationship between the mode of feeding in infancy and the incidence of caries. From the fluoride concentrations in human milk estimated by the Committee on Nutrition (1985), one could project that an exclusively breastfed infant would consume only 0.012 mg of fluoride per day. Fluoride levels are not easily increased by maternal dietary or supplementary fluoride (see Chapter 6). The only other likely source of fluoride in the infant's diet is water. The subcommittee supports the recommendations of the American Academy of Pediatrics that infants receive 0.25-mg fluoride supplements daily if their water supply contains less than 0.3 ppm of fluoride (Committee on Nutrition, 1986). GROWTH AND DEVELOPMENT Historically, growth has been used as the basis to judge the adequacy of nutrient intake by the infant. A major question before the subcommittee was whether nutrition of the lactating woman influences infant growth. Because slow infant growth is sometimes used as a reason for supplementing infants with formula or solid foods or for discontinuing breastfeeding, it was essential to include a brief review of the assessment of infant growth. Interrelationships among infant growth, other indices of development, and maternal nutritional status were found to be difficult to ascertain, since few sound studies had been conducted to address them. Pattern of Growth Although the most commonly used indicators of infant growth have been body weight and weight gain, it is desirable to consider simultaneously length in order to assess linear growth and adiposity (the relationship of weight to length, also indicated by skinfold thickness). Healthy, full-term infants lose an average of approximately 5 to 8% of their body weight during the first week after birth; the percentage lost is somewhat higher among breastfed infants (7.4%) than formula-fed infants (4.9%) (Podratz et al., 1986) but is unlikely to be of clinical importance. After the first week, the pattern of weight gain in infancy depends on the initial size of the infant, whether the infant is breastfed or formula fed, and other environmental and physiologic factors. In industrialized countries, the rate of weight gain of breastfed infants is similar to that of formula-fed infants and to National Center for Health Statistics (NCHS) reference data for infants up to age 2 to 3 months; however, it is less rapid over the subsequent 9 months (Chandra, 1982; Czajka-Narins and Jung, 1986; Dewey et al., 1990a; Duncan et al., 1984; Forsum and Sadurskis, 1986; Garza et al., 1987; Hitchcock et al., 1985; Saarinen and Siimes, 1979b; Salmenperä et al., 1985; Whitehead and Paul, 1984). In developing countries, breastfed infants tend to grow more rapidly than their formula-fed counterparts

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Nutrition During Lactation throughout the first 6 months of postnatal life (Mahmood and Feachem, 1987; Seward and Serdula, 1984; Unni and Richard, 1988). This difference may reflect a greater risk of infection and malnutrition among formula-fed infants in low-income populations living in areas with poor sanitation (Brown et al., 1989). Although most studies have linked differences in the rate of weight gain with the mode of feeding, differences in linear growth between breastfed and formula-fed infants are small if differences in size at birth are controlled (Czajka-Narins and Jung, 1986; Dewey et al., 1989; Hitchcock and Coy, 1989; Nelson et al., 1989). Weight for length tends to be somewhat lower for breastfed infants than for formula-fed infants after age 6 months (Czajka-Narins and Jung, 1986; Dewey et al., 1989; Hitchcock and Coy, 1989). Thus, it is likely that the differences in weight gain patterns represent primarily differences in adiposity. In affluent populations, the difference in rate of growth associated with mode of feeding during infancy is consistent with energy intakes of breastfed and formula-fed infants. At 3 to 4 months of age, reported average energy intakes of breastfed infants are lower than those of formula-fed infants—74 to 91 kcal/kg of body weight compared with 92 to 104 kcal/kg, respectively (Axelsson et al., 1987; Butte et al., 1984; Dewey and Lönnerdal, 1983; Dewey et al., in press; Shepherd et al., 1988). The subcommittee found only one study of infants older than 5 months that compared intakes by feeding method. Dewey et al. (in press) reported that average gross energy intakes of breastfed infants are consistently lower than those of formula-fed infants—84 and 98 kcal/kg, respectively, at 6 months; 87 and 97 kcal/kg, respectively, at 9 months; and 92 and 95 kcal/kg respectively, at 12 months—even though both groups received solid foods beginning at 4 to 6 months. As discussed in Chapter 5, these lower intakes by breastfed infants are governed primarily by infant demand, not by insufficient milk volume. Assessment of Growth of Breastfed Infants Growth charts used to assess infant growth are based on data derived primarily from formula-fed infants (Hamill et al., 1977). The commonly used NCHS infant growth charts are based on information collected by the Fels Research Institute from 867 infants born between 1929 and 1975. In that study, the mode of feeding was known for 75% of the infants. Of those, only 17% were exclusively breastfed and few were breastfed for more than 3 months. Furthermore, the infant formulas used at that time were less similar to human milk (for example, they were higher in total proteins, total fats, and saturated fatty acids) and the infants were more likely to be given solid foods before age 4 months than they are today (Fomon, 1987). Therefore, a number of investigators suggest that NCHS growth charts are inappropriate for breastfed

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Nutrition During Lactation infants (Dewey et al., 1990; Duncan et al., 1984; Hitchcock et al., 1985; Whitehead and Paul, 1984). Similarly, it has been noted (Dewey et al., 1989) that it can be misleading to assess growth of breastfed infants by using current reference data for the increment in weight or length during specified age intervals, such as data presented by Roche and colleagues (1989) based on the Fels Research Institute population. The 5th percentile of these reference data was suggested by Roche et al. as a cutoff to indicate infants at risk of malnutrition. Caution is needed in applying this cutoff because the data are based on predicted values obtained from measurements at 3- rather than 1-month intervals, which obscures some of the short-term variation in infant growth. Thus, more than 5% of all infants, regardless of feeding mode, would be expected to be below the Fels 5th percentile in any given month. Furthermore, Dewey and coworkers (1989) found that the percentage of breastfed infants who fell below the 5th percentile for weight gain was much larger than would be expected, averaging 31% over the six 1-month intervals up to age 6 months and 52% over the six 1-month intervals between ages 6 and 12 months. On average, infants grew less rapidly than the 5th percentile during 4.4 months out of the first 12 months. Although these percentages seem alarming, these were healthy infants who fed on demand and received solid foods beginning at 4 to 6 months. Furthermore, with regard to morbidity, activity levels, or time sleeping during the first year of life, the breastfed infants with growth rates below the 5th percentile were not different from the breastfed infants with faster growth rates (Dewey et al., in press). Therefore, it is highly likely that their growth rates were normal and not a sign of malnutrition. Recently, data have been published on weight and length gain of 419 breastfed and 720 formula-fed infants enrolled in growth studies in Iowa between 1965 and 1987 (Nelson et al., 1989). These infants were measured up to 112 days of age. One shortcoming of the study was that the breastfed infants were allowed up to 240 ml of formula per day, and before 1979, all infants were allowed solid foods beginning at 1 month of age. Therefore, additional data are necessary to construct appropriate growth charts for infants exclusively breastfed for the first 4 to 6 months and extensively breastfed throughout the remainder of the first year. Long-Term Growth Status Few investigators have examined whether the differences in growth rates between breastfed and formula-fed infants during the first year of life are maintained later on in childhood. Birkbeck et al. (1985) measured children at 7 years of age who were either breastfed for at least 12 weeks (N = 283) or formula fed from birth (N = 383). Children who had been breastfed were taller, but the difference was not statistically significant when controlled for

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Nutrition During Lactation Duncan, B., C. Schaefer, B. Sibley, and N.M. Fonseca. 1984. Reduced growth velocity in exclusively breastfed infants. Am. J. Dis. Child. 138:309-313. Duncan, B., R.B. Schifman, J.J. Corrigan, Jr., and C. Schaefer. 1985. Iron and the exclusively breastfed infant from birth to six months. J. Pediatr. Gastroenterol. Nutr. 4:421-425. Dworsky, M., M. Yow, S. Stagno, R.F. Pass, and C. Alford. 1983. Cytomegalovirus infection of breast milk and transmission in infancy. Pediatrics 72:295-299. Ek, J., and E.M. Magnus. 1979. Plasma and red blood cell folate in breastfed infants. Acta Paediatr. Scand. 68:239-243. Ek, J., and E. Magnus. 1982. Plasma and red cell folate values and folate requirements in formula-fed term infants. J. Pediatr. 100:738-744. Elias, M.F., N.A. Nicolson, C. Bora, and J. Johnston. 1986. Sleep/wake patterns of breastfed infants in the first 2 years of life. Pediatrics 77:322-329. Elliot, D.L., L. Goldberg, K.S. Kuehl, and C. Hanna. 1989. Metabolic evaluation of obese and nonobese siblings. J. Pediatr. 114:957-962. FAO (Food and Agriculture Organization). 1988. Requirements of Vitamin A, Iron, Folate, and Vitamin B12. Report of a Joint FAO/WHO Expert Consultation. FAO Food and Nutrition Series No. 23. Food and Agriculture Organization, Rome. 107 pp. Fedrick, J., and P. Adelstein. 1973. Influence of pregnancy spacing on outcome of pregnancy. Br. Med. J. 4:753-756. Fergusson, D.M., A.L. Beautrais, and P.A. Silva. 1982. Breastfeeding and cognitive development in the first seven years of life. Soc. Sci. Med. 16:1705-1708. Ferris, A.G., M.J. Laus, D.W. Hosmer, and V.A. Beal. 1980. The effect of diet on weight gain in infancy. Am. J. Clin. Nutr. 33:2635-2642. Filer, L.J., Jr. 1968. Evaluation and reduction of risks: Problems and applications of individual control measures. Pediatrics 41:308. Fomon, S.J. 1987. Reflections on infant feeding in the 1970s and 1980s. Am. J. Clin. Nutr. Suppl. 46:171-182. Fomon, S.J., R.R. Rogers, E.E. Ziegler, S.E. Nelson, and L.N. Thomas. 1984. Indices of fatness and serum cholesterol at age eight years in relation to feeding and growth during early infancy. Pediatr. Res. 18:1233-1238. Forsum, E., and A. Sadurskis. 1986. Growth, body composition and breast milk intake of Swedish infants during early life. Early Hum. Dev. 14:121-129. Friedman, G., and S.J. Goldberg. 1975. Concurrent and subsequent serum cholesterols of breast- and formula-fed infants. Am. J. Clin. Nutr. 28:42-45. Gambon, R.C., M.J. Lentze, and E. Rossi. 1986. Megaloblastic anemia in one of monozygous twins breastfed by their vegetarian mother. Eur. J. Pediatr. 145:570-571. Garry, P.J., G.M. Owen, E.M. Hooper, and B.A. Gilbert. 1981. Iron absorption from human milk and formula with and without iron supplementation. Pediatr. Res. 15:822-828. Garza, C., J. Stuff, and N. Butte. 1987. Growth of the breastfed infant. Pp. 109-121 in A.S. Goldman, S.A. Atkinson, and L.A. Hanson, eds. Human Lactation 3: The Effects of Human Milk on the Recipient Infant. Plenum Press, New York. Gladen, B.C., W.J. Rogan, P. Hardy, J. Thullen, J. Tingelstad, and M. Tully. 1988. Development after exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene transplacentally and through human milk. J. Pediatr. 113:991-995. Glass, R.I., and B.J. Stoll. 1989. The protective effect of human milk against diarrhea: a review of studies from Bangladesh. Acta Paediatr. Scand. Suppl. 351:131-136.

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Nutrition During Lactation Glass, R.I., A.M. Svennerholm, B.J. Stoll, M.R. Khan, K.M.B. Hossain, M.I. Huq, and J. Holmgren. 1983. Protection against cholera in breastfed children by antibodies in breast milk. N. Engl. J. Med. 308:1389-1392. Gleason, W.A., Jr., and G.A. Kerr. 1989. Questions about quinones in infant nutrition. J. Pediatr. Gastroenterol. Nutr. 8:285-287. Goldman, A.S., and R.M. Goldblum. 1989. Immunologic system in human milk: characteristics and effects. Pp. 135-142 in E. Lebenthal, ed. Textbook of Gastroenterology and Nutrition in Early Infancy, 2nd ed. Raven Press, New York. Goldman, A.S., and R.M. Goldblum, 1990. Human milk: immunologic-nutritional relationships. Ann. N.Y. Acad. Sci. 587:236-245. Goldman, A.S., L.W. Thorpe, R.M. Goldblum, and L.A. Hanson. 1986. Anti-inflammatory properties of human milk. Acta Paediatr. Scand. 75:689-695. Goldman, A.S., R.M. Goldblum, and L.A. Hanson. 1990a. Anti-inflammatory systems in human milk. Adv. Exp. Med. Biol. 262:69-76. Goldman, A.S., R.M. Goldblum, and L.A. Hanson. 1990b. Anti-inflammatory systems in human milk. Pp. 69-76 in A. Bendich, M. Phillips, and R.P. Tengerdy, eds. Antioxidant Nutrients and Immune Functions. Plenum Press, New York. Greer, F.R., J.E. Searcy, R.S. Levin, J.J. Steichen, P.S. Steichen-Asche, and R.C. Tsang. 1982. Bone mineral content and serum 25-hydroxyvitamin D concentrations in breastfed infants with and without supplemental vitamin D: one year follow-up. J. Pediatr. 100:919-922. Gromisch, D.S., R. Lopez, H.S. Cole, and J.M. Cooperman. 1977. Light (phototherapy)-induced riboflavin deficiency in the neonate. J. Pediatr. 90:118-122. Habicht, J.-P., J. DaVanzo, W.P. Butz, and L. Meyers. 1985. The contraceptive role of breastfeeding. Popul. Stud. 39:213-232. Hambidge, K.M., P.A. Walravens, C.E. Casey, R.M. Brown, and C. Bender. 1979. Plasma zinc concentrations of breastfed infants. J. Pediatr. 94:607-608. Hamill, P.V.V., T.A. Drizd, C.L. Johnson, R.B. Reed, and A.F. Roche. 1977. NCHS Growth Curves for Children from Birth to 18 Years: United States. Vital and Health Statistics, Series 11, No. 165. DHHS Publ. No. (PHS) 78-1650. National Center for Health Statistics, Public Health Service, U.S. Department of Health, Education, and Welfare, Hyattsville, Md. 74 pp. Hamosh, M. 1988. Does infant nutrition affect adiposity and cholesterol levels in the adult? J. Pediatr. Gastroenterol. Nutr. 7:10-16. Hamosh, M., and P. Hamosh. 1987. Does nutrition in early life have long-term metabolic effects? Can animal models be used to predict these effects in the human? Pp. 37-55 in A.S. Goldman, S.A. Atkinson, and L.A. Hanson, eds. Human Lactation 3: The Effects of Human Milk on the Recipient Infant. Plenum Press, New York. Hamosh, M., and P. Hamosh. 1990. Obesity. Annales Nestlé 48:59-69. Hansen, A.E. 1937. Serum lipids in eczema and in other pathologic conditions. Am. J. Dis. Child. 53:933-946. Hansen, A.E., E.M. Knott, H.F. Wiese, E. Shaperman, and I. McQuarrie. 1947. Eczema and essential fatty acids. Am. J. Dis. Child. 73:1-18. Hanson, L.A. 1986. The global responsibility towards child health. Aust. Paediatr. J. 22:157-159. Harmatz, P.R., D.G. Hanson, M. Brown, R.E. Kleinman, W.A. Walker, and K.J. Bloch. 1987. Transfer of maternal food proteins in milk. Pp. 289-299 in A.S. Goldman, S.A. Atkinson, and L.A. Hanson, eds. Human Lactation 3: The Effects of Human Milk on the Recipient Infant. Plenum Press, New York.

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Nutrition During Lactation Hatano, S., K. Aihara, Y. Nishi, and T. Usui. 1985. Trace elements (copper, zinc, manganese, and selenium) in plasma and erythrocytes in relation to dietary intake during infancy. J. Pediatr. Gastroenterol. Nutr. 4:87-92. Hattevig, G., B. Kjellman, N. Sigurs, E. Grodzinsky, J. Hed, and B. Bjorksten. 1990. The effect of maternal avoidance of eggs, cow's milk, and fish during location on the development of IgE, IgG, and IgA antibodies in infants. J. Allergy Clin. Immunol. 85:108-115. Herrera, M.G., J.O. Mora, B. de Paredes, and M. Wagner. 1980. Maternal weight/height and the effect of food supplementation during pregnancy and lactation. Pp. 252-263 in H. Aebi and R. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber Publishers, Bern. Higginbottom, M.C., L. Sweetman, and W.L. Nyhan. 1978. A syndrome of methylmalonic aciduria, homocystinuria, megaloblastic anemia and neurologic abnormalities in a vitamin B-12-deficient breastfed infant of a strict vegetarian . N. Engl. J. Med. 299:317-323. Hillman, L.S., and J.G. Haddad. 1974. Human perinatal vitamin D metabolism I: 25-hydroxyvitamin D in maternal and cord blood. J. Pediatr. 84:742-749. Himes, J.H. 1979. Infant feeding practices and obesity. J. Am. Diet. Assoc. 75:122-125. Hino, S. 1989. Milk-borne transmission of HTLV-I as a major route in the endemic cycle. Acta Paediatr. Jpn. 31:428-435. Hitchcock, N.E., and J.F. Coy. 1989. The growth of healthy Australian infants in relation to infant feeding and social group. Med. J. Aust. 150:306-311. Hitchcock, N.E., M. Gracey, and A.I. Gilmour. 1985. The growth of breastfed and artificially fed infants from birth to twelve months. Acta Paediatr. Scand. 74:240-245. Hobcraft, J. 1987. Does family planning save children's lives? Technical background paper prepared for the International Conference on Better Health for Women and Children Through Family Planning, Nairobi, Kenya, October, 1987. Population Council, New York. 77 pp. Hodgson, P.A., R.D. Ellefson, L.R. Elveback, L.E. Harris, R.A. Nelson, and W.H. Weidman. 1976. Comparison of serum cholesterol in children fed high, moderate, or low cholesterol milk diets during neonatal period. Metabolism 25:739-746. Hofvander, Y., U. Hagman, C. Hillervik, and S. Sjolin. 1982. The amount of milk consumed by 1-3 months old breast- or bottle-fed infants. Acta Paediatr. Scand. 71:953-958. Hoogenboezem, T., H.J. Degenhart, S.M.P.F. de Muinck Keizer-Schrama, R. Bouillon, W.F.A. Grose, W.H.L. Hackeng, and H.K.A. Visser. 1989. Vitamin D metabolism in breastfed infants and their mothers. Pediatr. Res. 25:623-628. Hovi, L., R. Hekali, and M.A. Siimes. 1979. Evidence of riboflavin depletion in breastfed newborns and its further acceleration during treatment of hyperbilirubinemia by phototherapy. Acta Paediatr. Scand. 68:567-570. Hunziker, U.A., and R.G. Barr. 1986. Increased carrying reduces infant crying: a randomized controlled trial. Pediatrics 77:641-648. Huttunen, J.K., U.M. Saarinen, E. Kostiainen, and M.A. Siimes. 1983. Fat composition of the infant diet does not influence subsequent serum lipid levels in man. Atherosclerosis 46:87-94. Jadhav, M., J.K.G. Webb, S. Vaishnava, and S.J. Baker. 1962. Vitamin-B 12 deficiency in Indian infants: a clinical syndrome. Lancet 2:903-907. Jakobsson, I., and T. Lindberg. 1978. Cow's milk as a cause of infantile colic in breastfed infants. Lancet 2:437-439.

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Nutrition During Lactation Jakobsson, I., and T. Lindberg. 1983. Cow's milk proteins cause infantile colic in breastfed infants: a double-blind crossover study. Pediatrics 71:268-271. Jason, J.M., P. Nieburg, and J.S. Marks. 1984. Mortality and infectious disease associated with infant-feeding practices in developing countries. Pediatrics 74:702-727. Jensen, A.A. 1983. Chemical contaminants in human milk. Residue Rev. 89:1-128. Kilshaw, P.J., and A.J. Cant. 1984. The passage of maternal dietary proteins into human breast milk. Int. Arch. Allergy Appl. Immunol. 75:8-15. Klein, E.B., T. Byrne, and L.Z. Cooper. 1980. Neonatal rubella in a breastfed infant after postpartum maternal infection. J. Pediatr. 97:774-775. Koldovskỳ, O., A. Bedrick, P. Pollack, R.K. Rao, and W. Thornburg. 1988. Possible physiological role of hormones and hormone-related substances present in milk. Pp. 123-139 in L.A. Hanson, ed. Biology of Human Milk. Nestle Nutrition Workshop Series, Vol. 15. Raven Press, New York. Koletzko, S., P. Sherman, M. Corey, A. Griffiths, and C. Smith. 1989. Role of infant feeding practices in development of Crohn's disease in childhood. Br. Med. J. 298:1617-1618. Kovar, M.G., M.K. Serdula, J.S. Marks, and D.W. Fraser. 1984. Review of the epidemiologic evidence for an association between infant feeding and infant health. Pediatrics 74:615-638. Kramer, M.S. 1981. Do breastfeeding and delayed introduction of solid foods protect against subsequent obesity? J. Pediatr. 98:883-887. Kramer, M.S. 1987. Breastfeeding and child health: methodologic issues in epidemiologic research. Pp. 339-360 in A.S. Goldman, S.A. Atkinson, and L.A. Hanson, eds. Human Lactation 3: The Effects of Human Milk on the Recipient Infant. Plenum Press, New York. Kramer, M.S. 1988. Does breastfeeding help protect against atopic disease? Biology, methodology, and a golden jubilee of controversy. J. Pediatr. 112:181-190. Lakdawala, D.R., and E.M. Widdowson. 1977. Vitamin-D in human milk. Lancet 1:167-168. Lampkin, B.C., and E.F. Saunders. 1969. Nutritional vitamin B12 deficiency in an infant. J. Pediatr. 75:1053-1055. Laug, E.P., F.M. Kunze, and C.S. Prickett. 1951. Occurrence of DDT in human fat and milk. Arch. Ind. Hyg. 3:245-246. Lawrence, R.A. 1989. Breastfeeding: A Guide for the Medical Profession, 3rd ed. C.V. Mosby, St. Louis. 652 pp. Lechtig, A., and R.E. Klein. 1980. Maternal food supplementation and infant health: results of a study in rural areas of Guatemala. Pp. 285-313 in H. Aebi and R. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber, Bern. Lewis, D.S., H.A. Bertrand, E.J. Masoro, H.C. McGill, Jr., K.D. Carey, and C.A. McMahan. 1983. Preweaning nutrition and fat development in baboons. J. Nutr. 113:2253-2259. Lichtenstein, P., B.L. Specker, R.C. Tsang, F. Mimouni, and C. Gormley. 1986. Calcium-regulating hormones and minerals from birth to 18 months of age: a cross-sectional study. I. Effects of sex, race, age, season, and diet on vitamin D status. Pediatrics 77:883-890. Linnemann, C.C., Jr., and S. Goldberg. 1974. HBAg in breast milk. Lancet 2:155. Little, R.E., K.W. Anderson, C.H. Ervin, B. Worthington-Roberts, and S.K. Clarren. 1989. Maternal alcohol use during breastfeeding and infant mental and motor development at one year. N. Engl. J. Med. 321:425-430.

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Nutrition During Lactation Lönnerdal, B., C.L. Keen, and L.S. Hurley. 1981. Iron, copper, zinc, and manganese in milk. Annu. Rev. Nutr. 1:149-174. Lönnerdal, B., C.L. Keen, and L.S. Hurley. 1984. Zinc binding ligands and complexes in zinc metabolism. Adv. Nutr. Res. 6:139-167. Losonsky, G.A., J.M. Fishaut, J. Strussenberg, and P.L. Ogra. 1982. Effect of immunization against rubella on lactation products. II. Maternal-neonatal interactions. J. Infect. Dis. 145:661-666. Lucas, A., P.J. Lucas, and J.D. Baum. 1981a. Differences in the pattern of milk intake between breast and bottle fed infants. Early Hum. Dev. 5:195-199. Lucas, A., S. Boyes, S.R. Bloom, and A. Aynsley-Green. 1981b. Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr. Scand. 70:195-200. Luck, W., and H. Nau. 1985. Nicotine and cotinine concentrations in serum and urine of infants exposed via passive smoking or milk from smoking mothers. J. Pediatr. 107:816-820. Luck, W., and H. Nau. 1987. Nicotine and cotinine concentrations in the milk of smoking mothers: influence of cigarette consumption and diurnal variation. Eur. J. Pediatr. 146:21-26. MacDonald, L.D., R.S. Gibson, and J.E. Miles. 1982. Changes in hair zinc and copper concentrations of breastfed and bottle fed infants during the first six months. Acta Paediatr. Scand. 71:785-789. Mahmood, D.A., and R.G. Feachem. 1987. Feeding and nutritional status among infants in Basrah City, Iraq: a cross-sectional study. Hum. Nutr.: Clin. Nutr. 41C:373-381. Manku, M.S., D.F. Horrobin, N. Morse, V. Kyte, K. Jenkins, S. Wright, and J.L. Burton. 1982. Reduced levels of prostaglandin precursors in the blood of atopic patients: defective delta-6-desaturase function as a biochemical basis for atopy. Prostaglandins, Leukot. Med. 9:615-628. Markestad, T. 1983. Effect of season and vitamin D supplementation on plasma concentrations of 25-hydroxyvitamin D in Norwegian infants. Acta Paediatr. Scand. 72:817-821. Markestad, T., L. Aksnes, P.H. Finne, and D. Aarskog. 1983. vitamin D nutritional status of premature infants supplemented with 500 IU vitamin D2 per day. Acta Paediatr. Scand. 72:517-520. Marmot, M.G., C.M. Page, E. Atkins, and J.W.B. Douglas. 1980. Effect of breastfeeding on plasma cholesterol and weight in young adults. J. Epidemiol. Commun. Health 34:164-167. Mason, K.E. 1979. A conspectus of research on copper metabolism and requirements of man. J. Nutr. 109:1979-2066. Mata, L.J., and J.J. Urrutia. 1971. Intestinal colonization of breastfed children in a rural area of low socioeconomic level. Ann. N.Y. Acad. Sci. 176:93-109. Mata, L.J., J.J. Urrutia, and J.E. Gordon. 1967. Diarrhoeal disease in a cohort of Guatemalan village children observed from birth to age two years. Trop. Geogr. Med. 19:247-257. Mata, L.J., J.J. Urrutia, B. García, R. Fernández, and M. Behar. 1969. Shigella infection in breastfed Guatemalan Indian neonates. Am. J. Dis. Child. 117:142-146. Mayer, E.J., R.F. Hamman, E.C. Gay, D.C. Lezotte, D.A. Savitz, and G.J. Klingensmith. 1988. Reduced risk of IDDM among breastfed children: the Colorado IDDM Registry. Diabetes 37:1625-1632. McPhee, A.J., G.P. Davidson, M. Leahy, and T. Beare. 1988. Vitamin B12 deficiency in a breastfed infant. Arch. Dis. Child. 63:921-923.

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