Contents - Previous - Next

This is the old United Nations University website. Visit the new site at http://unu.edu

The importance of dietary quality versus quantity for weanlings in less developed countries: a framework for discussion

Kenneth H. Brown

Abstract

Weanlings in less developed countries commonly grow more slowly than reference populations from industrialized societies. Although the functional implications of these different patterns of growth are not certain, it is generally believed that children's diets should permit full expression of their growth potential. To achieve this goal, the focus of public health nutrition programmes in less developed countries has evolved from an earlier emphasis on enhanced protein consumption to a current emphasis on increased energy intake. However, these programmes often neglect consideration of the quality of weanlings' diets and its potential importance for a variety of functional outcomes, including its relation to appetite and energy consumption. These issues are discussed in greater detail, and a conceptual framework is presented for the classification of different aspects of dietary quality.

Introduction

During the second half of infancy, when significant amounts of complementary foods are usually introduced into the diet in addition to breast milk, children in less developed countries are at greater risk of nutritional deficiencies and secondary functional disturbances than at any other time in postnatal life. During the weaning period these infants frequently consume less food energy and other nutrients, and display reduced linear and weight growth velocities compared with their counterparts in more affluent countries.

Despite recent advances in our understanding of the direct relationships among dietary intake, infectious diseases, and somatic growth of children in this age group, much remains unknown. For example, the specific factors that influence the amount of food consumed by weanlings in particular sociocultural and ecological contexts have not been well delineated. It is frequently assumed that nutritional inadequacies during the weaning period can be ascribed to one or more of the following three phenomena: insufficient food availability in the household, suboptimal child-feeding behaviours, and the frequent occurrence of infections, which may interfere with nutrient intake and utilization. However, compelling evidence exists that other factors may be at least as important. It is possible, for example, that inherent characteristics of the diet or of the child explain a substantial proportion of the observed differences in the amounts of food consumed.

Historical antecedents: From the protein gap to the energy gap

More than 50 years ago Cicely Williams first described kwashiorkor in Western medical literature [1]. With that report and the subsequent recognition of the role of protein in the aetiology of kwashiorkor, attention to the importance of dietary protein for children during the weaning period increased considerably. The United Nations agencies involved in nutrition programmes responded by creating the Protein Advisory Group, which was charged with the task of defining protein requirements and developing appropriate interventions to treat or prevent the presumed widespread deficiency.

Although these events had the positive effect of focusing global interest and resources on a nutritional-deficiency disease of the economically less developed world, broader appreciation of the "forest" of undernutrition may have been obscured by the "trees" of kwashiorkor. In a subsequent reaction to the perceived under-recognition of widespread food or energy deficiency, McLaren in 1974 published a strident essay in which he argued that food-consumption surveys, dietary-intake data, and the relative prevalences of marasmus and kwashiorkor all pointed to an energy gap rather than a protein gap [2]. This perspective was supported by subsequent analyses [3; 4].

Although McLaren's paper certainly fostered a more balanced appreciation of global nutritional problems, once again it appears that the nutrition pendulum may have swung too far from a scientifically valid centre of gravity. It now seems that recognition of the exaggerated programmatic responses to the problem of kwashiorkor may have resulted in an equivalent degree of overemphasis on food-energy production and consumption, and a corresponding disregard for the contents and bioavailability of macro- and micronutrients in common food sources. Regrettably, it now seems that nutrition-programme planners and nutrition scientists are frequently at odds in their assessment of priorities for nutrition policy. Programme planners often appear reluctant to accept the increasing complexity of nutrition science, with its overriding concern with the dietary requirements for multiple interacting nutrients, some of which are required in extremely small amounts. It is common, for example, to hear nutrition planners state - perhaps wishfully - that, if only enough food could be made available to children to satisfy their energy requirements, other nutrient needs would automatically take care of themselves. On the other hand, nutritionists often seem unwilling, or perhaps unable, to articulate the programmatically relevant aspects of their scientific advances in a manner that is readily understandable and realistically applicable.

At the same time that the protein-versus-energy controversy was unfolding, epidemiologists also began to recognize the importance of common childhood infections as determinants of nutritional status [5]. Indeed, some infectiousdisease specialists went so far as to claim that all undernutrition in the economically less developed world could be explained by the high rates of infection. Thus, a new and continuing controversy emerged, with debates centring on whether scarce resources for improved nutrition would be better invested in enhanced diets or in improved prevention of and nutritional therapy for infections.

Ideally, public health nutrition programmes should be designed to ameliorate identifiable nutritional problems of vulnerable populations or high-risk subgroups within those populations. If the assumptions regarding the causes of these nutritional problems are erroneous, the programmes themselves may be misguided. Because of the common aforementioned assumptions regarding the major causes of childhood malnutrition, nutrition intervention programmes have often understandably attempted to improve children's nutrition through increased food production and more equitable food distribution (with special targeting of high-risk regions, communities, households, and individuals), improved nutrition education regarding infant-feeding practices, and enhanced control and nutritional management of infectious diseases. If, however, inherent dietary and child factors are also critical determinants of total dietary intake and growth, it is conceivable that current programmatic efforts will be ineffective unless greater attention is simultaneously directed to improving the quality of the weaning diet and to treating the causes of poor appetite.

Examining the assumptions

If insufficient availability of food energy and high rates of infection are, indeed, the major limiting factors to improved nutritional status during the weaning period, the following propositions should also be true: (1) The nutrient densities of current weaning diets should be sufficient to supply the recommended dietary allowances of all nutrients when energy needs are satisfied. (2) The gastric capacity of children in this age range must be sufficient for adequate amounts of the traditional weaning diets to be consumed, given the usual feeding frequency that is observed and recognizing the time constraints of children's care givers, and infants must be willing to consume the additional required energy if given the opportunity. And (3) infections alone should explain a major proportion of observed growth faltering.

If infants eat more, will they satisfy their nutrient requirements?

If, as is frequently claimed, the amount of food consumed is the major constraint to achieving adequate nutrient intakes, the ratios of macro- and micro-nutrients to energy in selected weaning diets should be sufficient to satisfy nutrient requirements when enough energy is consumed to meet recommended levels of energy intake. To examine this assumption, we analysed quantitative dietary-intake data obtained by full-day observations of a cohort of infants in Huascar, a poor community on the outskirts of Lima, Peru. Our previous analyses showed that energy intake by these children during the second six months of life averaged between 70% and 75% of the amounts recommended for age by FAD/WHO [6]. Their weight and length growth velocities were substantially less than those of infants of international reference populations [7].

We expressed selected nutrient contents of these in fants' mixed diets in relation to the amounts of energy the diets contained. Only the non-breast-milk foods consumed by infants between 6 and 12 months of age were considered. Teas and sugar water were excluded because these generally provide carbohydrate energy but only trivial amounts of other nutrients. The data were analysed in two ways: including and excluding any non-human milk that may have been consumed, so that the importance of this milk could be examined independently.

FIG. 1. Dietary protein densities as cumulative proportion of child-days of observation - Huascar, Peru

FIG. 2. Dietary vitamin-A densities as cumulative proportion of child-days of observation

FIG. 3. Dietary calcium densities as cumulative proportion of child-days of observation

FIG. 4. Dietary iron densities as cumulative proportion of child-days of observation

The nutrient densities (amounts per 100 kcal) of the diets for selected nutrients that have been previously implicated as potentially important for linear or weight growth of children in less developed countries are presented in figures 15. The data are expressed as the cumulative proportion of child-days of observation during which the specified levels of nutrient density were provided by the mixture of non-breast-milk foods. The superimposed vertical lines indicate the theoretical nutrient densities that would be required for children one year old to receive their recommended dietary allowance of the respective nutrient [8] when they consume either 100% or 70% of the level of energy intake recommended by US National Research Council.

As may be seen in figure 1, during approximately 10% of days of observation the composite weaning food mixtures provided less than 1.6 g protein per 100 kcal, which is the protein density that is required to satisfy theoretical protein needs if 100% of the recommended amount of energy is consumed. (This does not take protein digestibility or amino acid balance into account.) However, the observed diets would supply insufficient protein approximately 25% of the time if only 70% of the recommended amount of energy were consumed. If the diets contained no milk, their protein densities would be unsatisfactory either 30% or 50% of the time, depending on the assumption regarding the total level of energy intake.

FIG. 5. Dietary zinc densities as cumulative proportion of child-days of observation

Similar calculations were made for the vitamin-A, calcium, iron, and zinc densities of the mixed diets. Figures 2-5 illustrate that the dietary densities of these micronutrients in the Huascar weaning diet were below the recommended levels during most days of observation. These analyses also demonstrate the tremendous nutritional advantage of including even small amounts of milk in the mixed diet, since milk was a major contributor of dietary protein and calcium and an important contributor of vitamin A and zinc.

In summary, the weaning diets currently consumed in this community would not be adequate sources of selected micronutrients believed to be important determinants of growth, even if energy were consumed at recommended levels. Similar results have been found for weaning foods in other parts of the world [9; 10]. Moreover, the present analyses may overestimate the adequacy of some of the micronutrients because they do not take into account the presumably poor bioavailability of the mineral components of the diet, which includes many phytate-containing plant sources. As discussed in more detail below, an early consequence of inadequate intake of specific nutrients may be a reduction in appetite and a subsequent decrease in energy consumption. Thus, suboptimal nutrient density in or availability from the diet may actually be the cause of inadequate energy intakes, rather than low food-energy intakes being the cause of micronutrient deficiencies. These observations suggest, then, that the quality of the weaning diet may be one of the factors limiting the dietary intake and growth of these children, and that the nutritional quality of the diet as well as the quantity of food-energy intake should be of concern in the formulation of nutrition policies and programmes affecting young children in the developing world.

TABLE 1. Factors potentially influencing total daily food energy intake by young children

Will weanlings eat more of their current diets if given the opportunity?

Factors that may influence the total food energy intake by young children are listed in table 1. In those areas of the world where household food security is tenuous, insufficient food availability may be a direct cause of low intakes. However, in much of the developing world, childhood undernutrition occurs in the same households where adults remain relatively well nourished. This suggests either that the available food is not distributed equitably or that particular characteristics of the feeding behaviours, the preparation or content of the diet, or the appetite of the child limit the child's intake.

Clinical studies are currently in progress in Peru to assess the functional gastric capacity and total daily ad libitum energy intake of children consuming semisolid diets of varied energy density. Preliminary data from these studies of non-breast-fed children whose body weights ranged between 4 and 9 kg suggest that the single-meal gastric capacity is at least 40 g per kilogram of body weight when a relatively dilute diet is consumed. Using this figure, it is possible to compute the minimum dietary energy density required to satisfy energy requirements for different frequencies of feeding (fig. 6). When children receive only three meals a day, which is the average for infants in Peru and in Nigeria (two sites where we have conducted direct observations of children's dietary intake), the energy density of the diet should be at least 80 kcal per 100 g to meet theoretical requirements. By contrast, the observed average energy density of mixed weaning diets in Peru is about 50 kcal per 100 g (H. Creed, unpublished data) and in Nigeria is less than 30 kcal per 100 g [11]. Thus, some combination of low feeding frequency and insufficient density of the weaning foods may restrict the total amounts consumed.

FIG. 6. Predicted maximal daily energy intake by dietary energy density and feeding frequency, assuming gastric capacity of 40 g per kilogram of body weight per feeding

If lack of food were the primary explanation for poor energy intake and secondary growth failure, it would be reasonable to expect that almost all the food that is offered to children would be consumed. During the previously mentioned Huascar studies, we measured not only the amounts of foods consumed but also the amounts offered. Thus we were able to assess whether the amount of food presented to the children during the second semester of life limited their intake. Surprisingly, on average only about two-thirds of the non-breast-milk energy served to the children was consumed. Similar results have been reported for older Mexican children [12].

When we compared children in the Huascar studies who became stunted during the period of observation with those whose growth increments were superior, we found that the former were offered greater amounts of non-breast-milk energy than the latter. Moreover, while the stunted children did eat a slightly greater proportion of the energy that was offered, children in both groups left a considerable amount of food unconsumed (table 2). These findings suggest that, at least in this area of Peru, factors in addition to household food availability affect total energy intake, even among undernourished children.

The incomplete consumption of available food may be explained by children's limited gastric capacity, as discussed above, by poor appetite, or by inappropriate composition or undesirable organoleptic prop erties of the diet. Surprisingly little research has been conducted on the factors that affect hunger, appetite, and satiety in children. Nevertheless, some studies do demonstrate that infants consume greater amounts of foods that are sweetened [13], although salt content does not influence consumption [14]. In any case, it is reasonable to suspect that modification of selected components of the weaning diet may affect the total amounts consumed. Although some authors have also suggested that the monotony of weaning diets may inhibit consumption [15], controlled studies using nutritionally complete diets and varied levels of diversity have yet to be undertaken in children. Also, recent investigations in east Africa and south India [16; 17] have suggested that the viscosity of the weaning diet may influence the amounts consumed. These interesting findings have to be confirmed with full-day observations in additional settings.

TABLE 2. Percentage of offered food energy consumed by stunted and non-stunted infants 6-12 months of age, Huascar, Peru

Values are means ± SD.

Stunted children also consumed 273 ± 170 kcal per day (= 38 ± 24 kcal per kilogram per day) from breast milk; and non-stunted children also consumed 366 ± 160 kcal per day (= 43 ± 19 kcal per kilogram per day) from breast milk.

a. Height for age al 12 months <= - 2Z (107 days of observation).
b. Height for age at 12 months > - 2Z (468 days of observation).

Interestingly, recent supplementation trials with single nutrients have found increased total dietary intake in some cases. For example, zinc supplementation of poor children in Denver, Colorado, USA, who showed some evidence of zinc deficiency resulted in a 40% greater increase in energy intake among boys who received zinc than among controls [18]. Similarly, some studies of iron supplementation of iron-deficient individuals suggest increased dietary intake or weight gain or both in response to additional iron intake [19; 20]. Whether these results indicate that the individual nutrients affect appetite directly or indirectly through changes in physical activity or rates of infection is not known.

Finally, the possible effects of infection on appetite and dietary intake must be considered. Although a number of studies have reported decreased dietary intake during common symptomatic childhood illnesses [21; 22], the cumulative impact of infection on growth is relatively small, as discussed below. Thus, the impact of infection-induced anorexia on children's growth may be less dramatic than the cumulative effect of poor daily dietary intake. Nevertheless, it is conceivable that subclinical infections, such as chronic parasitic infections or undiagnosed tuberculosis, may interfere with appetite over more prolonged periods. Again, it is surprising that these questions have not been studied more extensively. It would be useful, for example, to undertake studies of circulating cytokines such as cachectin, which influence appetite, in children with different levels of dietary intake and with various types of infections in less developed and industrialized countries.

TABLE 3. Estimated cumulative impact of diarrhoea on children's growth increments during longitudinal studies in less developed countries

a. Cumulative impact on weight gain was significant only for less than three months.
b. No effect of illness was identified in younger infants.

Breast-feeding status may also have important effects on appetite, although the complex interaction of nutritional, emotional, and behavioural factors related to breast-feeding make the limited number of available studies difficult to interpret. Breast milk provides substantial proportions of the total nutrient intakes of many weanlings in less developed countries well into the second and sometimes the third year of life [9; 10]. For this reason, continued breast-feeding for as long as possible is generally believed to contribute to the overall quality of the weaning diet. On the other hand, some evidence suggests that breast-feeding may inhibit the child's appetite for non-breast-milk foods [23; 24]. Additional information is necessary to assess the net effect of continued breast-feeding on nutrient intakes by older weanlings.

To what extent do infections alone affect growth?

A comprehensive review of the effects of infections on children's dietary intake and physical growth is beyond the scope of this review. Nevertheless, it would be inappropriate to discuss the relationships between the dietary intake and growth of weaning-aged children in less developed countries without considering the potential influence of infections. Many studies from all regions of the developing world have documented a significant negative relationship between infections and children's growth [25-30]. However, less attention has been directed to the magnitude of the nutritional impact of these infections and to possible factors that may modify this relationship.

A brief summary of some of the community-based studies that have attempted to quantify the impact of common childhood infections on children's growth is shown in table 3. In all of these studies, diarrhoea! diseases consistently had the greatest, and often the only, significant influence on growth. The effect was more consistently observed in relation to weight gain than to linear growth, and younger infants (who usually receive their recommended nutrient allowances primarily or exclusively from breast milk) seem to have been more resistant to the nutritional impact of infections. Of particular interest are several recent studies in which information on children's dietary intake is available together with the morbidity and growth data. In Colombia, for example, diarrhoea had no effect on the linear growth of children residing in villages that were participating in food supplementation programmes, whereas there was a significant negative relationship between diarrhoea and the growth of children in the non-supplemented control villages [31].

Statistical modelling of data from longitudinal studies in Bangladesh indicate that increasing dietary intake to recommended levels would be expected to produce a substantially greater impact on children's weight increments than complete eradication of diarrhoea [32]. Finally, recently completed analyses of the Huascar data suggest an interaction between the prevalence of diarrhoea and usual energy intake as determinants of weight gain (K. H. Brown, unpublished data). In other words, only those children habitually consuming lower levels of dietary energy (and presumably other nutrients) had significant negative relations between diarrhoea and weight-gain velocity. Thus, infections may be an important determinant of nutritional status only when the child's usual diet is suboptimal. These studies all suggest that the most appropriate programmatic approach to reduce the nutritional complications of infections might be the promotion of improvements in the basic quality and quantity of the weaning diet.

Aspects of dietary quality

Much of the foregoing discussion argues for a reemphasis on the importance of dietary quality as well as quantity for weanlings in less developed countries. However, a critical discussion of issues of dietary quality and quantity requires the existence of relevant vocabulary and units of measurement for these aspects of the diet. Whereas the concept of dietary quantity usually refers to the total amount of food or food energy, which can be measured as total grams of weight or kilocalories of energy respectively, that is either offered or consumed, dietary quality remains rather vaguely defined and is often difficult to measure. Among the specific characteristics of the diet that may be included in definitions of dietary quality are the following (when logical units of measurement of these factors are available, they are also noted):

- energy density (kcal/100 g),
- macro- and micronutrient density (amount/ 1,000 kcal),
- digestibility, bioavailability (amount absorbed, retained/amount ingested),
- proportion of energy, protein from animal sources (energy derived from animal sources/total energy),
- diversity of diet (unit of measurement?),
- absence of antinutritional factors,
- appropriate organoleptic characteristics for age.

Nutrient density and bioavailability are probably the factors most commonly considered as major indicators of dietary quality. The former is relatively easy to measure (assuming that one accepts results of dietary intake studies and food composition databases), whereas the latter is difficult to quantify for most nutrients in mixed diets. Attempts are currently being made to assess specific aspects of the diet, however, such as proportion of energy from animal or dairy sources, as proxies for the bioavailability of selected nutrients. Whether these indicators will be satisfactory for practical application remains to be determined.

Increased diversity of the diet has often been assumed to improve the quality of the diet. Obviously, this would be true only when the additional food sources provide a broader range of easily digestible nutrients than the basic staple diet. Little information exists on the relations between dietary diversity and dietary quality for weanlings in less developed countries; and, indeed, there is no commonly agreed-upon unit of measurement of diversity by which to evaluate these diets. These are research issues that deserve greater attention.

Other food components that may influence the quality of the diet include antinutritional factors that interfere with digestive enzymes or vitamin activity. The presence of these factors is often modified by traditional or modern foodprocessing techniques such as milling, toasting, fermentation, and others. Thus, dietary quality is not only an inherent characteristic of the foods present in the diet but may also be affected by the processing and cooking techniques employed. Again, the uncertain quantitative effects of these substances and processing techniques on the nutritional adequacy of the diet make assessment of dietary quality particularly difficult. Thus, despite increasing recognition of the importance of the quality of the diet, the current state of nutrition science does not permit a simple way to assess it. We are left, then, to evaluate each of these aspects of the diet separately, often with measurement techniques that are semi-quantitative at best.

Conclusions

This discussion points to a need for renewed emphasis on the importance of dietary quality for weanlings in less developed countries. The energy and nutrient density of the diet, the techniques of food processing, and the organoleptic characteristics of the diet may all influence the amounts of energy and nutrients consumed and utilized. Moreover, the amount and bioavailability of specific nutrients in the child's diet may be at least as important for growth and other functional outcomes as the total amount of available food or food energy. To facilitate further discussion of dietary quality, scientists must develop simple measurement techniques to assess diets in ways that stress the functional implications of specific characteristics.

It is ironic to note that, just when many nutritionists in industrialized countries are beginning to encourage greater consumption of plant-derived complex carbohydrate and decreased intake of saturated fat, nutritionists in less affluent countries are recognizing the importance of animal products and dietary lipids, both to increase the energy and nutrient density of the diet and to enhance nutrient bioavailability for young children. One certainly hopes that a mutually satisfactory resolution to these divergent, but not necessarily contradictory, goals can be found through better sharing of available knowledge and other resources.

Acknowledgements

Data are presented from the Huascar studies, which were conducted in collaboration with Guillermo Lopez de Romaña and Hilary Creed de Kanashiro (Instituto de Investigación Nutricional, Lima, Peru) and Robert E. Black (Johns Hopkins University).

Janet M. Peerson of the Program in International Nutrition, University of California, Davis, assisted with analysis of data. Gretel H. Pelto, Kathryn G. Dewey, and George G. Graham reviewed earlier drafts of the paper and offered many helpful suggestions.

References

1. Williams CD. A nutritional disease of childhood associated with a maize diet. Arch Dis Child 1933;8:423-33.

2. McLaren DS. The great protein fiasco. Lancet 1974; 2:93-96.

3. Payne PR. Safe protein-calorie ratios in diets: the relative importance of protein and energy intake as causal factors in malnutrition. Am J Clin Nutr 1975;28:281-86.

4. Waterlow JC, Payne PR. The protein gap. Nature 1975;258:113-17.

5. Gordon JE, Chitkara ID, Wyon JB. Weanling diarrhea. Am 1 Med Sci 1963;13U:345-76.

6. Creed de Kanashiro H, Brown KH, Lopez de Romaña G, Lopez T, Black RE. Consumption of food and nutrients by infants in Huascar (Lima), Peru. Am J Clin Nutr 1990;52:995-1004.

7. Lopez de Romaña G, Brown KH, Black RE, Kanashiro HC. Longitudinal studies of infectious diseases and physical growth of infants in Huascar. an underprivileged pert-urban community of Lima, Peru. Am J Epidemiol 1989;129:769-84.

8. Food and Nutrition Board. Recommended dietary allowances. 10th ed. Washington, DC: National Academy Press, 1989.

9. Prentice A, Paul AA. Contribution of breast-milk to nutrition during prolonged breast-feeding. In: Atkinson S, Hanson L, Chandra R, eds. Breastfeeding, nutrition, infection and infant growth in developed and emerging countries. St. John's, Newfoundland, Canada: ARTS Biomedical Publishers. 1990:87-101.

10. Brown KH, Black RE, Becker S, Nahar S. Sawyer J. Consumption of foods and nutrients by weanlings in rural Bangladesh. Am J Clin Nutr 1982;36:87X-89.

11. Brown KH. Dickin KL, Bentley ME et al. Consumption of weaning foods from fermented cereals: Kwara State, Nigeria. In: Alnwick D, Moses S, Schmidt OG, eds. Improving young child feeding in eastern and southern Africa: household-level food technology. Ottawa, Canada: IDRC. 1988:181-97.

12. Garcia SE, Kaiser LL, Dewey KG. Self-regulation of food intake among rural Mexican preschool children. Eur J Clin Nutr 1990;44:371-80.

13. Fomon SJ, Ziegler EE, Nelson SE, Edwards BB. Sweetness of diet and food consumption by infants. Proc Soc Exp Biol Med 1983;173:19(1-93.

14. Fomon SJ, Thomas LN, Filer LJ. Acceptance of unsalted strained foods by normal infants. J Pediatr 1970;76:24246.

15. Underwood BA. Weaning practices in deprived environments: the weaning dilemma. Pediatrics 19X5; 75(suppl): 194-98.

16. Mosha AC, Svanberg U. The acceptance and intake of bulk-reduced weaning foods: the Luganga village study. Food Nutr Bull 1990;12(1):69-74.

17. Gopaldas T, Deshpande S, John C. Studies on a wheat-based amylase-rich food. Food Nutr Bull 1988; 10 (3):5559.

18. Krebs NF, Hambidge M, Walravens PA. Increased food intake of young children receiving a zinc supplement. Am J Dis Child 1984;138:270-73.

19. Aukett MA, Parks YA, Scotts PH, Wharton BA. Treatment with iron increases weight gain and psychomotor development. Arch Dis Child 1986;61 :849-57.

20. Chwang L-C, Soemantri AG, Pollitt E. Iron supplementation and physical growth of rural Indonesian children. Am J Clin Nutr 1988;47:496-501.

21. Martorell R, Yarbrough C. Yarbrough S, Klein RE. The impact of ordinary illnesses on the dietary intake of malnourished children. Am J Clin Nutr 1980;33:345-50.

22. Brown KH, Stallings RY, Creed de Kanashiro H, Lopez de Romaña G, Black RE. Effects of common illnesses on infants' energy intakes from breast milk and other foods during longitudinal community-based studies in Huascar (Lima), Peru. Am J Clin Nutr 1990;52:1005-13.

23. Brakohiapa LA. Bille A, Quansah E et al. Does prolonged breastfeeding adversely affect a child's nutritional status? Lancet 1988;2:416-18.

24. Bentley ME, Stallings RY, Fukumoto M, Elder JA. Maternal feeding behavior and child acceptance of food during diarrhea, convalescence, and health in the central sierra of Peru. Am J Pub Health 1991 ;81 :43-47.

25. Martorell R, Habicht J-P, Yarbrough C. Lechtig A, Klein RE, Western KA. Acute morbidity and physical growth in rural Guatemalan children. Am J Dis Child 1975;129:1296-1301.

26. Condon-Paoloni D, Cravioto J, Johnston FE, de Licardie ER, Scholl TO. Morbidity and growth of infants and young children in a rural Mexican village. Am J Pub Health 1977;67:651-56.

27. Rowland MGM. Cole TJ, Whitehead RG. A quantitative study into the role of infection in determining nutritional status in Gambian village children. Br J Nutr 1977;37:441-50.

28. Black RE, Brown KH. Becker S. Effects of diarrhea associated with specific enteropathogens on the growth of children in rural Bangladesh. Pediatrics 1984;73:799805.

29. Zumrawi FY, Dimond H, Waterlow JC. Effects of infection on growth in Sudanese children. Hum Nutr Clin Nutr 1987;41C:453-61.

30. Rowland MGM, Goh Rowland SGJ. Cole TJ. Impact of

infection on the growth of children from 0 to 2 years in an urban west African community. Am J Clin Nutr 1988;47: 134-38.

31. Lutter CK, Mora JO, Habicht J-P, Rasmussen KM, Robson DS, Sellers SG. Nutritional supplementation: effects on child stunting associated with diarrhea. Am J Clin Nutr 1989;50:1-8.

32. Becker S, Black RE, Brown KH. Relative effects of diarrhea, fever, and dietary energy intake on weight gain in rural Bangladeshi children. Am J Clin Nutr (in press).

Contents - Previous - Next