6
Impact of Physical Activity and Diet on Lactation

Physical activity during pregnancy has potential effects on subsequent lactation performance in humans, but these effects are difficult to assess because of the limited available data. The consideration of any relationship requires the definition of at least two terms: lactation performance and physical activity. Lactation performance usually is defined from measurements of milk volume and composition and infant growth (Hamosh and Goldman, 1986). A few studies have incorporated other variables that reflect maternal health, but such broad evaluations are uncommon. The effects of maternal nutritional status on milk volume and composition have been reviewed by various authors and thus will not be of primary interest in this report (Belavady, 1979; Garza and Butte, 1985; Jelliffe and Jelliffe, 1978). In generally, milk volume appears to be more sensitive to maternal nutritional status than is gross milk composition. Although dietary intake may alter selected milk components, milk protein, carbohydrate, and total fat appear to be fairly unaffected unless the diet becomes excessively restrictive.

It is more difficult to provide an unambiguous definition of physical activity than the term's familiarity may suggest. All healthy pregnant and lactating women, regardless of socioeconomic context, remain active to some degree. For purposes of this discussion, physical activity refers to moderate and heavy work loads, as defined by the World Health Organization (WHO), and the Food and Agricultural Organization of the United Nations (FAO), unless otherwise indicated (WHO, 1985). Mean energy expenditures at specified work loads for 55-kg reference woman are 1.6–1.8 times their basal metabolic rate. The mean rates of expenditure allow 1,000 and 1,400 kcal/8 hours of moderate and heavy work, respectively. The equivalent rates expressed per minute are 2.1 and 2.9 kcal, respectively.

Although assessments of the effects of physical activity during pregnancy on lactation performance have not been published, the nature of the



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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation 6 Impact of Physical Activity and Diet on Lactation Physical activity during pregnancy has potential effects on subsequent lactation performance in humans, but these effects are difficult to assess because of the limited available data. The consideration of any relationship requires the definition of at least two terms: lactation performance and physical activity. Lactation performance usually is defined from measurements of milk volume and composition and infant growth (Hamosh and Goldman, 1986). A few studies have incorporated other variables that reflect maternal health, but such broad evaluations are uncommon. The effects of maternal nutritional status on milk volume and composition have been reviewed by various authors and thus will not be of primary interest in this report (Belavady, 1979; Garza and Butte, 1985; Jelliffe and Jelliffe, 1978). In generally, milk volume appears to be more sensitive to maternal nutritional status than is gross milk composition. Although dietary intake may alter selected milk components, milk protein, carbohydrate, and total fat appear to be fairly unaffected unless the diet becomes excessively restrictive. It is more difficult to provide an unambiguous definition of physical activity than the term's familiarity may suggest. All healthy pregnant and lactating women, regardless of socioeconomic context, remain active to some degree. For purposes of this discussion, physical activity refers to moderate and heavy work loads, as defined by the World Health Organization (WHO), and the Food and Agricultural Organization of the United Nations (FAO), unless otherwise indicated (WHO, 1985). Mean energy expenditures at specified work loads for 55-kg reference woman are 1.6–1.8 times their basal metabolic rate. The mean rates of expenditure allow 1,000 and 1,400 kcal/8 hours of moderate and heavy work, respectively. The equivalent rates expressed per minute are 2.1 and 2.9 kcal, respectively. Although assessments of the effects of physical activity during pregnancy on lactation performance have not been published, the nature of the

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation interaction can be inferred from studies of women with presumably heavy work loads and marginal or adequate nutritional status. Physical activity appears to exacerbate the negative effects of poor nutritional status on milk volume. Data from studies done in The Gambia illustrate this point in comparisons of milk volume under conditions of work and maternal planes of nutrition (Prentice et al., 1982). The physiologic basis for this view and representative data that examine potential relationships between physical activity and lactation performance are considered in more detail in subsequent sections of this chapter. INFLUENCE OF PHYSICAL ACTIVITY ON FAT STORAGE DURING PREGNANCY AND LACTATION Because the nutrient demands of physical activity are closely associated with energy, concern arises for the sufficiency of maternal energy stores at the end of a physically active woman's pregnancy. As reviewed earlier in this report, a significant proportion of weight gained during pregnancy represents maternal adipose tissue. One possible functional role of fat stores accumulated during pregnancy may be to buffer the need for additional dietary energy imposed by lactation. If physical activity during pregnancy interferes with the accumulation of normal quantities of fat, lactation performance may be affected adversely. Two mechanisms that can be postulated for those adverse influences are 1) a putative dependence on minimal fat stores to produce milk of normal volume and composition for an acceptable period of time and 2) the likelihood that increased demands for dietary energy for lactation will not be met if the mother has insufficient stores of energy. Women who gain 11 to 13 kg body weight during pregnancy should have stored 2 to 4 kg of fat. Those energy stores may be assumed to have been accumulated in a physiologic anticipation of lactation. On the basis of an estimated mean milk output during the first 4 to 6 months of lactation of approximately 750 ml/day and a gross caloric concentration in milk of approximately 0.64 kcal/ml, the lactating woman loses approximately 500 kcal/day in milk (Butte, et al., 1984). Estimates of the efficiency of milk production range from 80 percent to 95 percent. The energy required to synthesize 750 ml of milk, therefore, is approximately 25 to 125 kcal/day plus 500 kcal accounted for by the gross energy content of the milk. If a conservative estimate of 500 kcal/day (i.e., 100-percent efficiency) for the cost of milk production is used, 2 to 4 kg of fat (i.e., 17,000 to 34,000 kcal) would theoretically represent sufficient energy for approximately 1.2 to 2.5 months of milk production. If an estimate of 625 kcal/day (i.e., 80-percent

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation efficiency) is used, 2 to 4 kg of fat stores would theoretically represent sufficient energy for approximately 1 to 2 months of milk production. Those estimates are based on two assumptions. The first is that energy intake during lactation is balanced against all other maternal energy needs. An excessive or deficient intake of energy has a corresponding effect on the length of time that will lapse before fat accumulated during pregnancy is exhausted. If energy intakes before and after work is begun are similar, an increased work load imposes correspondingly greater demands on maternal energy stores. Under low energy intake, it is not known whether maternal functions are defended at the expense of milk production, or whether milk production is maintained at a cost to maternal functions. The second assumption is that reductions in milk production (in terms of volume or composition) and maternal well-being occur concurrently under unfavorable circumstances. Quantitative relationships among maternal nutrient stores, activity patterns, diet, and milk production have not been described for humans. It is assumed that all maternal adipose tissue stores accumulated during pregnancy are directly or indirectly available for milk production. The general availability of energy derived from fat, however, depends partially on an individual's aerobic conditioning, the type of work that is performed, and the duration of work episodes (Astrand and Rodahl, 1970). All three factors determine the proportion of fat and glucose required to perform specific tasks. Generally, individuals with good aerobic status, compared with those less aerobically conditioned, oxidize greater proportions of fat when performing specific energy-requiring work. Knowledge of milk composition is pertinent to these considerations. Only 50 percent of milk energy is derived from fat; the remaining 50 percent is represented by protein and lactose, neither of which is obtained from fat. Because neither protein nor glucose is stored like fat, they must be supplied from the diet. Dietary carbohydrates that are not used immediately for energy are either converted to fat or are used to replenish glycogen stores. Dietary protein is used for the production of milk, is used to replenish body protein lost through the inefficiency of the body's protein turnover, or is converted to fat or glucose. Fat and glucose derived from protein are oxidized immediately or stored in either adipose tissue or glycogen. If dietary carbohydrate and excess protein can be redirected to the production of milk, and if a corresponding amount of stored fat can be substituted in the other usual metabolic pathways that produce energy, the 2 to 4 kg of fat accumulated during pregnancy should suffice for 1 to 2.5 months of milk production without concurrent reductions in prepregnancy maternal stores. If maternal needs for carbohydrate-derived energy cannot be adjusted, the use of maternal fat stores may be limited largely to the provision of fat for milk.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Such a limitation may prolong the availability of accumulated fat, but will increase the demand on dietary requirements and maternal lean body mass. Physical activity during pregnancy is likely to contribute to the maintenance of aerobic conditioning in the postpartum state, and thus, the redirection of nutrients for milk production should not be impaired. There are no data, however, to evaluate that possibility. Nevertheless, if maternal energy intakes increase sufficiently to meet all needs except those represented by the loss of stored fat into milk, there should be no adverse effects on maternal function. If maternal energy intakes do not increase sufficiently to meet requirements, then milk production, other maternal functions, or both will be impaired. The degree of impairment will depend on the demands of physical activity, nutrient stores, and diet. Data are insufficient, however, to support quantitative inferences. The relationships among lactation performance, maternal diet, and body composition have been evaluated in the lactating ruminant, but results of these studies are difficult to assess because of genetic inbreeding of ruminants for milk production and significant differences in the derivation of milk components from rumen metabolism (Larson and Smith, 1974). The few studies done in nonruminants that address these relationships suggest that dietary intake during pregnancy influences the balance between milk production and the maintenance of maternal well-being. As a typical example, studies in the sow have demonstrated that milk production assessed by litter weight gain is not hampered by dietary deprivation during pregnancy if adequate or surplus nutrients are provided during the subsequent lactation. If, however, an inadequate diet during lactation follows an inadequate diet during pregnancy, litter weight gain is compromised (Mahan and Mangan, 1975). Other studies in the rat have compared energy expenditures for maintenance and activity in virgin and lactating animals (Roberts and Coward, 1984). Lactating rats fed restricted amounts of food expended less energy for maintenance and activity than did virgin rats on similar diets. Those results suggest an increased efficiency of energy use during lactation among food-restricted rats. How maternal activity patterns during pregnancy may influence such responses is difficult to predict, even if confident extrapolations of the results of animal studies to humans were possible. As in other physiologic processes, endocrine signals are expected to influence the use of nutrients either for milk production or for more immediate maternal needs. Endocrine controls of milk production have been evaluated primarily in animals. The investigations suggest that animals with high milk yields tend to maintain lower insulin levels and higher growth hormone (GH) levels than do those with low milk yields (Hart et al., 1979).

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation The link between insulin levels and milk production may be the subsequent availability of glucose. Relatively low levels of insulin usually are associated with increased levels of glucose output by the liver, decreases in the uptake of glucose by competing tissues, and higher levels of lipolysis. Higher levels of circulating free fatty acids should decrease glucose oxidation by tissues able to metabolize either fat or glucose. The net result would be an increased availability of glucose for milk production. This chain of events, though plausible, is speculative; few data obtained in human experiments are available to assess its accuracy. Nonetheless, if physical activity during pregnancy helps to maintain lower baseline insulin levels in the postpartum state, this mechanism may promote increased milk production and thereby modulate other factors that affect lactation performance adversely. RELATED FUNCTIONAL ASPECTS OF ENERGY STORES Although diet and activity patterns during pregnancy may influence the amount and distribution of stored fat, available data do not allow confident predictions of their effects on lactation performance. Adipose tissue does not appear to be mobilized uniformly under all conditions during lactation, and evidence suggests that adipose tissue is not functionally homogeneous. Subscapular skin fold thickness has been noted to decrease during the first 4 months of lactation at a greater rate than the decrease of the triceps or suprailiac region in well-nourished American women (Butte et al., 1984). The lipolytic and lipoprotein lipase (LPL) activities in biopsies of sample femoral and abdominal adipose tissues of healthy nonpregnant women and of pregnant and lactating women also suggest that there are important functional differences that are specific for site and physiologic state (Lafontan et al., 1979; Rebuffe-Scrive et al., 1985). Basal lipolytic rates are similar in both tissues in nonpregnant women, but significantly higher in the femoral depot of lactating women. The lipolytic effect of noradrenaline administration is similar in both sites during lactation, but is significantly less in the femoral tissue of nonpregnant women and women during early pregnancy. The LPL activity in abdominal adipose tissue remains the same in all three physiologic states (nonpregnant, pregnant, and lactating), but it is decreased in the femoral adipose tissue of lactating women. These observations suggest that lipid accumulation in both nonpregnant and pregnant women is favored in femoral stores over the abdominal depot. Femoral adipose tissue undergoes unique adaptations, however, during lactation. The LPL activity falls and the response to lipolytic stimuli increases. Lipid mobilization, therefore, is favored by femoral tissue during

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation lactation. Thus, in specific physiologic states, different adipose tissue sites appear to be specialized in their relative availability as energy sources. Specific changes in adipose tissue also occur during lactation in rats and mice (Trayhurn and Brown, 1985). Lipolysis is favored in white adipose tissue during lactation. Lactation also is associated with a decrease in the number of insulin receptors and a heightened insulin resistance. Changes also are observed in brown adipose tissue (BAT). The concentration of uncoupling protein in BAT mitochondria is substantially decreased in lactating mice. The inverse relationship between the number of pups and the levels of uncoupling protein and cytochrome oxidase activity suggest that the suppression of thermogenesis in BAT is related directly to the nutritional demands imposed on the mother. Although the suppression of thermogenesis promotes a heightened efficiency of energy use by the lactating rat, functional consequences of that adjustment are poorly defined. The insulin resistance reported for adipose tissue is in direct contrast to the generally increased insulin sensitivity and responsiveness reported for the lactating rat (Burnol et al., 1986). Insulin concentrations that induce half maximal stimulation of glucose use and metabolic clearance are decreased by 50 percent during lactation. The interactive effects, however, between physical activity during pregnancy and lactation and the accumulation and use of fat stores in each physiologic state have not been described. INFLUENCE OF PHYSICAL ACTIVITY DURING PREGNANCY ON THE EFFICIENCY OF MILK PRODUCTION There are no apparent physiologic mechanisms through which physical activity during pregnancy is expected to affect the efficiency of milk synthesis in the subsequent postpartum period. The few studies that have measured the resting metabolic rate (RMR) or the basal metabolic rate (BMR) in lactating women are inconsistent in their conclusions. Studies of Guatemalan women in month 10 of lactation reported an RMR of 46 ± 6 kcal/hour or 32.5 kcal/m2/hour, values that were similar to measurements in nonlactating controls (Schutz et al., 1980). Studies of Indian lactating women report a BMR approximately 6 to 12 percent above those reported for nonlactating control women in India (Khan and Benady, 1973); the reported mean values for lactating women 1 to 6 months postpartum ranged from approximately 35 to 37 kcal/m2/hour. In contrast to reports of RMRs in women in Guatemala and India, RMRs in young Gambian women whose intakes were not supplemented have been reported to fall at 10 to 25 weeks gestation but to rise after the provision of a daily food supplement. The reduction in RMR appears to

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation persist during lactation in the unsupplemented group (Lawrence et al., 1984; Whitehead et al., 1986). Whether the fall in the RMR represents a response to increased nutritional stress analogous to that seen with starvation is not clear from those studies. If the analogy is appropriate, impairment of functions that require multiple organ systems should be expected, as was documented in partial starvation studies of young adult men in Minnesota (Keys, 1950). If the higher metabolic rates of the supplemented group represented responses to an excessive intake of energy, the functional consequences are less certain. CARDIOVASCULAR ADAPTATIONS Physical activity during pregnancy and lactation is expected to influence a woman's cardiovascular status. The supply of substrates to the mammary glands for milk production should also require significant cardiovascular adaptations. Unfortunately, there are few studies in humans that evaluate this aspect of normal lactation physiology. Most studies of postpartum physiology do not describe activity patterns during pregnancy and the postpartum period and do not indicate whether the subjects chose to breast or bottle feed their infants. The best animal studies are those of Hanwell and Linzell (1973a), who reported that cardiac output remains above prepregnancy levels when lactation follows pregnancy, and there is a heightened flow of blood to the mammary glands and to organs of the alimentary system. There is no certainty, however, whether those changes occur in humans or what the interactive effects with physical activity may be. The mechanisms responsible for the cardiovascular changes in animals are not well defined. Hanwell and Linzell (1973b; 1972) demonstrated that increased cardiac output in rats appears to be dependent upon the suckling stimulus and not necessarily on milk removal. Mammary blood flow and high cardiac outputs in these animals were maintained by administration of prolactin or growth hormone. Prolactin stimulation due to physical activity also has been reported, but studies in lactating or pregnant women have not been published (Cavanaugh, 1982). FIELD STUDIES AND LACTATION PERFORMANCE Lactation in well-and marginally nourished women with distinct activity patterns has been assessed in field studies. For example, Gambian women were reported to consume approximately 1,600 kcal/day and to lose approximately 500 to 600 kcal/day in milk (Prentice et al., 1981) in the dry

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation season characterized by lessened farm work activities. When energy intake, weight changes, and milk output were compared, the residual energy available for basal and activity needs was approximately 1,000 kcal. That amount of energy should be sufficient only to cover basal metabolic costs. Yet, those women were reported to have deposited subcutaneous fat and therefore appeared to be in positive energy balance. The volume of milk produced by the Gambian women appears similar to that produced by North American women who consume approximately 600 additional kcal/day and presumably have lower work loads. Similar calculations of energy available to North American women suggest that after basal needs are met, 300 kcal/day remain for activity (Butte et al., 1984). Periods of the heaviest work loads in the Gambian population were characterized by intakes of approximately 1,400 kcal/day. Lactating women lost weight during periods of lowest energy intakes and highest work loads, that is, the wet season. Energy output in milk may be examined in two ways. For the period 2 to 6 months postpartum, milk production was reported to decrease from. 850 g/day in June (dry season) to 540 g/day in October. Alternatively, energy outputs in milk during similar trimesters may be compared. Such contrasts indicated that milk production was, on average, only 2 percent greater in the dry season than in the wet one. An earlier publication reported a negative correlation between milk production at 3 months and in skinfold thickness over the second 6 weeks of lactation. The authors interpreted this observation to indicate that repletion of maternal fat stores adversely affected the volume of milk that was produced. The alternative hypothesis, that is, that skin fold changes were a result of milk production, was not given sufficient consideration (Paul et al., 1979). The estimate of energy available for basal and activity needs that was derived from estimates of intake, weight changes, and milk production during the period of more intense work (i.e., the wet season) was also approximately 1,000 kcal. The efficiency of energy use appears to be much greater than anticipated in both seasons. The energy expenditure of lactating women also was measured by the doubly labeled water method in preliminary studies conducted in The Gambia. Higher estimates of energy expenditure than were predicted by more conventional methodologies were reported (Prentice, 1987). Estimates of energy expenditure from those studies were not consistent with estimates of residual energy made by more conventional methods (Prentice, 1987). In these studies, as well as in others, the lack of correlation between energy intake and expenditure measurements is alarming. The growth of breast-fed infants also may be used to assess lactation performance. Gambian infants are reported to grow at acceptable rates until approximately 3 months of life, the approximate age at which weaning foods

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation are added to their diets (Rowland et al., 1981). The basis for the drop in growth rates from the expected values is not known. Increased morbidity is one potential explanation. An inadequate intake of milk is another. Milk volumes appear to decrease at about 3 months post partum. In contrast to the lowered outputs, sustained outputs are common in North American women who continue to breastfeed their infants exclusively through 4 to 5 months. However, once solid foods are introduced into the diets of exclusively breast-fed North American infants, their milk intakes also drop. The magnitude of the decreased intake of milk appears to be proportional to the intake of solid foods. Therefore, whether the fall in milk volumes in Gambian women represents a maternal inability to sustain adequate volumes of milk production or is the result. of the introduction of other foods to their infants' diet is unclear (Stuff et al., 1986). The Gambian studies also included assessments of the effects of dietary supplementation on milk volume and quality (Prentice et al., 1983). When a food supplement was added to the mothers' diets, their energy intakes were increased from 1,568 kcal/day to 2,291 kcal/day. The supplement had no effect on milk volume at any stage of lactation or in any season of the year, and the effects on milk composition appeared trivial. Also, there were no selective effects on women with the lowest rates of milk production. The energy provided in the supplement could not be accounted for by increased maternal weight (Prentice et al., 1983b). Although a weight gain of 1.8 kg was noted over the year the supplement was provided, the subjects still experienced weight loss during the period of heaviest activity. The increased average weight increment accounted for approximately 7 percent of the total energy provided by the supplement over the year. Supplemented women were noted to have fewer health-related complaints, but maternal morbidity was not well characterized. The authors speculate that unaccounted energy may have been used for increased activity or accounted for by changes in the efficiency of energy use. Other investigators who have examined the effects of supplementation on milk yield report data that are not in agreement with the Gambian observations. Sosa et al. (1976) report significant improvements in lactation performance from intensive observations on one undernourished woman. More recently, Girija et al. (1984) have evaluated the effects of a supplement that provided 417 kcal and 30 g protein for approximately 12 weeks to women with baseline diets providing approximately 1,700 kcal/day and 40 g/day of protein. Supplemented women gained approximately 1.3 kg; control women lost weight. Milk yields of supplemented and control women were similar until the third month postpartum. After that time, the supplemented group produced approximately 30 percent more milk than the control group.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Animal studies also have shown a positive influence of supplements during lactation (Roberts and Coward, 1985). A confident evaluation of the relationship among activity during pregnancy, supplements provided during pregnancy, and subsequent lactation performance is not possible with the data currently available. Maternal nutritional status in the Gambian studies did not appear to deteriorate with increasing parity. Body weight and nutrient status with respect to iron, hemoglobin, riboflavin, and vitamins A and C are reported to be independent of parity (Prentice et al., 1981). Those data suggest that repeated cycles of pregnancy and lactation superimposed on heavy work loads in that population do not lead to a detectable impairment of maternal well-being. Nonetheless, a disparity in available data is evident from reviews such as those of Jelliffe, in which impaired lactation performance is reported in marginally nourished women, some with presumably heavy work loads (Jelliffe and Jelliffe, 1978). Recent reports, such as that of Manjrekar et al. (1985) indicate that women who consumed approximately 1,500 or 1,100 kcal/day produced insufficient volumes of milk within the first 4 months of lactation. Women who delivered low-birthweight infants (< 2.6 kg) produced insufficient milk volumes by 2 months. These findings are complicated by various factors. Many of the subjects returned to work in the early postpartum period, and their early return may have affected lactation performance. Also, milk production is known to depend on both maternal factors and infant behaviors. Conditions that may have an adverse effect on an infant's feeding behavior (e.g., low birth weight) may also have negative results on the volume of milk produced. The effects of maternal physical activity on birth weight also are relevant to this discussion. Part of the rationale for postulating that physical activity may impair birth weight is an expected adverse effect of activity on placental perfusion. That expectation rests on the suggestion that the sympathetic nervous system is activated by physical activity. Its activation may result in the redirection of cardiac output to priority organs that may not include the placenta. If the blood supply is directed away from the mammary glands during physical activity, one may speculate that the glands' preparation for milk synthesis is adversely affected and that after parturition, increased sympathetic activity may continue to impair mammary gland function. Such a response may explain why nutrient supplementation was not associated with an increased volume of milk production in the Gambian studies.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation SUMMARY The potential effects of physical activity during pregnancy on lactation performance are difficult to predict. If physical activity during pregnancy limits or interferes with fat deposition, maternal well-being may be adversely affected. Conversely, maintenance of a high level of activity may promote more efficient use of fat stores during pregnancy, reduce baseline insulin levels, and result in higher milk yields. The effects of continued activity during lactation on lactation performance also are difficult to predict. The added demands of physical activity impose greater nutritional needs on the mother, and the maintenance of higher sympathetic ''tone'' may impair mammary gland function. Although this is highly speculative, there is little question of the need for sound experiments that define lactation physiology in humans. REFERENCES Astrand, P., and K. Rodahl. 1970. Textbook of Work Physiology. McGraw Hill, New York. Belavady, B. 1979. Quantity and composition of breast milk in malnourished mothers Pp. 62–68 in L. Hambraeus and S. Sjölin, eds. The Mother/Child Dyad—Nutritional Aspects. Symposia of the Swedish Nutrition Foundation XIV. Almqvist & Wiksell International, Stockholm. Burnol, A.F., A. Leturque, P. Ferre, J. Kande, and J. Girard. 1986. Increased insulin sensitivity and responsiveness during lactation in rats. Am. J. Physiol. 251:E537–E541. Butte, N.F., C. Garza, J.E. Stuff, E.O. Smith, and B.L. Nichols. 1984. Effect of maternal diet and body composition on lactational performance. Am. 5. Clin. Nutr. 39:296–306. Cavanaugh, J.I. 1982. Acute and chronic effects of exercise on plasma concentrations of prolactin and hematological parameters in women runners (Doctoral thesis). The Ohio State University, Columbus. Garza, C., and N.F. Butte. 1985. The effect of maternal nutrition on lactational performance. Pp. 15–35 in N. Kretchmer, ed. Frontiers in Clinical Nutrition. Aspen Publishers, Rockville, Md. Girija, A., P. Geervani, and G.N. Rao. 1984. Influence of dietary supplementation during lactation on lactation performance . J. Trop. Pediatr. 30:140–144. Hamosh, M., and A.S. Goldman, eds. 1986. Human Lactation 2: Maternal Factors in Lactation. Plenum Press, NY. Hanwell, A., and J.L. Linzell. 1972. Elevation of cardiac output in the rat by prolactin and growth hormone. J. Endocrinol. 53.57A–58A. Hanwell, A., and J.L. Jinzell. 1973a. The effect of engorgement with milk and of suckling on mammary blood flow in the rat. J. Physiol. 233.111–125. Hanwell, A. and J.L. Linzell. 1973b. The time course of cardiovascular changes in lactation in the rat. J. Physiol. 233.93–109. Hart, I.L., J.A. Bines, and S.V. Morant. 1979. Endocrine control of energy metabolism in the cow: Correlations of hormones and metabolites in high and low yielding cows for stages of lactation. J. Dairy Sci. 62:270–277. Jelliffe, D.B., and E.F.P. Jelliffe. 1978. The volume and composition of human milk in poorly nourished communities: A review. Am. J. Clin. Nutr. 31:492–515.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Keys, A., J. Brozek, A. Henschel, O. Mickelsen, and H.L. Taylor. 1950. The Biology of Human Starvation. Univ. Minn. Press, Minn. Khan, L., and B. Belavady. 1973. Basal metabolism in pregnant and nursing women and children. Indian J. Med. Res. 61:1953–1960. Lafontan, M., L. Dang-Tran, and M. Berlan. 1979. Adlpha-adrenergic antilipolytic effect of adrenaline in human fat cells of the thigh: Comparison with adrenaline responsiveness of different fat deposits. Eur. J. Clin. Invest. 9.261–266. Larson, B.L., and V.R. Smith, eds. 1974. Lactation: A Comprehensive Treatise. Vol. I–IV. Academic Press, New York. Lawrence, M., F. Lawrence, W.H. Lamb, and R.G. Whitehead. 1984. Maintenance energy cost of pregnancy in rural Gambian women and influence of dietary status. Lancet 2(8399):363–365. Mahan, D.C., and L.T. Mangan. 1975. Evaluation of various protein sequences on the nutritional carry over from gestation to lactation with first litter sows. J. Nutr. 105:1921–1928. Manjrekar, C., M.P. Vishalakshi, N.J.A. Begum, and G.N. Padma. 1985. Breastfeeding ability of undernourished mothers and physical development of their infants during 0–1 year. Indian Pediatr. 22.801–809. Paul, A.A., M. Mueller, and R.G. Whitehead. 1979. The quantitative effects of maternal dietary energy intake on pregnancy and lactation in rural Gambian women. Trans. Soc. Trop. Med. Hyg. 73:686–692. Prentice, A.M. 1987. Applications of the 2H2180 method in free-living adults. Presented at a symposium of stable isotopic methods for measuring energy expenditure, July 16–17. The Nutrition Society, Cambridge, U.K. Prentice, A.M., R.G. Whitehead, S. Roberts, A.A. Paul. 1981. Long-term energy balance in child-bearing Gambian women. Am. J. Clin. Nutr. 34:2790–2799. Prentice, A.M., S.B. Roberts, A. Prentice, A.A. Paul, M. Watkinson, A.A. Watkinson, and R.G. Whitehead. 1983a. Dietary supplementation of lactating Gambian women. I. Effect on breast-milk volume and quality. Hum. Nutr. Clin. Nutr. 37:53–64. Prentice, A.M., P.G. Lunn, M. Watkinson, and R.G. Whitehead. 1983b. Dietary supplementation of lactating Gambian women. II. Effect on maternal health, nutritional status and biochemistry. Hum. Nutr. Clin. Nutr. 37C:65–74. Rebuffe-Scrive, M., L. Enk, N. Crona, P. Lonnroth, L. Abrahamsson, U. Smith, and P. Bjorntorp. 1985. Fat cell metabolism in different regions in women. J. Clin. Invest. 75:1973–1976. Roberts, S.B., and W.A. Coward. 1984. Lactation increases the efficiency of energy utilization in rats. J. Nutr. 114:2193–2200. Roberts, S.B., and W.A. Coward. 1985. Dietary supplementation increases milk output in the rat. Br. J. Nutr. 53:1–9. Rowland, M.G.M., A.A. Paul, and R.G. Whitehead. 1981. Lactation and Infant Nutrition. Br. Med. Bull. 37:77–82. Schutz, Y., A. Lechtig, and R.B. Bradfield. 1980. Energy expenditures and food intakes of lactating women in Guatemala. Am. J. Clin. Nutr. 33:892–902. Sosa R., M. Klaus, and J.J. Urrutia. 1976. Feed the nursing mother, thereby the infant. J. Pediatr. 88:668–670. Stuff, J.E., C. Garza, C. Boutte, and B.L. Nichols. 1986. Caloric intake of older breast-fed infants: Human milk and solid food. Am. J. Clin. Nutr. 43:679. Trayhurn, P., and R.D. Brown. 1985. Adipose tissue thermogenesis and the energetics of pregnancy and lactation in rodents. Biochem. Soc. Trans. 13:826–827. Whitehead, R.G., M. Lawrence, and A.M. Prentice. 1986. Maternal nutrition and breastfeeding. Hum. Nutr. Appl. Nutr. 40:1–10. WHO (World Health Organization). 1985. Technical Report Series No. 724. Energy and Protein Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. WHO, Geneva.