5
Milk Volume

The nutritional demands imposed by breastfeeding depend primarily on the absolute quantities of nutrients transferred from the mother to the infant through the milk. Thus, in considering recommendations for maternal nutrition during lactation, it is essential to carefully examine both the volume and composition of human milk. Milk volume is the focus of this chapter; Chapter 6 covers composition.

The subcommittee addressed the following questions in its review of milk volume:

  • Is the volume or energy content of human milk compromised when intake of energy or other nutrients is restricted during lactation? Do maternal body fat or other nutrient stores modify this relationship?

  • Does energy supplementation or increased intake of protein or fluid increase milk volume?

  • What other factors must be considered when examining the effects of maternal nutrition on milk volume?

These questions can be examined only in the context of a clear understanding of the regulation of milk production in humans. For this reason, this chapter includes consideration of the physiologic control of lactation and of the infant's role in this process, in addition to maternal factors such as age, parity, stress, substance use, and nutrition.



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Nutrition During Lactation 5 Milk Volume The nutritional demands imposed by breastfeeding depend primarily on the absolute quantities of nutrients transferred from the mother to the infant through the milk. Thus, in considering recommendations for maternal nutrition during lactation, it is essential to carefully examine both the volume and composition of human milk. Milk volume is the focus of this chapter; Chapter 6 covers composition. The subcommittee addressed the following questions in its review of milk volume: Is the volume or energy content of human milk compromised when intake of energy or other nutrients is restricted during lactation? Do maternal body fat or other nutrient stores modify this relationship? Does energy supplementation or increased intake of protein or fluid increase milk volume? What other factors must be considered when examining the effects of maternal nutrition on milk volume? These questions can be examined only in the context of a clear understanding of the regulation of milk production in humans. For this reason, this chapter includes consideration of the physiologic control of lactation and of the infant's role in this process, in addition to maternal factors such as age, parity, stress, substance use, and nutrition.

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Nutrition During Lactation MEASUREMENT OF MILK VOLUME A key element defining lactation performance is the total amount of milk produced. The amount of milk transferred to the infant affects the infant's nutrient intake and the mother's nutrient requirements. In this report, the subcommittee distinguishes between milk intake by the infant (also referred to as milk volume) and milk production by the mother. Ordinarily, production is measured as intake, but it may exceed intake if extra milk is removed from the breast and is not consumed by the infant or the infant regurgitates milk. The most widely accepted method for measuring milk intake is test weighing, a procedure in which the infant is weighed before and after each feeding, preferably using a balance scale accurate to ±1 g. In this method, milk intake is usually underestimated by approximately 1 to 5% (Brown et al., 1982; Woolridge et al., 1985) because of evaporative water loss from the infant between weighings. The procedure is potentially disruptive to the nursing patterns of the mother and infant, especially if nursing is very frequent or the infant nurses occasionally during the night while sleeping with the mother. Under conditions typical of breastfeeding mothers in the United States, the method is generally well accepted (Dewey and Heinig, 1987). Intake is usually reported in grams because they are the unit of measurement used in test weighing; the density of human milk is approximately 1.03 g/ml (Neville et al., 1988; Woolridge et al., 1985). Newer techniques for measuring breast milk intake based on the use of stable isotopes have been developed, but few data obtained with them have been published (Butte et al., 1988; Coward et al., 1982; Fjeld et al., 1988; Wong et al., 1990). Maternal milk production can be measured mechanically by extracting all the milk or by using a combination of test weighing and extraction of residual milk. NORMAL RANGE OF MILK INTAKE AND PRODUCTION There is a very wide range in milk intake among healthy, exclusively breastfed infants. Figure 5-1 illustrates variability in infant milk intake during established lactation. In industrialized countries, milk intakes average approximately 750 to 800 g/day in the first 4 to 5 months, but range from approximately 450 to 1,200 g/day (Butte et al., 1984b; Chandra, 1981; Dewey and Lönnerdal, 1983; Hofvander et al., 1982; Lönnerdal et al., 1976; Neville et al., 1988; Pao et al., 1980; Picciano et al., 1981; Rattigan et al., 1981; Wallgren, 1944/1945; Whitehead and Paul, 1981). Recent data from developing countries indicate a similar mean level of intake when a rigorous methodology for measuring milk volume is used (Brown et al., 1986b; Prentice et al., 1986) (see Figure 5-2). Milk intake after the first 4 to 5 months varies even more widely. In U.S. infants who were breastfed for at least 12 months and were given solid foods beginning at 4 to 7 months, milk intake averaged 769 g/day (range, 335 to

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Nutrition During Lactation FIGURE 5-1 Milk intakes during established lactation from studies meeting defined criteria, from Neville et al. (1988) with permission. The lines show the smoothed mean ± standard deviation, from Neville et al. (1988). The points represent average intakes from studies that obtained data from test weighing, validated exclusive breastfeeding, studied three or more subjects, and reported milk transfer by monthly intervals. FIGURE 5-2 Average intake of human milk by infants at age 3 months in industrialized and developing countries. Data were compiled from studies later than the year 1975. Adapted from Prentice et al. (1986) with permission.

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Nutrition During Lactation 1,144 g/day) at 6 months (N = 56), 637 g/day (range, 205 to 1,185 g/day) at 9 months (N = 46), and 445 g/day (range, 27 to 1,154 g/day) at 12 months (N = 40) (Dewey et al., in press). Several studies indicate that potential milk production in humans is considerably higher than the average intake by single infants. Kaucher and colleagues (1945) measured maximum milk output with intrusive and tedious mechanical methods to extract all the mother's milk and reported that production averaged almost 1,200 g/day at 6 to 10 days post partum. This level is much higher than the 500 to 700 g/day consumed by breastfed infants at the same age (Casey et al., 1986; Saint et al., 1984). In two separate studies, milk production increased by 15 to 40% when a breast pump was used to remove additional milk after feedings (Dewey and Lönnerdal, 1986; Neville and Oliva-Rasbach, 1987). Mothers who exclusively breastfeed twins or triplets can produce 2,000 to 3,000 g/day, although this involves nursing an average of 15 or more times per day (Saint et al., 1986). Women who express surplus milk for a milk bank have been shown to produce as much as 3,000 g/day (Macy et al., 1930). BREAST DEVELOPMENT AND PHYSIOLOGY The data discussed above illustrate that lactation is a physiologic process with a great deal of plasticity—that is, milk production can be regulated up or down, depending on the degree of stimulation to the mammary gland. The processes leading to a woman's ability to secrete milk start long before lactation commences. Mammary development begins in early fetal life and extends through puberty; it resumes early in pregnancy. The process is influenced by several hormones, including estrogens, progesterone, and lactogenic hormones (Neville and Neifert, 1983). Mammary gland enlargement is especially pronounced during the first half of pregnancy, when lobuloalveolar growth is accompanied by differentiation of the epithelial cells. Both prolactin and placental lactogen may initiate this enlargement, although either one alone may provide sufficient stimulus for mammary development. Insufficient development before or during pregnancy may contribute to lactation failure (Neifert and Seacat, 1986). The prevalence of this problem has not been studied but is likely to be very low. Lactogenesis, defined as ''the onset of copious milk secretion around parturition" (Neville and Neifert, 1983, p. 108), is believed to be triggered by the decrease in progesterone following parturition. Incomplete delivery of the placenta has been shown to delay lactogenesis, presumably because it is accompanied by continued high levels of progesterone (Neifert et al., 1981). Prolactin is believed to be essential for normal lactogenesis, but the mechanism or mechanisms for its influence are not clearly understood. Once milk production has begun, the hormonal mechanisms maintaining milk secretion are believed to depend primarily on the actions of prolactin and oxytocin.

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Nutrition During Lactation Prolactin is generally understood to promote milk synthesis and secretion into the alveolar spaces. Its metabolic effects include promotion of fat synthesis in mammary tissue, increased fat mobilization at other body sites, enhancement of casein synthesis and casein messenger RNA formation in the rat and rabbit, and stimulation of milk α-lactalbumin and lactose levels in cows (Horrobin, 1979). Prolactin levels are influenced by the amount and frequency of suckling, but vary considerably among women producing comparable volumes of milk (Martin, 1983; Noel et al., 1974; Strode et al., 1986; Tyson et al., 1978). Oxytocin is secreted by the maternal pituitary in response to suckling and in turn stimulates contraction of the myoepithelial cells, leading to milk ejection. This milk-ejection reflex, or let-down, moves milk from the storage alveoli to the lacteal sinuses, allowing the milk to be easily removed by the infant (Woolridge and Baum, 1988). Milk production may also be governed by local negative feedback within each breast, referred to by Wilde et al. (1988) as "autocrine" control. These investigators reported that a constituent of milk whey protein inhibits milk secretion in a dose-dependent manner in goats. As milk builds up in the mammary gland between feedings, the concentration of this inhibitor presumably increases and thus retards and eventually stops milk production. Removal of milk eliminates the inhibitory effect and milk production resumes or increases. This inhibitory mechanism could explain why two breasts of the same woman with different milk removal rates can produce very different quantities of milk. Breast engorgement and the resulting increased pressure in and distension of the mammary gland also lead to decreased milk production. Studies in animals suggest that when milking ceases, distension of the alveoli caused by pooling of the milk brings about a decrease in milk secretion within 6 hours (Neville and Neifert, 1983). INFANT FACTORS INFLUENCING MILK PRODUCTION AND TRANSFER Management of lactation during the first few weeks is critical to the establishment of an adequate milk supply. Successful lactation depends on several factors, such as proper positioning of the infant at the breast, precautions to avoid sore nipples, frequent feedings, avoidance of formula feeding, and timing of feedings to coincide with the infant's desire to suck. These factors are discussed in detail in breastfeeding guides (e.g., Goldfarb and Tibbetts, 1989, Lawrence, 1989). For the purposes of this report, the subcommittee restricted its discussion to infant characteristics that may influence milk volume, such as birth weight, sucking strength, gestational age at delivery, and illness, and to maternal characteristics, such as age, parity, stress, substance use, and nutritional status. These characteristics appear to be those that are most likely to affect

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Nutrition During Lactation milk volume if they influence the frequency, intensity, or duration of sucking by the infant. Nursing Frequency During the early postpartum period, when the milk supply is being established (Lawrence, 1985), there is a positive association between nursing frequency and milk production (de Carvalho et al., 1983, 1985; Hopkinson et al., 1988; Salariya et al., 1978). In a study of 32 mothers of preterm infants, optimal milk production was achieved when milk was pumped five or more times per day during the first month post partum (Hopkinson et al., 1988). Among women breastfeeding full-term infants, mean nursing frequency of 10 ± 3 times per day during the first 2 weeks post partum was associated with adequate milk production (de Carvalho et al., 1982). Although there is considerable interindividual variability in infants' need to suck, nursing on demand (at least eight times per day in the early postpartum period) is recommended to provide the necessary degree of hormonal stimulation to the mammary gland. Once lactation is established, cross-sectional studies of well-nourished, exclusively breastfeeding women nursing 4 to 16 times per day indicate that there is little, if any, relationship between nursing frequency and infant milk intake (Butte et al., 1984a; de Carvalho et al., 1982; Dewey et al., 1986) or between basal serum prolactin levels and milk volume (Lunn et al., 1984; Noel et al., 1974; Strode et al., 1986; Tyson et al., 1978). These findings do not imply, however, that the milk output of individual mothers cannot be altered by changing nursing frequency. At least one report illustrates that limiting the number of feedings can reduce milk production (Egli et al., 1961), and during gradual weaning, it is obvious that mothers are able to decrease their infant's intake of human milk by nursing less often. Thus, although some infants are capable of consuming adequate amounts of milk by feeding only four to five times a day, women who are concerned about the adequacy of their milk supply are well advised to nurse more often. Birth Weight Prentice et al. (1986) and Dewey et al. (1986) observed an association between infant birth weight and volume of milk intake. This appears to be related to the greater sucking strength, frequency, or feeding duration among larger infants—all of which could increase milk volume. Pollitt and colleagues (1978) demonstrated that infant weight at 2 days and at 1 month of age was strongly correlated with sucking strength, which appeared to be responsible for the large variations in intake per feeding among formula-fed infants. Among breastfed infants, de Carvalho et al. (1982) found a positive relationship between

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Nutrition During Lactation infant birth weight and frequency and duration of feeding during the first 14 days post partum. Gestational Age at Delivery The interaction of gestational age and birth weight may have a stronger influence on milk intake than does either one alone, because preterm infants (especially those born at <34 weeks of gestation) may be too weak or immature to suck effectively. Studies of the volume of milk produced by mothers of preterm infants are complicated by the fact that many mothers must pump milk for several days or weeks before the infant can suck directly from the breast. The degree of maternal motivation to breastfeed plays a large role in the success of this phase. Self-Regulation Self-regulation of milk intake was studied among 18 exclusively breastfed infants of mothers who increased their milk supply by expressing extra milk daily for 2 weeks (Dewey and Lönnerdal, 1986). On average, these infants took in more milk immediately following this 2-week period, but about half of them returned to near baseline levels of milk intake after another 1 to 2 weeks. Net change in milk intake at the end of the study was greater among heavier infants and was not associated with baseline milk volume. This indicates that milk intake was influenced more by infant demand than by maternal capacity for milk production. In a subsequent study, Dewey et al. (in press) showed that residual milk volume (the difference between the amount that can be extracted by pump compared with usual infant intake) averages about 100 g/day, even among mothers whose infants consume relatively low amounts of milk (<650 g/day). Likewise, Woolridge and Baum (1988) demonstrated that when 29 mothers randomly selected the breast from which to feed the baby first, intake from the second breast was only about 60% of the amount taken from the first breast. These results illustrate that infants ordinarily do not take all the available milk and therefore govern their own intake to a considerable extent. Self-regulation of milk intake by infants was also demonstrated by Stuff and Nichols (1989), who studied 45 breastfed infants before and after they began consuming solid foods. Energy intake per kilogram of body weight of these infants during exclusive breastfeeding was considerably lower than the Recommended Dietary Allowance (NRC, 1989) and did not increase after solid foods were introduced. Instead, the infants responded to solid foods by reducing breast milk intake, thereby maintaining constant levels of energy intake. Similarly, Nommsen and colleagues (1989) found that solid foods displaced energy intake from human milk in 6-month-old infants even though they were breastfed on demand.

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Nutrition During Lactation Factors influencing the infant's demand for milk have not been studied thoroughly. When the milk supply is ample, the infant's milk intake is positively associated with infant weight. Because the mean weight of boys is heavier than that of girls of the same age, intake is also associated with the sex of the infant. Illness of the infant may reduce appetite and therefore milk intake. In The Gambia, Prentice et al. (1986) observed that decreases in milk intake by infants during the wet season (a period of food scarcity) were usually associated with gastrointestinal or respiratory infections. As described later in this chapter, maternal supplementation did not prevent the seasonal decline in milk volume, indicating that this pattern was probably not due to maternal nutritional limitations but to either altered feeding practices or illness-induced anorexia among the infants. From the Gambian data, it is difficult to separate the influence of these factors. In contrast, Brown et al. (in press) found that milk intake among breastfed infants in Peru remained constant, whereas intake of other foods was reduced during illness. MATERNAL FACTORS Age and Parity Maternal variables such as age and parity have little or no relationship to milk production in most populations (as measured by the infant's intake of human milk). There have been few studies of the volume of milk produced by adolescent mothers. In one study, Lipsman et al. (1985) found that milk intake appeared adequate (based on measures of infant growth) for 22 of the 25 infants of well-nourished, lactating teenagers. Among women aged 21 to 37, no association was observed between maternal age and infant milk intake (Butte et al., 1984b; Dewey et al., 1986), despite Hytten's (1954) concerns that milk yield may decrease because of "disuse atrophy" after age 24. There is some evidence that milk production on the fourth day post partum is higher among multiparous than it is among primiparous women (Zuppa et al., 1988); however, once lactation is established, there is no statistically significant association between parity and infant milk intake in well-nourished populations (Butte et al., 1984a; Dewey et al., 1986; Rattigan et al., 1981). In The Gambia, infants of mothers who had borne 10 or more children had low milk intakes (Prentice, 1986), but this level of parity is rarely seen in industrialized countries.

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Nutrition During Lactation Stress and Acute Illness Maternal anxiety and stress, which may be exacerbated by poor lactation management, are believed to influence milk production by inhibiting the milk-ejection reflex. This reflex usually operates well in women who are relaxed and confident of their ability to breastfeed. In tense women, however, the reflex may be impaired. Limited documentation of the effects of stress or relaxation on let-down is provided by Newton and Newton (1948, 1950) and Feher et al. (1989), but further studies are needed to explore the effects of various types of maternal stress, especially chronic anxiety and tension, on milk production. There are also few data concerning the potential influence of common short-term maternal illnesses on breastfeeding. It is known, however, that mothers can and should continue to nurse when they have mastitis (Lawrence, 1989). Substance Use Maternal behavior such as cigarette smoking and alcohol consumption may influence both milk production and milk composition. Potential consequences to the infant are discussed in Chapter 7; this section is restricted to effects on milk volume. Cigarette Smoking Smoking may reduce milk volume through an inhibitory effect on prolactin or oxytocin levels. Studies in rats have shown decreased release of prolactin in response to suckling and decreases in both milk output and pup growth upon exposure to nicotine or tobacco fumes (Blake and Sawyer, 1972; Ferry et al., 1974; Hamosh et al., 1979; Terkel et al., 1973). Smoking is also known to stimulate release of adrenaline, which in turn can inhibit oxytocin release (Cross, 1955). Studies in humans show a consistent association between smoking and early weaning (Lyon, 1983; Matheson and Rivrud, 1989; Whichelow and King, 1979), but milk volume was not measured directly in those studies. Since smoking is usually more common among women of lower socioeconomic status and educational level than among more advantaged women, it is possible that the smoking itself is not the factor that contributes to early weaning. However, both Lyon (1983) and Matheson and Rivrud (1989) reported a lower prevalence of breastfeeding at 6 to 12 weeks post partum among smokers compared with nonsmokers even within the same socioeconomic group. Furthermore, Matheson and Rivrud (1989) found a greater incidence of colic among infants of breastfeeding mothers who smoked. Andersen and coworkers (1982) demonstrated that women who smoked 15 or more cigarettes per day had 30 to 50% lower basal prolactin levels on days 1 and 21 post partum than did nonsmokers, although the suckling-induced rise in prolactin was not different between groups. Oxytocin levels were not

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Nutrition During Lactation influenced by smoking. Since the infants of smokers tend to have average birth weights that are approximately 200 g lower than those of the infants of nonsmokers (IOM, 1990) (which is the case in the study by Andersen et al. [1982]), and since lower birth weight may decrease infant demand for milk and thus both prolactin levels and milk volume, it is difficult to separate cause and effect in these studies. Nonetheless, the evidence from investigations in both animals and humans strongly suggests that smoking has an adverse effect on milk volume. Alcohol Consumption The influence of alcohol consumption on milk production is less straightforward than that of smoking. It has long been maintained that small amounts of alcoholic beverages can help breastfeeding mothers to relax and thus foster effective functioning of the milk-ejection reflex (Lawrence, 1989). On the other hand, ethanol is a known inhibitor of oxytocin release (Fuchs and Wagner, 1963). Two studies have demonstrated that the milk-ejection reflex can be at least partially blocked by maternal alcohol intake and that this effect is dose dependent (Cobo, 1973; Wagner and Fuchs, 1968). Wagner and Fuchs (1968) measured uterine contractions during suckling as an indicator of oxytocin release. At ethanol doses of 0.5 to 0.8 g/kg of maternal body weight, uterine activity was 62% of normal; at 0.9 to 1.1 g/kg, it was 32% of normal. Cobo (1973) measured the milk-ejection reflex by recording intraductal pressure in the mammary gland. He observed no effect of ethanol intake at doses below 0.5 g/kg; but the milk-ejection response was inhibited by 18.2, 63.2, and 80.4% at doses of 0.5 to 0.99, 1.0 to 1.49, and 1.5 to 1.99 g/kg, respectively. At 0.5 to 0.99 g/kg, this effect was not statistically significant, but at 1.0 to 1.49 g/kg, the milk-ejection reflex was completely blocked in 6 of the 14 subjects. The effect of alcohol on this reflex was not apparent when oxytocin was injected, indicating that the inhibition involved the release rather than the activity of oxytocin. For an average woman weighing 60 kg (132 lb), an ethanol dose of 0.5 g/kg of body weight corresponds to approximately 2 to 2.5 oz of liquor, 8 oz of wine, or 2 cans of beer. Thus, these studies indicate that the adverse effects of alcohol consumption on the milk-ejection reflex are apparent only at relatively high intakes. Oral Contraceptive Agents The impact of oral contraceptive agents on lactation performance has been the subject of numerous studies (see reviews by Koetsawang [1987] and Lönnerdal [1986]). In the United States, 12.6% of lactating women who participated in the 1982 National Survey of Family Growth reported that they

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Nutrition During Lactation used oral contraceptives; this proportion was much higher among blacks (26.9%) than among whites (11.7%) (Ford and Labbok, 1987). In providing guidance to women planning to use oral contraceptives, it is important to consider the composition and dosage of the pill and the intended duration of exclusive breastfeeding. In most studies conducted on the subject, the use of combined estrogen and progestin pills has been associated with reduced milk volume and duration of breastfeeding (Koetsawang, 1987; Lönnerdal, 1986). A recent multi-center, randomized double-blind trial in Hungary and Thailand demonstrated that even low-dose combined oral contraceptives (150 µg of levonorgestrel and 30 µg of ethinyl estradiol) have this effect: between 6 and 24 weeks post partum, the rate of milk volume decrease in women taking these pills was about twice the rate observed in control women (WHO Task Force on Oral Contraceptives, 1988). The nitrogen content of milk also was lower in those taking the combined pills, but there was no consistent effect on lactose or fat concentrations. In contrast, no effect on milk volume or composition has been associated with progestin-only pills (Koestsawang, 1987; Lönnerdal, 1986; WHO Task Force on Oral Contraceptives, 1988). Although progesterone is known to inhibit lactogenesis, once lactation has been established it has no known inhibitory effect on milk production, possibly because progesterone binding sites are apparently not present in lactating tissues (Neville and Neifert, 1983). Further, there are substantial chemical differences between natural progesterone and synthetic progestins. Progestin-only pills have been found to be slightly less effective contraceptives than combined pills in studies of nonlactating women (Winikoff et al., 1988), but it is not known if this difference in effectiveness applies to lactating women as well. Progestin-only pills are also associated with altered menstrual cycles in nonlactating women, but the prevalence of this dysfunction is unknown in lactating women, who are likely to have a longer period of postpartum amenorrhea. For lactating women who wish to use oral contraceptives and maintain milk production, the World Health Organization states that progestin-only pills are the preferred choice (WHO Task Force on Oral Contraceptives, 1988). Maternal Nutrition and Energy Balance This section begins with consideration of maternal energy balance during lactation; this is followed by discussions of protein and fluid intakes. Studies on the influence of other nutrients have dealt primarily with milk composition, rather than volume, and are discussed in Chapter 6. In its review, the subcommittee gave greatest weight to evidence with the greatest relevance to making causal inferences to human populations. Causal relationships can be most definitively demonstrated in intervention studies with

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Nutrition During Lactation FIGURE 5-4 Relationship between increase in maternal fluid intake for 3 days and percent change in milk production. From Dusdieker et al. (1985) with permission. days among 21 lactating women in the United States and found no change in milk volume and no correlation between fluid intake and milk volume (Figure 5-4). In an earlier study, Illingworth and Kilpatrick (1953) asked 104 lactating women to drink at least 2,880 ml of liquid per day (high-fluids group) and 106 control women to drink as much as desired. In the first 9 days post partum, actual fluid intake averaged approximately 3,200 ml/day in the high-fluids group and about 2,100 ml/day in the control group. Neither infant growth in the first month nor duration of breastfeeding differed between groups. Milk intake at a test feed on the eighth day post partum tended to be lower in the high-fluids group. The authors thus cautioned against drinking fluids in excess of natural thirst inclination. However, thirst may sometimes function too slowly to prevention dehydration among women with high fluid losses resulting from exercise or high ambient temperature (experienced by many women without air conditioning in the summer). Thus, careful attention to adequacy of fluid intake is warranted in such situations, but under most conditions there appears to be no justification for emphasizing high fluid intake as a way to improve milk production.

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Nutrition During Lactation CONCLUSIONS Studies conducted in the United States, other developed countries, and developing countries indicate that the average level of milk production is approximately 750 to 800 ml/day in women with widely varying dietary intakes and with varying nutritional status, as measured by weight and skinfold thickness. Potential production of milk by lactating women appears to be considerably higher than actual intakes by single infants, as indicated by the high milk volumes produced by women nursing twins or even triplets. Factors other than maternal nutrition affect milk volume and should be considered in any evaluation of lactation performance. Maternal age and parity appear to have little, if any, influence, but variables such as maternal stress and the nursing behavior of both mother and infant are potentially important. Maternal nutritional status, as measured by anthropometric indices prenatally or post partum, is not related to milk volume in studies conducted in industrialized countries such as the United States. In other words, infants of thin women generally consume as much breast milk as infants of normal-weight or overweight women. In less developed countries, the results are mixed; some studies show a positive association between maternal body composition (adiposity) and milk volume. Average milk volumes of lactating women are comparable in industrialized and developing countries, despite substantial differences in energy and nutrient intake. This suggests that maternal energy intake is not strongly associated with milk volume. Studies in animals indicate that there may be a threshold below which energy intake is insufficient to support normal milk production; it is likely that most studies in humans have been conducted in groups with intakes above this hypothesized threshold. Food supplementation of lactating women in areas where malnutrition is prevalent has generally had little, if any, impact on milk volume. However, such supplementation may improve maternal health and therefore is more likely to benefit the mother than the infant, except in cases in which milk composition is affected (see Chapter 6). It is customary to lose weight gradually during lactation. In the United States, lactating women tend to be heavier than their ideal body weight immediately post partum, and some successfully lose up to 2 kg (˜4.5 lb) per month with no apparent deleterious effects on milk production. Women who exercise regularly appear to produce an adequate volume of milk. The influence of maternal intake of specific nutrients on milk volume has not been investigated thoroughly. Early studies in developing countries show an association of protein intake with milk volume, but limitations of the study designs prohibit definitive conclusions.

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Nutrition During Lactation Adequate fluid intake during lactation is desirable to maintain maternal health, but supplemental fluids consumed in excess of natural thirst have no effect on milk volume. RECOMMENDATIONS FOR CLINICAL PRACTICE Advise women that the average rate of weight loss post partum (0.5 to 1.0 kg, or 1 to 2 lb, per month after the first month) appears to be consistent with maintaining adequate milk volume. If a lactating woman is overweight, a weight loss of up to 2 kg (˜4.5 lb) per month is unlikely to adversely affect milk volume, but such women should be alert for any indications that the infant's appetite is not being satisfied. Rapid weight loss (>2 kg/month after the first month post partum) is not advisable for breastfeeding women. The level of physical activity needs to be considered when advising women about adequacy of energy intake during lactation. Intakes below 1,500 kcal/day are not recommended at any time during lactation, although brief fasts (lasting less than 1 day) are unlikely to decrease milk volume. Liquid diets and weight loss medications are not recommended. Since the impact of curtailing maternal energy intake during the first 2 to 3 weeks post partum is unknown, dieting during this period is not recommended. If alcohol is used, advise the lactating woman to limit her intake to no more than 0.5 g of alcohol per kg of maternal body weight per day. Intake over this level may impair the milk ejection reflex. For a 60-kg (132-lb) woman, 0.5 g of alcohol per kg of body weight corresponds to approximately 2 to 2.5 oz of liquor, 8 oz of table wine, or 2 cans of beer. Actively discourage cigarette smoking among lactating women, not only because it may reduce milk volume but because of its other harmful effects on the mother and her infant. Discourage intake of large quantities of coffee, other caffeine-containing beverages and medications, and decaffeinated coffee. Because the early management of lactation has a strong influence on the establishment of an adequate milk supply, breastfeeding guidance should be provided prenatally and continued in the hospital after delivery and during the early postpartum period. Promote breastfeeding practices that are responsive to the infant's natural appetite. In the first few weeks, infants should nurse at least 8 times per day, and some may nurse as often as 15 or more times per day. After the first month, infants fed on demand usually nurse 5 to 12 times per day.

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Nutrition During Lactation REFERENCES Andersen, A.N., C. Lund-Andersen, J.F. Larsen, N.J. Christensen, J.J. Legros, F. Louis, H. Angelo, and J. Molin. 1982. Suppressed prolactin but normal neurophysin levels in cigarette smoking breastfeeding women. Clin. Endocrinol. 17:363-368. Blackburn, M.W., and D.H. Calloway. 1976. Energy expenditure and consumption of mature, pregnant and lactating women. J. Am. Diet. Assoc. 69:29-37. Blackburn, M.W., and D.H. Calloway. 1985. Heart rate and energy expenditure of pregnant and lactating women. Am. J. Clin. Nutr. 42:1161-1169. Blake, C.A., and C.H. Sawyer. 1972. Nicotine blocks the suckling-induced rise in circulating prolactin in lactating rats. Science 177:619-621. Brown, K.H., R.E. Black, A.D. Robertson, N.A. Akhtar, G. Ahmed, and S. Becker. 1982. Clinical and field studies of human lactation: methodological considerations. Am. J. Clin. Nutr. 35:745-756. Brown, K.H., A.D. Robertson, and N.A. Akhtar. 1986a. Lactational capacity of marginally nourished mothers: infants' milk nutrient consumption and patterns of growth. Pediatrics 78:920-927. 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. Brown, K.H., R.Y. Stallings, H. Creed de Kanashiro, G. Lopez de Romaña; and R.E. Black. In press. Effects of common illnesses on infants' energy intakes from breast milk and other foods during longitudinal community-based studies in Huascar (Lima), Peru. Am. J. Clin. Nutr. 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., and C. Garza. 1985. Energy and protein intakes of exclusively breastfed infants during the first four months of life. Pp. 63-83 in M. Gracey and F. Falkner, eds. Nutritional Needs and Assessment of Normal Growth. Raven Press, New York. Butte, N.F., C. Garza, J.E. Stuff, E.O. Smith, and B.L. Nichols. 1984a. Effect of maternal diet and body composition on lactational performance. Am. J. Clin. Nutr. 39:296-306. Butte, N.F., C. Garza, E.O. Smith, and B.L. Nichols. 1984b. Human milk intake and growth in exclusively breastfed infants. J. Pediatr. 104:187-195. Butte, N.F., W.W. Wong, B.W. Patterson, C. Garza, and P.D. Klein. 1988. Human-milk intake measured by administration of deuterium oxide to the mother: a comparison with the test-weighing technique. Am. J. Clin. Nutr. 47:815-821. 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. Chandra, R.K. 1981. Breastfeeding, growth and morbidity. Nutr. Res. 1:25-31. Chávez, A., and C. Martinez. 1980. Effects of maternal undernutrition and dietary supplementation on milk production. Pp. 274-284 in H. Aebi and R. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber, Bern. Cobo, E. 1973. Effect of different doses of ethanol on the milk-ejecting reflex in lactating women. Am. J. Obstet. Gynecol. 115:817-821. Coward, W.A., T.J. Cole, H. Guber, S.B. Roberts, and I. Fleet. 1982. Water turnover and measurement of milk intake. Pflugers. Arch. 393:344-347.

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Nutrition During Lactation Fuchs, A., and G. Wagner. 1963. The effect of ethyl alcohol on the release of oxytocin in rabbits. Acta Endocrinol. 44:593-605. Girija, A., P. Geervani, and R.G. Rao. 1984. Influence of dietary supplementation during lactation on lactation performance. J. Trop. Pediatr. 30:140-144. Goldfarb, J., and E. Tibbetts. 1989. Breastfeeding Handbook: A Practical Reference for Physicians, Nurses, and Other Health Professionals. Enslow, Hillside, N.J. 256 pp. Gopalan, C. 1958. Studies on lactation in poor Indian communities. J. Trop. Pediatr. 4:87-97. Gunther, M. 1968. Diet and milk secretion in women. Proc. Nutr. Soc. 27:77-82. Hamosh, M., M.R. Simon, and P. Hamosh. 1979. Effect of nicotine on the development of fetal and suckling rats. Biol. Neonate 35:290-297. Hofvander, Y., U. Hagman, C. Hillervik, and S. Sjölin. 1982. The amount of milk consumed by 1-3 months old breast- or bottle-fed infants. Acta Paediatr. Scand. 71:953-958. Hopkinson, J.M., R.J. Schanler, and C. Garza. 1988. Milk production by mothers of premature infants. Pediatrics 81:815-820. Horrobin, D. 1979. Prolactin. Annual Research Reviews, X. Vol. 7. Eden Press, St. Albans, Vt. 126 pp. Hytten, F.E. 1954. Clinical and chemical studies in human lactation. VIII. Relationship of the age, physique, and nutritional status of the mother to the yield and composition of her milk. Br. Med. J. 2:844-845. Hytten, F.E., and A.M. Thomson. 1961. Nutrition of the lactating woman. Pp. 3-46 in Kon, S.K., and A.T. Cowie, eds. Milk: the Mammary Gland and Its Secretion. Academic Press, New York. Illingworth, R.S., and B. Kilpatrick. 1953. Lactation and fluid intake. Lancet 2:1175-1177. Illingworth, P.J., R.T. Jung, P.W. Howie, P. Leslie, and T.E. Isles. 1986. Diminution in energy expenditure during lactation. Br. Med. J. 292:437-441. IOM (Institute of Medicine). 1990. Nutrition During Pregnancy: Weight Gain and Nutrient Supplements. Report of the Subcommittee on Nutritional Status and Weight Gain During Pregnancy, Subcommittee on Dietary Intake and Nutrient Supplements During Pregnancy, Committee on Nutritional Status During Pregnancy and Lactation, Food and Nutrition Board. National Academy Press, Washington, D.C. 468 pp. Janas, L.M., and M.F. Picciano. 1986. Quantities of amino acids ingested by human milk-fed infants. J. Pediatr. 109:802-807. Janas, L.M., M.F. Picciano, and T.F. Hatch. 1985. Indices of protein metabolism in term infants fed human milk, whey-predominant formula, or cow's milk formula. Pediatrics 75:775-784. Jansen, G.R., and W.C. Monte. 1977. Amino acid fortification of bread fed at varying levels during gestation and lactation in rats. J. Nutr. 107:300-309. Jansen, A.A.J., R. Luyken, S.H. Malcom, and J.J.L. Willems. 1960. Quantity and composition of breast milk in Baik Island (Neth. New Quinea). Trop. Geog. Med. 2:138-144. Kaucher, M., E.Z. Moyer, A.J. Richards, H.H. Williams, A.L. Wertz, and I.G. Macy. 1945. Human milk studies. XX. The diet of lactating women and the collection and preparation of food and human milk for analysis. Am. J. Dis. Child. 70:142-147. Khan, L., and B. Belavady. 1973. Basal metabolism in pregnant and nursing women and children. Indian J. Med. Res. 61:1853-1860.

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Nutrition During Lactation Kliewer, R.L., and K.M. Rasmussen. 1987. Malnutrition during the reproductive cycle: effects on galactopoietic hormones and lactational performance in the rat. Am. J. Clin. Nutr. 46:926-935. Koetsawang, S. 1987. The effects of contraceptive methods on the quality and quantity of breast milk. Int. J. Gynaecol. Obstet. 25 Suppl.:115-127. Lawrence, R.A. 1985. Breastfeeding: A Guide for the Medical Profession, 2nd ed. C.V. Mosby, St. Louis. 601 pp. Lawrence, R.A. 1989. Breastfeeding: A Guide for the Medical Profession, 3rd ed. C.V. Mosby, St. Louis. 652 pp. Lelong, M., F. Alison, and J. Vinceneux. 1949. Secretion lactee humaine et alimentation hydrique. Lait 29:237-246. Lipsman, S., K.G. Dewey, and B. Lönnerdal. 1985. Breastfeeding among teenage mothers: milk composition, infant growth, and maternal dietary intake. J. Pediatr. Gastroenterol. Nutr. 4:426-434. Lönnerdal, B. 1986. Effect of oral contraceptives on lactation. Pp. 453-465 in M. Hamosh and A.S. Goldman, eds. Human Lactation 2: Maternal and Environmental Factors. Plenum Press, New York. Lönnerdal, B., E. Forsum, M. Gebre-Medhin, and L. Hambraeus. 1976. Breast milk composition in Ethiopian and Swedish mothers. II. Lactose, nitrogen. and protein contents. Am. J. Clin. Nutr. 29:1134-1141. Lovelady, C.A., B. Lönnerdal, and K.G. Dewey. 1990. Lactation performance of exercising women. Am. J. Clin. Nutr. 52:103-109. Lunn, P.G., A.M. Prentice, S. Austin, and R.G. Whitehead. 1980. Influence of maternal diet on plasma-prolactin levels during lactation. Lancet 1:623-625. Lunn, P.G., S. Austin, A.M. Prentice, and R.G. Whitehead. 1984. The effect of improved nutrition on plasma prolactin concentrations and postpartum infertility in lactating Gambian women. Am. J. Clin. Nutr. 39:227-235. Lyon, A.J. 1983. Effects of smoking on breastfeeding. Arch. Dis. Child. 58:378-380. Macy, I.G., H.A. Hunscher, E. Donelson, and B. Nims. 1930. Human milk flow. Am. J. Dis. Child. 39:1186-1204. Mahan, D.C. 1977. Effect of feeding various gestation and lactation dietary protein sequences on long-term reproductive performance in swine. J. Anim. Sci. 45:1061-1072. Martin, R.H. 1983. The place of PRL in human lactation. Clin. Endocrinol. 18:295-299. Matheson, I., and G.N. Rivrud. 1989. The effect of smoking on lactation and infantile colic. J. Am. Med. Assoc. 26:42-43. Moore, B.J., T. Gerardo-Gettens, B.A. Horwitz, and J.S. Stern. 1986. Hyperprolactinemia stimulates food intake in the female rat. Brain Res. Bull. 17:563-569. Motil, K.J., C.M. Montandon, and C. Garza. 1986. Effect of dietary protein intake on milk production in lactating women. Am. J. Clin. Nutr. 43:677. 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. Naing, K.M., and T.T. Oo. 1987. Effect of dietary supplementation on lactation performance of undernourished Burmese mothers. Food Nutr. Bull. 9:59-61. Naismith, D.J., D.P. Richardson, and A.E. Pritchard. 1982. The utilization of protein and energy during lactation in the rat, with particular regard to the use of fat accumulated in pregnancy. Br. J. Nutr. 48:433-441.

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Nutrition During Lactation Neifert, M.R., and J.M. Seacat. 1986. Mammary gland anomalies and lactation failure. Pp. 293-299 in M. Hamosh and A.S. Goldman, eds. Human Lactation 2: Maternal and Environmental Factors. Plenum Press, New York. Neifert, M.R., S.L. McDonough, and M.C. Neville. 1981. Failure of lactogenesis associated with placental retention. Am. J. Obstet. Gynecol. 140:477-478. Neville, M.C., and M.R. Neifert, eds. 1983. Lactation: Physiology, Nutrition, and Breast-Feeding. Plenum Press, New York. 466 pp. Neville, M., and J. Oliva-Rasbach. 1987. Is maternal milk production limiting for infant growth during the first year of life in breastfed infants? Pp. 123-133 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. Neville, M.C., R. Keller, J. Seacat, V. Lutes, M. Neifert, C. Casey, J. Allen, and P. Archer. 1988. Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am. J. Clin. Nutr. 48:1375-1386. Newton, M., and N.R. Newton. 1948. The let-down reflex in human lactation. J. Pediatr. 33:698-704. Newton, N.R., and M. Newton. 1950. Relation of the let-down reflex to the ability to breastfeed. Pediatrics 5:726-733. Noel, G.L., H.K. Suh, and A.G. Frantz. 1974. Prolactin release during nursing and breast stimulation in postpartum and nonpostpartum subjects. J. Clin. Endocrinol. Metab. 38:413-423. Nommsen, L.A., M.J. Heinig, B. Lönnerdal, and K.G. Dewey. 1989. Appropriate timing of complementary feeding of breastfed infants. FASEB J. 3:A10-54 (abstract). Nommsen, L.A., C.A. Lovelady, M.J. Heinig, B. Lönnerdal, and K.G. Dewey. In press. Determinants of energy, protein, lipid and lactose concentrations in human milk during the first 12 mo of lactation: The DARLING Study. Am. J. Clin. Nutr. Olsen, A. 1941. Om diegivningsevnen under torst og under extradrikning. Ugeskr. Laeg. 103:897-905. Pao, E.M., J.M. Himes, and A.F. Roche. 1980. Milk intakes and feeding patterns of breastfed infants. J. Am. Diet. Assoc. 77:540-545. Paul, A.A., E.M. Muller, and R.G. Whitehead. 1979. The quantitative effects of maternal dietary energy intake on pregnancy and lactation in rural Gambian women. Trans. R. Soc. Trop. Med. Hyg. 73:686-692. Picciano, M.F., E.J. Calkins, J.R. Garrick, and R.H. Deering. 1981. Milk and mineral intakes of breastfed infants. Acta Paediatr. Scand. 70:189-194. Pollitt, E., M. Gilmore, and M. Valcarcel. 1978. The stability of sucking behavior and its relationship to intake during the first month of life. Infant Behav. Dev. 1:347-357. Prentice, A.M. 1980. Variations in maternal dietary intake, birth weight and breast-milk output in The Gambia. Pp. 167-183 in Aebi, H. and R.G. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber Publishers, Bern, Switzerland. Prentice, A. 1986. The effect of maternal parity on lactational performance in a rural African community. Pp. 165-173 in M. Hamosh and A.S. Goldman, eds. Human Lactation 2: Maternal and Environmental Factors. Plenum Press, New York. Prentice, A.M., and A. Prentice. 1988. Energy costs of lactation. Annu. Rev. Nutr. 8:63-79. Prentice, A.M., and R.G. Whitehead. 1987. The energetics of human reproduction. Symp. Zool. Soc. London 57:275-304.

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