3
Relationships Between Nutrition and Diarrhea

The interaction between malnutrition and diarrheal diseases, as for most infections, is bidirectional; that is, the nutritional state alters the host response to infection and infectious illness alters nutritional state (Scrimshaw et al., 1968). When infections are frequent, especially recurrent diarrheal diseases, the interaction may become circular, with an increasing frequency of infection and a parallel and progressive deterioration in host nutritional status that proceeds to overt protein energy malnutrition if the cycle is not interrupted (Keusch and Scrimshaw, 1986).

Acute, repetitive, or chronic infections are invariably the cause of some degree of nutrient losses due to associated anorexia, catabolism of nutrient stores, and malabsorption due to intestinal infection. Nutritional losses occur in virtually all infected hosts, regardless of their nutritional status at the outset, but the consequences are most visible in those with the least ability to replace the losses. These losses can be exacerbated by the withdrawal of food during the infection and by the usual lack of suitable foods in developing countries that should be fed to convalescents (Beisel, 1977; Keusch and Scrimshaw, 1986; Watson, 1984).

EVIDENCE THAT MALNUTRITION PREDISPOSES THE HOST TO DIARRHEAL DISEASE

Most studies attempting to investigate whether malnutrition predisposes the host to diarrheal diseases have used anthropometric measures as the indicator of nutritional status. The reported outcome measures, such as incidence, duration, or some measure of seventy of diarrhea, have been more variable. Although it is necessary to control the studies for poverty (which



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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation 3 Relationships Between Nutrition and Diarrhea The interaction between malnutrition and diarrheal diseases, as for most infections, is bidirectional; that is, the nutritional state alters the host response to infection and infectious illness alters nutritional state (Scrimshaw et al., 1968). When infections are frequent, especially recurrent diarrheal diseases, the interaction may become circular, with an increasing frequency of infection and a parallel and progressive deterioration in host nutritional status that proceeds to overt protein energy malnutrition if the cycle is not interrupted (Keusch and Scrimshaw, 1986). Acute, repetitive, or chronic infections are invariably the cause of some degree of nutrient losses due to associated anorexia, catabolism of nutrient stores, and malabsorption due to intestinal infection. Nutritional losses occur in virtually all infected hosts, regardless of their nutritional status at the outset, but the consequences are most visible in those with the least ability to replace the losses. These losses can be exacerbated by the withdrawal of food during the infection and by the usual lack of suitable foods in developing countries that should be fed to convalescents (Beisel, 1977; Keusch and Scrimshaw, 1986; Watson, 1984). EVIDENCE THAT MALNUTRITION PREDISPOSES THE HOST TO DIARRHEAL DISEASE Most studies attempting to investigate whether malnutrition predisposes the host to diarrheal diseases have used anthropometric measures as the indicator of nutritional status. The reported outcome measures, such as incidence, duration, or some measure of seventy of diarrhea, have been more variable. Although it is necessary to control the studies for poverty (which

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation can affect both food availability and nutritional status, sometimes in a seasonal fashion), as well as for environmental factors that govern transmission (including the level of sanitation, hygienic practices, water availability, and others), this is not commonly done, because resistance to infection is graded rather than being an all or none phenomenon. Therefore, clinical disease can occur in relatively immune competent hosts from an inoculum large enough to overcome host defenses. Recent studies have attempted to control for these variables. The results reveal a consistent finding that malnutrition has an adverse effect on diarrheal disease, however there is little consistency from study to study as to the diarrheal disease parameter that is affected. For example, Tomkins (1981) assessed the attack rate and prevalence of diarrhea in 343 Nigerian children, aged 6–32 months, who were observed closely for 3 months. No difference in attack rate was observed between the better nourished children and those with either less than 75 percent of the weight-for-age or less than 90 percent of the height-for-age standard. In contrast, the attack rate was significantly greater in children with less than 80 percent weight-for-height (P < 0.01). On average, the duration of diarrhea appears longer in wasted children. They were clinically ill with diarrhea 13.6 percent of the time compared with 7.6 percent of the time for the better nourished children (P < 0.01). Tomkins (1981) assumed exposure to pathogens was similar in all children because they drank the same well water and consumed food that was contaminated to a similar degree with Escherichia coli. Thus he concluded that differences in attack rates and number of illness days were attributable to nutritional state and that malnutrition resulted in impaired resistance to enteric pathogens. A more recent well-controlled cohort study of children less than 2 years of age was conducted in Mexico by Sepulveda et al. (1988). Subjects were selected by their weight-for-age, morbidity was determined by weekly home visits, and confounding variables (including seasonal, demographic, and socioeconomic parameters) were controlled. The incidence of diarrhea in children who were poorly nourished (60–75 percent of the weight-for-age standard) increased by 80 percent over that in children who were initially found to be greater than 90 percent of weight-for-age. In addition, malnourished children were more likely to experience multiple episodes of diarrhea, even though no difference in the duration of diarrhea was noted. Black et al. (1984b) studied the relationship of nutritional status and subsequent diarrheal disease morbidity in 197 Bangladeshi children in a longitudinal, community-based investigation. An important feature of this study was the separation of subjects by etiology of the diarrhea. No difference in disease incidence was detected among groups that were distinguished by nutritional status; however, the duration of illness was 56

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation percent longer in those infants with weight-for-length of less than 80 percent of the median National Center for Health Statistics (NCHS) standard compared with that in infants who were greater than 90 percent of this benchmark. The effect was also most evident in patients with documented shigellosis or enterotoxigenic E. coli infections. The mean duration of illness in patients infected with Shigella was 22.2 days compared with 8.8 days in patients in the non-Shigella-infected group. Black et al. (1984a) concluded that the increased duration of diarrhea could explain the well-known increase in diarrheal disease prevalence in malnourished children, with no change in incidence being attributable to poor nutrition. The conclusions are supported by similar data obtained in a more recent study in the same area of Bangladesh (Bairagi et al., 1987). Intervention studies represent another source of available data for evaluation of the relationship between nutritional status and susceptibility to diarrheal disease. Feachem (1983) recently reviewed this topic and found that results of most available studies are inconclusive because the study designs did not allow discrimination between the preventative and the therapeutic effects of feeding on malnutrition associated with diarrheal disease. Because of the close association between diarrheal disease and growth faltering (Black et al., 1984a; Guerrant et al., 1983), it is difficult to make this distinction, especially in populations with a high burden of infection (James, 1972; Trowbridge et al., 1981), where crowding, poor sanitation and personal hygiene, poverty, and inadequate access to health care all contribute to perpetuating both the high prevalence of infection in general and diarrhea in particular. Nutritional status can potentially influence the severity of diarrheal diseases. Definition of severity is arbitrary, however, and no consistent criteria have been applied in different studies. The stool purging rate in children with enterotoxigenic E. coli or rotavirus infection was inversely related to weight-or length-for-age in Bangladeshi children (Black et al., 1984b). This observation is consistent with the more frequent occurrence of severe dehydration in children with rotavirus diarrhea with a low weight-for-age (Black et al., 1984a). Another criterion of severity is mortality rate. The relevant question is whether there is an association between mortality from diarrhea and nutritional state. An often cited major review of mortality in Latin America concluded that about three-fifths of the infection-related deaths (including those as a result of diarrheal diseases and other infections) in children under 5 years of age occurred in malnourished children, whereas one-third of deaths from other, noninfectious causes were in poorly nourished children (Puffer and Serrano, 1973). Similar data have been reported from Bangladesh and India (Chen et al., 1980; Kielmann and McCord, 1978). Diarrhea-

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation specific deaths were tallied separately, irk the Bangladesh study, and a child with a weight-for-age of less than 65 percent of the standard was 3.7 times more likely to die with diarrhea during the following 24 months than children with a better initial nutritional status. In northern India case fatality rates were 3.5 times higher in severely malnourished children than moderately malnourished children, but this level was nearly 20 times higher than the rate for mildly malnourished and well-nourished subjects together (Bhan et al., 1986). In addition, Briend et al. (1987) showed that malnutrition, as indicated by mid-upper-arm circumference (MUAC) measurements, is a strong predictor of mortality within a month of the measurement (relative risk of 20), achieving a specificity of 94 percent and a sensitivity of 56 percent with a MUAC cutoff of less than 110 mm. In the same population, diarrhea was independently associated with a relative risk of death of 4.8, with a specificity of 87 percent and a sensitivity of 42 percent; deaths were almost entirely associated with bloody diarrhea or there was a prolonged duration of greater than 1 week. Causes of death were not assessed in this population. Mortality data from hospitalized children show the same trends; however, these data are likely to be biased because of the admission of children with more clinically severe cases of diarrhea to the hospital. A study from Bangladesh used multivariate analysis to evaluate the risk factors for death in children with diarrheal disease (Samadi et al., 1985). Increased mortality was associated with malnutrition, and all of the increased risk was accounted for by the use of hyponatremia as a criterion. Case fatality rates were also higher among patients with Shigella infection, which was more frequently associated with malnutrition than was infection from other pathogens (Islam and Shahid, 1986). Deaths in patients with shigellosis also correlate with bacteremia in hospitalized patients; deaths were caused by either the infecting pathogen itself or other gram-negative organisms (Struelens et al., 1985). Bacteremia is, in turn, associated with age (patients who are less than 1 year of age), weaning, and nutritional status. Finally, a close relationship between mortality during an episode of diarrhea and nutritional state on admission, as assessed by MUAC, has been shown in Bangladeshi children (Briend et al., 1986). IMMUNOLOGICAL CONSEQUENCES OF MALNUTRITION Nutritional factors are known to affect immunologic function. Several reviews have documented and evaluated published data (Chandra and Newberne, 1977; Keusch and Farthing, 1986; Keusch et al., 1983; Watson, 1984). While the mechanisms and specific nutritional causes are not yet

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation clear, there is general agreement that single or multiple deficits in immune function do occur in malnourished hosts. Moreover, a consistent pattern of immunologic defects is found in the malnourished subjects, including depressed cell-mediated immunity, as indicated by anergy to delayed-type hypersensitivity antigens in vivo; a reduction in the number of circulating T lymphocytes and impaired in vitro responses to mitogens and specific antigens; diminished activity of the serum complement system, particularly activation via the alternative pathway; and a reduction in the mucosal secretory immunoglobulin A (sIgA) concentration and specific antibody activity. These various functional alterations are associated with maturational arrest of T cells at the level of the thymus gland, increased in vivo degradation and reduced synthesis of serum complement, and impaired production of sIgA. Defects in cell-mediated and/or mucosal immunity could have important effects on host susceptibility to diarrheal disease pathogens. A direct relationship between skin test reactivity to a panel of antigens and the subsequent morbidity from diarrheal diseases in malnourished Bangladeshi children has been reported by Koster et al. (1987). Nutritional deficits without anergy did not explain any of the variance not attributable to malnutrition with anergy. THE CONTRIBUTION OF DIARRHEA TO MALNUTRITION It is not difficult to demonstrate that infections cause a deterioration in nutritional status. Mata (1978) carried out prospective studies of growth and disease in a cohort of Mayan Indian children who were studied intensively from birth to 3 years of age. Diarrheal diseases were very frequent and were strongly associated with diminished food intake and growth faltering. Using similar methods Mata (1980) found that in comparison, the Guaymi Indians in Costa Rica, who consumed a diet similar to that of the Mayans that was inadequate in energy and protein, had lower morbidity rates due to diarrhea and better growth. Other field studies support the contention that infection exerts a significant negative influence on nutritional status. For example, Rowland et al. (1977) found that diarrheal disease in The Gambia, West Africa, is the major cause of growth retardation in young children, resulting in a 50 percent decrease in expected monthly weight gain during the first few years of life. Diarrhea prevalence was associated with a significant decrement in both linear growth and weight gain. Rowland and colleagues calculated that if diarrhea had not been present, the children would have grown at a velocity equivalent to that of the NCHS reference population. Black et al. (1984a) also found a similar decrease in expected weight gain (34 percent) in

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Bangladeshi infants during periods of high diarrheal disease prevalence. The magnitude of the growth faltering associated with diarrhea is variable and may depend on the age of the individual, the season, the etiologic agent, dietary intake, and food preparation and feeding practices. Such factors may vary from place to place. Thus, a significant effect of age was noted by Martorell et al. (1975) in Guatemala, but not by Rowland et al. (1977) in The Gambia. Rowland et al. (1977) also reported that the effect of diarrhea on weight gain was least apparent during the months of highest diarrheal disease prevalence, when all children grew poorly, regardless of the presence of diarrhea. These observations suggest that other seasonal factors have a greater adverse influence on growth than diarrheal disease does. HUMAN MILK AND DIARRHEAL DISEASES Comparisons of morbidity between human milk-fed and formula-fed infants have demonstrated that there are significantly fewer or less severe illnesses in breastfed infants (Cunningham, 1979; Duffy et al., 1986; Grulee et al., 1934; Mata et al., 1967; Woodbury, 1922), and a few studies have found no differences (Adebonojo, 1972; Fergusson et al., 1978; NRC, 1972), but no researchers have reported increases in morbidity among human milk-fed groups (Feachem and Koblinsky, 1984). Breastfeeding also protects against mortality (Briend et al., 1988; Victora et al., 1987). Most studies associate the lowest morbidities in those who are exclusively breastfed and the highest rates of illness in those who are completely weaned. Morbidity in partially breastfed infants lies between those extremes (Butz et al., 1984; Habicht et al., 1986). In one longitudinal study, estimates of the potential impact of exclusive breastfeeding on rates of diarrhea during the first 6 months of life showed that interventions that successfully motivate adoption of this feeding practice could dramatically reduce infant morbidity. Continued breastfeeding for more than 6 months, although not practiced exclusively, was still associated with reduced risk of illness. The protective effect of breastfeeding may be explained by reduced exposure to fecally contaminated foods and feeding utensils or by the anti-infective components of breast milk. Also, growth factors that are present in human milk may hasten intestinal mucosal renewal and recovery from enteric infections. The benefit provided by breastfeeding was of greater magnitude for diarrheal prevalence than for incidence (Brown et al., 1989). This suggests that breastfeeding not only lessens the risk of new illnesses but also shortens the duration of those illnesses that occur. This phenomenon might be explained by the ingestion of a smaller infectious dose of pathogens by more

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation intensively breastfed infants, by more rapid recovery from the infection, or by reduced infection-induced malabsorption and secondary diarrhea. In one clinical study, stool volume was reduced among breastfed infants with diarrhea compared with that among infants whose breastfeeding was discontinued during the early phase of therapy; these observations suggest that breast milk itself may reduce the severity of illness and hasten recovery (Khin-Maung-U et al., 1985). Nonetheless, data presented in favor of human milk's direct protective effects are disputed because of confounding environmental and demographic variables that are difficult to control (Bauchner et al., 1986; Habicht et al., 1986), e.g., the degree of preventable contamination of other infant foods, the number of caretakers with whom the index child has contact, and the behavioral characteristics of the caretaker. Each of these variables is a potential determinant of morbidity. Protective Factors in Human Milk Three mechanisms have been proposed by which human milk constituents directly protect the infant from infection. Two are based on the immunologic factors in human milk, and the third is based on human milk's high nutritive value. The relative protective contributions of human milk's immunologic and nutrient constituents are difficult to estimate. Potentially protective proteins in human milk can be classified into antigen-specific and non-antigen-specific agents. They have been the subject of numerous reviews (Goldman and Goldblum, 1985; Welsh and May, 1979). The major functioning important whey proteins are lactoferrin and sIgA. Lactoferrin is a non-antigen-specific factor. It binds iron avidly, and thereby presumably limits iron availability to bacteria (Griffiths and Humphreys, 1977). Lactoferrin may also modulate inflammatory responses by inhibiting complement (Goldman et al., 1986), and has been reported to act synergistically with sIgA to enhance the antibacterial effects of peroxidase (Moldoveanu et al., 1982). Secretory IgA is the major antigen-specific component in human milk Specific activity against a wide array of enteric and respiratory bacterial and viral pathogens is found in human milk (Goldman and Goldblum, 1995). The attachment of sIgA to the glycocalyx of epithelial cells in the microvilli of the small intestine may block the attachment to the intestinal tract by infectious agents (Nagura et al., 1978). The concentrations of most immunologically active proteins appear to fall after the first 2 or 3 months of lactation and subsequently either rise (e.g., lysozyme) or remain stable

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation (e.g., lactoferrin and sIgA). Immunoprotein concentrations generally rise or remain constant after the onset of gradual weaning (Goldman et al., 1983). Growth factors also have been identified in human milk (Klagsbrun, 1978; Moran et al., 1983). These factors may promote the maturation of the infant's gastrointestinal epithelium, and thereby augment mucosal barriers against the penetration of the gastrointestinal tract by antigens. The relationships among breastfeeding, specific anti-pathogen activities in human milk, and specific enteric illnesses have not been examined completely. Breastfeeding appears to ameliorate shigellosis (Mata et al., 1967). Although the evidence is mixed, rotaviral diarrhea appears to be milder in breastfed infants, and not all anti-rotaviral activity is associated with specific antigenic properties (Duffy et al., 1986). Cholera and infections with Giardia lamblia are less likely in infants of women with high titers of specific sIgA in their milk (Glass et al., 1983; Nayak et al., 1987). Lactation Performance The enhancement of lactation performance is expected to minimize the need for supplementary foods to meet the nutrient requirements of infants and to maximize the protection afforded in the practice of breastfeeding and the immunologic constituents of human milk. Lactation performance is defined from measurements of the quality and volume of milk that is produced, the duration of adequate milk production, and/or infant growth. Available studies suggest that milk volume is more sensitive to maternal nutritional status than is milk composition (Garza and Butte, 1985). Most studies have focused on total nitrogen, lactose, and fat. Few studies have measured micronutrients in milk produced by women whose nutritional status has been documented carefully (Lönnerdal, 1986). Nonbehavioral maternal and environmental factors that may influence the duration of lactation also have received limited attention. Generally, the fatty acid composition and the concentrations of the fat-and water-soluble vitamins of milk are affected most by diet. Protein concentrations are influenced by selected dietary conditions, but the effects appear to be relatively limited. Lactose, mineral, trace element, and electrolyte concentrations appear to be relatively resistant to wide variations in maternal intakes.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Effects of Maternal Nutritional Status on Lactation Performance A relationship between maternal nutritional status and lactation performance has been demonstrated among poorly nourished women. Longitudinal studies of poorly nourished, lactating Bangladeshi mothers from an underprivileged, periurban community demonstrated that average milk production and fat and energy concentrations in milk were similar to those described for well-nourished women. Fat and energy concentrations in milk and the amounts produced per day were greater in women with larger triceps skinfold thickness, or arm circumference; and increases in body weight were associated with increases in the amounts of milk and all macronutrients produced. Milk production, however, declined significantly before the major harvest period, when food was least available (Brown et al., 1986). Manjrekar et al. (1985) found that women who consumed 1,100 to 1,500 kcal/day produced insufficient volumes of milk within the first 4 months of lactation. Women who delivered low-birthweight infants produced insufficient milk volumes by 2 months postpartum. This and other similar studies, however, are complicated by the early return of women to work outside the home whereby the frequency of breastfeeding must be reduced or breastfeeding must be stopped entirely. The effects on lactation performance of superimposing high levels of activity on a woman with a marginal nutritional status were investigated in The Gambia. Breast milk composition remained relatively stable through an periods of the year, but breast milk output was minimal during the farming season, when activity was highest. Reductions in milk output of up to 10 percent were observed in mothers 3 to 12 months postpartum who kept their infants with them while they worked outside the home; reductions of 25 percent were seen in mothers who were separated from their older infants during the work day (Roberts et al., 1982). Impaired lactation performance may result from heightened activity, shortfalls in nutrient intakes during periods of intense work, or maternal and infant separation. In well-nourished women with Western life-styles, successful lactation is compatible with gradual weight reduction and energy intakes of approximately 2,200 kcal/day. The mother's dietary protein, carbohydrate, and fat intake apparently has no detectable impact on milk quantity. Milk fat composition is influenced by dietary fat. Most studies of well-nourished women report no significant interactions between milk quantity and quality and maternal weight, height, metabolic size, body surface area, change in body fat, prepregnancy weight, and weight gain during pregnancy (Butte et al., 1984b).

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Effects of Food Supplementation, on Lactation Performance Several studies have examined the effects of food supplementation on lactation performance (Forsum and Lönnerdal, 1980; Girija et al., 1984; Gopalan, 1958). The body of information neither supports nor refutes a positive effect from this type of intervention. Failure to control complex intervening variables in supplemental trials accounts substantially for the present state of knowledge. Variations in the degree of malnutrition or undernutrition, differences in the quantity and quality of the supplement used, the difficulty in measuring compliance, the possibility that the supplement is used to replace rather than augment dietary intake, and the wide variability in protocols make available studies difficult to evaluate. In studies conducted in India, women with baseline diets of 1,700 kcal/day and 40 g of protein/day were provided food supplements that contributed an added 30 g of protein and 417 kcal/day. Differences in the milk yield of supplemented and unsupplemented women were noted, but only from the third month postpartum on. After that time, the supplemented group produced 30 percent more milk than control women (Girija et al., 1984). Studies in animals also have shown a positive influence of supplements during lactation. Not all studies, however, have concluded that improvements in maternal intakes lead to enhanced milk production. In studies of Gambian women with baseline diets of approximately 1,600 kcal/day, approximately 700 kcal/day was added to the diet. No changes in milk production were detected (Prentice et al., 1983) in supplemented groups. Data from protein supplementation trials published by Edozien et al. (1976), Forsum and Lönnerdal (1980), and Gopalan (1958) suggest that protein supplementation increases milk volume. The specificity of protein for increasing milk volume, however, is not certain. Gopalan (1958) attempted to control one confounding variable, energy intake. Energy consumption was maintained at 2,900 kcal/day both before and after protein supplementation. A positive effect on milk volume was reported with protein supplementation. Manipulation of Immunologic Protein Factors in Human Milk Maternal nutritional status appears to influence the concentrations and total amounts of immunologically active proteins produced in human milk, but available data are inconsistent. Some studies report decreases in the concentrations of immunological protein in the milk of undernourished women (Miranda et al., 1983), whereas others find no differences between

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation such women and control women (Cruz et al., 1982). Nevertheless, the significant reductions in milk volume that are expected with maternal undernutrition would reduce the protective effects of human milk if the efficacy of immunological proteins is dose-related. No effective means of enhancing the concentrations of nonspecific protective components in human milk have been identified. While the specificity of sIgA in human milk depends on the mother's antigenic exposure, the mechanism responsible for the presence of specific sIgA in human milk is understood only partially, and a successful strategy for the enhancement of specific sIgA levels directed against enteric pathogens has not been demonstrated in humans. WEANING FOODS Following the period during which exclusive breastfeeding can support adequate growth, improvement in the nutritional status of target populations through feeding interventions requires the timely introduction of nutritious complementary foods and improved dietary therapy of common childhood illnesses. Planning each of these interventions requires, in turn, knowledge of locally available foods; the nutritional content and quality of these foods; and the social, economic, cultural, and seasonal constraints to their appropriate use under different circumstances. Nutrient Composition of Common Foods The nutrient compositions of foods can be measured by standard analytic techniques and are usually expressed per unit weight of raw edible portions. Although the data base for food composition is constantly expanding, information is currently available primarily for macronutrients (protein, fat, and carbohydrate), total metabolizable energy (''calories''), and selected vitamins and minerals (Rand, 1985). Additional tables of amino acid content, carbohydrate profiles (sugars, starches, and nonstarch polysaccharides or fiber), fatty acid composition, and trace element concentrations of limited numbers of foods are also becoming available or are under development. Food composition tables have been prepared for different regions of the world. These composition tables consider locally available and commonly consumed products. Unfortunately only small numbers of samples have been analyzed for each type of food, and it has been found that the nutrient compositions of individual foods vary greatly. Thus, food composition tables—although

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation indispensable for planning diets—provide fairly crude guidelines of the actual amounts of nutrients consumed (Cameron and Hofvander, 1983). The major nutrient sources are (1) the staple foods, which provide the majority of energy and protein as well as some vitamins and minerals; (2) fruits and vegetables, which are important additional sources of vitamins and minerals; (3) animal products, which can supplement the amount and quality of dietary protein, specific vitamins, and minerals; and (4) fats, oils, and sugars, which can enhance the energy density of mixed diets. The staple foods include cereals, such as wheat, rice, maize, and millet; roots and tubers, such as white potatoes, sweet potatoes, yams, and cassavas; and pulses or legumes, such as peas, beans, and groundnuts. Cereals are composed mostly of carbohydrate (primarily starch and nonstarch polysaccharides), protein (at a level between 6 and 14 percent of dry weight), and little fat. Nutrients are not distributed equally throughout the anatomic structures of grains, so the final nutrient composition of a cereal product depends on the degree of milling and other types of food processing (see Chapter 5). The outer layers of the grain contain relatively higher concentrations of protein, vitamins, and fiber, whereas the endosperm is generally higher in starch. The germ is relatively rich in protein, fat, and some vitamins. The water-soluble vitamins of the husk can be partially transferred to the endosperm by parboiling, which also improves the storage characteristics of the grain. Cereals are important quantitative sources of protein, but their protein quality is limited by the inadequate content of selected essential amino acids (WHO, 1985). Tubers, like cereals, have a high starch content and may contain reasonably good levels of protein. However, the water content of unprocessed roots and tubers is substantially greater than that for cereals. While the concentration of nutrients per unit of raw weight of tubers is lower than that for cereals, the ratio of protein to energy for some tubers, such as white potatoes, may be similar to that for some cereals. On the other hand, cassava is very low in protein, and the limited amount of protein it contains is of poor quality. Unlike the cereals, fresh tubers contain sizable quantities of ascorbic acid. Legumes are rich in protein and starch and can be good sources of calcium, iron, and B vitamins. Some (e.g., soybean and groundnuts) are excellent sources of edible oils. Although dry legumes contain between 20 and 40 percent protein, the digestibility and quality of the protein can be restricted, respectively, by the presence of protease inhibitors and by a relative deficiency of the essential amino acid methionine. However, the relative excess of lysine in legumes makes them excellent complementary protein sources for the cereals, which in turn can compensate for the inadequate levels of methionine in the legumes (Bressani, 1977). Thus, if

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation sufficient amounts of legumes are provided to overcome the reduced digestibility of vegetable diets, appropriate mixtures of these vegetable protein sources can yield diets with a protein quality that is indistinguishable from that of reference animal protein. Fruits and vegetables are primarily valued as sources of vitamins and minerals. Dark pigmented fruits and vegetables are major sources of vitamin A precursors and provide ascorbic acid, folic acid, other B vitamins, iron, and other minerals. Dairy products contain readily digestible protein of excellent quality and are rich in calcium and vitamins. Animal products are the only food source of vitamin B12. These foods tend to be expensive, and they often contain lactose, which may not be well tolerated in amounts greater than 1 g/kg per feeding when provided as the sole source of nutrients for children with diarrhea. However, milk is generally well tolerated when mixed in small amounts with staple foods, even by children with diarrhea and by children with clinical evidence of lactose malabsorption (Brown et al., 1980). Because only small amounts of these products are required to improve protein quality and content of the diet, the issue of cost and lactose intolerance may not be an important limiting factor for their use in a mixed diet. Because the bulkiness of the diet may limit the amounts of nutrients that are consumed, separated fats and oils that contain high amounts of energy per unit volume can make a valuable contribution to the diet. Likewise, sugars can be considered dense in energy since they can enter into solution, thereby adding energy to liquid or semiliquid diets without increasing their volume. Current recommendations to lower the consumption of fat and cholesterol to reduce the risk of cardiovascular disease is of little concern to most people in developing countries, where the intakes of fats and animal products are extremely low after the period of weaning. When fat intakes beyond infancy are greater than 30 percent of dietary energy and a substantial proportion of the fat is provided by saturated fatty acids (as in animal fats, coconut oil, and palm oil), some consideration of the possible cardiovascular risk is warranted. Bioavailability of Nutrients The quality of the mixed diet is a function of the nutrient content of the diet and the bioavailability of its nutrients. The bioavailability of nutrients, which can be defined simply as the efficiency of absorption and utilization or retention of the nutrients that are present in food, can vary substantially and has often not been well characterized. It is determined in part by nutrient content, food processing, the physiological status of the host,

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation interactions among components of. the mixed diet, and the presence of antinutritional factors. The effects of food processing techniques on nutrient bioavailability and on microbial contamination are discussed in more detail in Chapter 5. NUTRIENT REQUIREMENTS OF INFANTS AND YOUNG CHILDREN Age-specific nutrient requirements and recommended intakes or allowances are published by national and international authorities (WHO, 1985; NRC, 1980). Recommended allowances of all nutrients except energy are calculated by estimating average population requirements and by adding a quantity to account for individual variability and bioavailability from usual food sources. Recommended intakes of energy usually are calculated by a factorial approach, which is the sum of average estimates of the needs for maintenance, growth, and activity. Nutrient needs during periods of catch-up growth (5–8 kcal and approximately 0.4 g of protein per gram of desired gain of lean body mass) are reasonable supplements to baseline requirements if accelerated growth is desirable during illness-free intervals (NRC, 1985). Estimates of energy intake for a range of weight gains during convalescence have been published (NRC, 1985). The recommended intakes of most micronutrients are likely sufficient for adequate growth unless micronutrient deficiency states are present. Estimates of nutrient needs calculated from recommended levels of intake, however, should not be used by themselves as a target of strategies to ameliorate or prevent enteric disease. Rather, the morbidity and growth response of the child should be used to monitor the adequacy of general food safety and dietary intake. Until recently, little information has been available regarding the relationship between growth during infancy and the normal volumes and composition of human milk consumed in the first 4 to 6 months of life by breastfed infants (Butte et al., 1984b; Chandra, 1981; Dewey and Lönnerdal, 1982; Picianno et al., 1981). This has prevented the resolution of apparent discrepancies between the projected volumes of milk required to meet energy and protein requirements estimated by factorial approaches and the volumes of milk consumed by apparently healthy infants (Waterlow and Thomson, 1979). With few exceptions, the milk intake of infants of well-nourished women range from 600 to 900 ml/day. Well-nourished, breastfed infants consume approximately 100 to 120 kcal/kg during the first month of life; their energy intakes decrease to approximately 70 to 90 kcal/kg by the fourth month and appear to remain at that level for at least 8 to 9 months,

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation even after solid foods are added to their diet. Those energy intakes appear to be substantially lower than the intakes of formula-fed infants (Fomon et al., 1971; Montandon et al., 1986). Most recent studies of infants who live in favorable environments indicate that the exclusively breastfed infant's weight-for-age, weight-for-length, and less frequently, length-for-age percentiles demonstrate statistically significant negative trends after the third month of postnatal life (Butte et al., 1984a; Garza et al., 1987; Hitchcock et al., 1985). Generally, cohorts of breastfed infants appear to gain weight during the first 2 to 3 months of life at a more rapid rate than is expected on the basis of the NCHS reference population. In later months infants appear to reduce the rate of weight gain relative to that of the reference population, even when supplementary foods are available ad libitum. Although such trends commonly are not sufficiently severe in economically developed countries to arouse clinical concern, they support the view that human milk may become limiting by the third or fourth month of life (Waterlow and Thomson, 1979). That conclusion, however, is based on the acceptance of NCHS growth curves as normative standards, despite their derivation from observations of infants who were principally formula-fed. The general persistence of negative trends in growth percentiles of breastfed infants whose diets are supplemented ad libitum with solid foods and who live in favorable environments suggests that NCHS growth curves may not be appropriate and that as a result health practitioners may identify growth faltering prematurely. An important caveat in this discussion is that there are no convincing data to show that infants in areas with high endemic rates of enteric infections can maintain comparable rates of growth as their counterparts in more privileged environments, when both groups of infants consume similar amounts of human milk. If the effects of unsanitary environments on infant health are to be compensated for by specific human milk constituents, infants must provide sufficient stimulation to the breast to increase milk production when needed, and the mammary glands' response to the infant and the environment must be timely. Failure by either mother or infant may result in progressive nutrient deficits. Most data from economically developing countries indicate that milk volumes and contents are similar or lower than those observed in economically developed settings (Brown et al., 1986; Jelliffe and Jelliffe, 1978; Prentice et al., 1983). SUMMARY The nutritional state of the host and susceptibility to infection are interrelated in the broadest sense. Most of the clinical and epidemiological

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation studies reviewed indicate that malnutrition is a bona fide risk factor for diarrheal disease, affecting one or more key parameters including incidence, duration, and severity of illness. One mechanism for this is impaired immune function secondary to malnutrition; however, poverty, inadequate food availability or kinds of food, and increased transmission of pathogens can each have major affects. Whether or not nutrient losses as a result of infection become clinically manifest depends on the individual's nutritional status at the outset of infection, the duration and severity of the infection, and the availability of energy-dense and high-quality foods during convalescence. If the individual is well nourished initially, the illness is short, and appropriate foods are available, catch-up growth during convalescence can be rapid and the impact of the infection may not be detectable. These conditions are rarely present in developing countries. Breastfeeding is also protective. Three mechanisms have been proposed by which human milk constituents protect the infant from infection. Two are based on immunologic factors in human milk and the third is the high nutrient value of human milk. The practice of breastfeeding provides a fourth mechanism, as it decreases exposure to potential pathogens. Weaning foods consist of mixtures of ingredients formulated to supplement the nutrients from human milk. They must be calorie-and nutrient-dense and preferably formulated on the basis of the nutrient content and bioavailability of locally available foods. Age-specific nutrient recommendations made by national and international health agencies are useful guides for planning diets (WHO, 1985; NRC, 1980). Allowances for catch-up growth also are available in a separately published report (NRC, 1985). Neither standard, however, is a substitute for growth and gastrointestinal morbidity as an index of the nutrient adequacy and safety of the diet. The appropriateness of accepted references for the assessment of growth in breastfed infants is difficult to evaluate. Relationships among growth, intakes of human milk, and milk composition require improved definition in breastfed infants who live in areas with high endemic rates of enteric infections. Available studies suggest that maternal nutritional status influences the volume of milk that is produced and may influence its composition. Assessments of the effects of maternal supplementation on lactation performance, however, neither support nor refute a positive effect of this type of intervention. The few studies that have assessed the impact of protein supplements suggest that milk volume may be increased by increments in protein intake. The effects of maternal-infant separation and varying degrees of physical activity among women complicate the interpretation of available data. No effective strategies for enhancing the immunologic

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation content of milk as a means of enhancing human milk's protective effects have been described. The enhancement of lactation performance is expected to benefit gastrointestinal morbidity in infants. REFERENCES Adebonojo, F.O. 1972. Artificial versus breastfeeding: Relation to infant health in a middle class American community. Clin. Pediatr. 11:25–29. Bairagi, R., M.K. Chowdhury, Y.J. Kim, G.T. Curlin, and R.H. Gray. 1987. The association between malnutrition and diarrhoea in rural Bangladesh. Int. J. Epidemiol. 16:477–481. Bauchner, H., J.M. Leventhal, and E.D. Shapiro. 1986. Studies of breastfeeding and infections. How good is the evidence? J. Am. Med. Assoc. 256:887–892. Beisel, W.R. 1977. Magnitude of the host nutritional responses to infection. Am. J. Clin. Nutr. 30:1236–1247. Bhan, M.K., N.K. Arora, O.P. Ghai, K. Ramachandran, V. Khoshoo, and N. Bhandari. 1986. Major factors in diarrhoea related mortality among rural children. Indian J. Med. Res. 83:9–12. Black, R.E., K.H. Brown, and S. Becker. 1984a. Effects of diarrhea associated with specific enteropathogens on the growth of children in rural Bangladesh. Pediatr. 73:799–805. Black, R.E., K.H. Brown, and S. Becker. 1984b. Malnutrition is a determining factor in diarrheal duration, but not incidence, among young children in a longitudinal study in rural Bangladesh. Am. J. Clin. Nutr. 39:87–94. Bressani, R. 1977. Protein supplementation and complementation. Pp. 204–232 in C.E. Bodwell, ed. Evaluation of Proteins for Humans. Avi Publishing Co., Westport, Conn. Briend, A., C. Dykewicz, R.N. Mazunder, B. Wojtyniak, M. Bennish, and K. Graven. 1986. Usefulness of nutritional indices and classifications in predicting death of malnourished children. Br. Med. J. 293:373–375. Briend, A., B. Wojtyniak, and M.G.M. Rowland. 1987. Arm circumference and other factors in children at high risk of death in rural Bangladesh. Lancet 2:725–728. Briend, A., B. Wojtyniak, and M.G.M. Rowland. 1988. Breastfeeding, nutritional state, and child survival in rural Bangladesh. Br. Med. J. 296:879–882. Brown, K.H., R.E. Black, and L. Parry. 1980. The effect of acute diarrhea on the incidence of lactose malabsorption among Bangladeshi children. Am. J. Clin. Nutr. 33:2226–2227. Brown, K.H., N.A. Akhtar, A.D. Robertson, and M.G. Ahmed. 1986. Lactational capacity of marginally nourished mothers: Relationships between maternal nutritional status and quantity and proximate composition of milk. Pediatr. 78:909–919. Brown, K.H, R.E. Black, G. Lopez de Romaña, and H. Creed de Kanashiro. 1989. Infant-feeding practices and their relationship with diarrheal and other diseases in Huascar (Lima), Peru. Pediatr. 83:31–40. Butte, N.F., R.M. Goldblum, L.M. Fehl, K. Loftin, E.O. Smith, C. Garza, and A.S. Goldman. 1984a. Daily ingestion of immunologic components in human milk during the first four months of life. Acta Paediatr. Scand. 73:296–301. Butte, N.F., C. Garza, E.O. Smith, and B.L. Nichols. 1984b. Human milk intake and growth performance of exclusively breastfed infants. J. Pediatr. 104:187–195. Butz, W.P., J.P. Habicht, and J. DeVanzo. 1984. Environmental factors in the relationship between breastfeeding and infant mortality: The role of sanitation and water in Malaysia. Am. J. Epidemiol. 119:516–525. Cameron, M., and Y. Hofvander. 1993. Manual on Feeding Infants and Young Children, 3rd ed. Oxford University Press, Oxford. 214 pp.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Chandra, R.K. 1991. Breastfeeding, growth, and morbidity. Nutr. Res. 1:25–31. Chandra, R.K., and P.M. Newberne. 1977. Nutrition, Immunity, and Infection: Mechanism Interactions. Plenum Press, New York. 246 pp. Chen, L.C., A.K.M.A. Chowdhury, and S.L. Huffman. 1980. Anthropometric assessment of energy-protein malnutrition and subsequent risk of mortality among preschool aged children. Am. J. Clin. Nutr. 33:1836–1845. Cruz, J.R., B. Carisson, B. García, M. Gebre-Medhin, V. Hofjander, J.J. Urrutia, and L.A. Hanson. 1982 Studies on human milk III. Secretory IgA quantity and antibody levels against Escherichia coli in colostrum and milk from underprivileged and privileged mothers. Pediatr. Res. 16:272–276. Cunningham, A.S. 1979. Morbidity in breastfed and artificially fed infants, II. J. Pediatr. 95:685–689. Dewey, K.G., and B. Lönnerdal. 1982. Nutrition, growth, and fatness of breast-fed infants from one to six months. Fed. Proc. (Abst. 486) 41:352 Duffy, L.C., T.E. Byers, M. Riepenhoff-Talty, L.J. La Scolea, M. Zielezny, and P. L. Ogra. 1986. The effects of infant feeding on rotavirus-induced gastroenteritis: A prospective study. Am. J. Publ. Health 76.259–263. Edozien, J.C., M.A.R. Khan, and C.I. Waslien. 1976. Human protein deficiency: Results of a Nigerian village study. J. Nutr. 106:312–328. Feachem, R.G. 1983. Interventions for the control of diarrhoeal diseases among young children: Supplementary feeding programmes . Bull. World Health Org. 61:967–979. Feachem, R.G., and M.A. Koblinsky. 1984. Interventions for the control of diarrhoeal diseases among young children: Promotion of breastfeeding. Bull. World Health Org. 62:271–291. Fergusson, D.M., L.J. Horwood, F.T. Shannon, and B. Taylor. 1979. Infant health and breastfeeding during the first 16 weeks of life. Aust. Pediatr. J. 14:254–258. Fomon, S.J., L.N. Thomas, L.J. Filer, E.E. Ziegler, and M.T. Leonard. 1971. Food consumption and growth of normal infants fed milk-based formulas. Acta Psediatr. Scand. (Suppl.) 223:1–29. Forsum, E., and B. Lönnerdal. 1980. Effect of protein intake on protein and nitrogen composition of breast milk. Am. J. Clin. Nutr. 33:1809–1813. Garza, C., and N.F. Butte. 1985. The effect of maternal nutrition on lactational performance. Pp. 15–36 in N. Kretchmer, ed. Frontiers in Clinical Nutrition. Aspen Press, Rockville, Md. 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. Girija, A., P. Geervani, and G.N. Rao. 1984. Influence of dietary supplementation during lactation on lactation performance. J. Trap. Pediatr. 30:140–144. Glass, R.I., A.M. Svennerholm, B.J. Stoll, M.R. Khan, K.M.B. Hossain, M.I. Huq, and J. Holmgren. 1993. Protection against cholera in breast-fed children by antibodies in breast milk. N. Engl. J. Med. 308:1389–1392. Goldman, A.S., and R.M. Goldblum. 1985. Protective properties of human milk. Pp. 819–928 in W.A. Walker and J.B. Watkins, eds. Nutrition in Pediatrics: Basic Science and Clinical Application. Little, Brown, and Co., Boston. Goldman, A.S., R.M. Goldblum, and C. Garza. 1983. Immunologic components in human milk during the second year of lactation . Acta Pediatr. Scand. 72:461–462. Goldman, A.S., L.W. Thorpe, R.M. Goldblum, and L.A. Hansan. 1986. Anti-inflamatory properties of human milk. Acta Pediatr. Scand. 75:689–695. Gopalan, C. 1958. Effect of protein supplementation and some so-called galactogogues on lactation of poor Indian women. Ind. J. Med. Res. 46:317–324.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Griffiths, E., and J. Humphreys. 1977. Bacteriostatic effect of human milk and bovine colostrum on Escherichia coli: Importance of bicarbonate. Infect. Immunol. 15:396–401. Grulee, C.G., H.N. Sanford, and P.H. Herron. 1934. Breast and artificial feeding: Influence on morbidity and mortality of twenty thousand infants. J. Am. Med. Assoc. 103:735–739. Guerrant, R.L., L.V. Kirchhoff, D.S. Shields, M.K. Nations, J. Leslie, M.A. de Sousa, J.G. Araujo, L.L. Correia, K.T. Sauer, K.E. McClelland, F.L. Trowbridge, and J.M. Hughes. 1983. Prospective study of diarrheal illnesses in Northeastern Brazil: Patterns of disease, nutritional impact, etiologies, and risk factors . J. Infect. Dis. 148:986–997. Habicht, J.P., J. DaVanze, and W.P. Butz. 1986. Does breastfeeding really save lives, or are apparent benefits due to biases? Am. J. Epidem. 123:279–290. 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. Islam, S.S., and N.S. Shahid. 1986. Morbidity and mortality in a diarrhoeal diseases hospital in Bangladesh. Trans. R. Soc. Trop. Mod. Hyg. 80:748–752. James, J.W. 1972. Longitudinal study of the morbidity of diarrheal and respiratory infections in malnourished children. Am. J. Clin. Nutr. 25:690–694. 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. Keusch, G.T., and M.J.G. Farthing. 1986. Nutrition and infection. Annu. Rev. Nutr. 6:131–154. Keusch, G.T., and N.S. Scrimshaw. 1986. Selective primary health care. Strategies for control of disease in the developing world. XXIII. Control of infection to reduce the prevalence of infantile and childhood malnutrition. Rev. Infect. Dis. 8:273–287. Keusch, G.T., C.S. Wilson, and S.D. Waksai. 1993. Nutrition, host defenses, and the lymphoid system. Pp. 275–359 in J.I. Gallin and A.S. Fauci, eds. Advances in Host Defense Mechanisms, Vol. 2. Lymphoid Cells. Raven Press, New York. Khin-Maung-U, Nyunt-Nyunt-Wai, Myo-Khin, Mu-Mu-Khin, Tin-U, and Thane-Toe. 1985. Effect on clinical outcome of breastfeeding during acute diarrhoea. Br. Med. J. 290:587–589. Kielmann, A.A., and C. McCord. 1978. Weight-for-age as an index of risk of death in children. Lancet 1:1247–1250. Kiagsbrun, M. 1978. Human milk stimulates DNA synthesis and cellular proliferation in cultured fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 75:5057–5061. Koster, F.T., D.L. Palmer, J. Chakraborty, T. Jackson, and G.C. Curlin. 1987. Cellular immune competence and diarrheal morbidity in malnourished Bangladeshi children: A prospective field study. Am. J. Clin. Nutr. 46:115–120. Lönnerdal, B. 1986. Effects of maternal dietary intake on human milk composition. J. Nutr. 116:499–513. Manjrekar, C., M.P. Vishalakshi, N.J. Begum, and G.N. Padma. 1995. Breastfeeding ability of undernourished mothers and physical development of their infants during 0–1 year. Indian Pediatr. 22:801–809. Martorell, R., J.P. Habicht, C. Yarbrough, A. Lechtig, R.E. Klein, and K.A. Western. 1975. Acute morbidity and physical growth in rural Guatemalan children. Am. J. Dis. Child. 129:1296–1301. Mata, L.J. 1978. The Children of Santa Maria Cauque: A Prospective Field Study of Health and Growth. MIT Press, Cambridge, Mass. 395 pp. Mata, L.J. 1980. Child malnutrition and deprivation-observations in Guatemala and Costa Rica. Food Nutr. 6:7–14. Mata, L.J., J.J. Urrutia, and J.E. Gordon. 1967. Diarrheal disease in a cohort of Guatemalan village children observed from birth to age two years. Trop. Geog. Med. 19:247–257.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Miranda, R., N.G. Saravia, R. Ackerman, N. Murphy, S. Berman, and D.N. McMurray. 1983. Effect of maternal nutritional status on immunological substances in human colostrum and milk. Am. J. Clin. Nutr. 37:632–640. Moldoveanu, Z., J. Tenovuo, J. Mestecky, and K.M. Pruitt. 1982 Human milk peroxidase as derived from milk leukocytes. Biochem. Biophys. Acta 718:103–108. Montandon, C.M., C.A. Wills, C. Garza, E.O. Smith, and B.L. Nichols. 1986. Formula intake of one-and four-mouth-old infants. J. Pediatr. Gastroenterol. Nutr. 5:434–438. Moran, J.R., M.E. Courtney, D.N. Orth, R. Vaugh, S. Coy, C.D. Mount, B.J. Sherrell, and H.L Greene. 1983. Epidermal growth factor in human milk: Daily production and diurnal variation during early lactation in mothers delivering at term and at premature gestation. J. Pediatr. 103:402–405. Nagura, H., P.K. Nakane, and W.R. Brown. 1978. Breast milk IgA binds to jejunal epithelium in suckling rats. J. Immunol. 120:1333–1339. Nayak, N., N.K. Ganguly, B.N.S. Walia, N. Wahi, S.S. Kanwar, and R.C. Mahajan. 1987. Specific secretory IgA in the milk of Gardia lamblia-infected and uninfected women. J. Infec. Dis. 155:724–727. NRC (National Research Council). 1972. Background Information on Lactose and Milk Intolerance. A statement of the Committee on International Nutrition Programs, Food and Nutrition Board, Division of Biology and Agriculture. National Academy of Sciences, Washington, D.C. NRC (National Research Council). 1980. Recommended Dietary Allowances, 9th ed. Report of the Committee on Dietary Allowances, Food and Nutrition Board, Division of Biological Sciences, Assembly of Life Sciences, National Academy of Sciences, Washington, D.C. NRC (National Research Council). 1985. Nutritional Management of Acute Diarrhea in Infants and Children. Subcommittee on International Nutrition Programs, Food and Nutrition Board, Commission on Life Sciences. National Academy Press, Washington, D.C. Picianno, M.F., E.J. Calkins, J.R. Garrick, and R.H. Deering. 1981. Milk and mineral intake of breastfed infants. Acta Paediatr. Scand. 70:189–194. Prentice, A.M., S.B. Roberts, A. Prentice, A.A. Paul, M. Watkinson, and R.G. Whitehead. 1983. Dietary supplementation of lactating Gambian women. I. Effect on breast milk volume and quality. Hum. Nutr. Clin. Nutr. 37C:53–64. Puffer, R.R., and C.V. Serrano. 1973. Patterns of Mortality in Childhood. Report of the Inter-American Investigation of Mortality in Childhood. Scientific Publication No. 262. Pan American Health Organization, Washington, D.C. 470 pp. Rand, W.M. 1985. Food composition data: Problems and plans. J. Am. Diet. Assoc. 85:1081–1083. Roberts, S.B., and W.A. Coward. 1985. The effects of lactation on the relationship between metabolic rate and ambient temperature in the rat. Ann. Nutr. Metab. 29:19–22. Roberts, S.B., A.A. Paul, T.J. Cole, and R.G. Whitehead. 1982. Seasonal changes in activity, birth weight and lactational performance in rural Gambian women . Trans. R. Soc. Trop. Med. Hyg. 76:668–678. Rowland, M.G.M., T.J. Cole, and R.G. Whitehead. 1977. A quantitative study into the role of infection in determining nutritional status in Gambian village children. Br. J. Nutr. 37:441–450. Samadi, A.R., A.I. Chowdhury, M.I. Hug, and N.S. Shahid. 1985. Risk factors for death in complicated diarrhoea of children. Br. Med. J. 290:1615–1617. Scrimshaw, N.S., C.E. Taylor, and J.E. Gordon. 1968. Interaction of Nutrition and Infection. Monograph Series No. 57. World Health Organization, Geneva. 329 pp. Sepulveda, J., W. Willett, and A. Munoz. 1988. Malnutrition and diarrhea. A longitudinal study among urban Mexican children. Am. J. Epidemiol. 127:365–376.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Struelens, M.J., D. Patte, I. Kabir, A. Salam, S.K. Nath, and T. Butler. 1985. Shigella septicemia: Prevalence, presentation, risk factors, and outcome . J. Infect. Dis. 152:784–790. Tomkins, A. 1981. Nutritional status and severity of diarrhoea among pre-school children in rural Nigeria. Lancet 7:860–862. Trowbridge, F.L., L.H. Newton, and C.C. Campbell. 1981. Nutritional status and severity of diarrhoea. Lancet 7:1375. Victora, C.G., P.G. Smith, J.P. Vaughan, L.C. Nobre, C. Lombardi, A.M.B. Teixeira, S.M.C Fuchs, L.B. Moreira, L.P. Gigante, and F.C Barrcs. 1987. Evidence for protection by breastfeeding against infant deaths from infectious diseases in Brazil. Lancet 2:319–322. Waterlow, J.C., and A.M. Thomson. 1979. Observations on the adequacy of breastfeeding. Lancet 2:138–142. Watson, R.R., ed. 1984. Nutrition, Disease Resistance, and Immune Function. Marcel Dekker, New York. 404 pp. Welsh, J.K., and J.T. May. 1979. Anti-infective properties of breast milk. J. Pediatr. 94:1–9. Woodbury, R.M. 1922. Relation between breast and artificial feeding and infant mortality. Am. J. Hyg. 2:668–687. WHO (World Health Organization). 1985. Energy and Protein Requirements. Report of a Joint FAO/WHO/UNO Expert Consultation. WHO Technical Report Series 724. World Health Organization, Geneva. 206 pp.

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