Among the several causes of preschooler malnutrition discussed in this symposium, consumption of an inadequate diet obviously is a primary causal factor. In this review we summarize current knowledge about lack of an adequate diet during specific stages of early childhood development, and the relative importance of macronutrient intake versus dietary quality (dietary diversity and the consumption of animal source foods [ASF]). Although this review addresses the diet of preschoolers (≈2–5 y), data were often lacking from this age group so that some information was used from younger and older children.
An “adequate diet” for children is one that contains an appropriate density of nutrients, is sufficiently diverse that it supplies adequate but not excessive amounts of nutrients, is palatable and culturally acceptable, affordable and available year-round and overall supports normal growth and development.
IMPORTANCE OF NUTRITIONAL DEPLETION ON ENTRY TO THE PRESCHOOL PERIOD
When discussing the needs of preschoolers, it is important to recognize that a high proportion of children in developing countries are already nutritionally depleted when they enter this phase of life. Many are born low birth weight or preterm, which results in their nutrient (eg, iron) stores at birth being relatively depleted (1). Poor maternal micronutrient status during pregnancy almost certainly contributes to lower infant nutrient deposition in utero, for example, for iron (2) and vitamin B12 (3,4). These mothers are likely to continue to be at high risk for micronutrient deficiencies during lactation, a time when nutrient requirements of the mother are even higher due to the secretion of nutrients in breast milk. This means that the concentrations of some nutrients in the breast milk will be lower than normal, especially B vitamins (except for folate), vitamin A, iodine and selenium, which puts the breast-feeding infant and child at risk for these micronutrient deficiencies (5). Thus, infants may often be subjected to in utero depletion and/or low breast milk concentrations of nutrients, leading to nutritional deficiency during the first 6 to 12 months of life (5). For example, we have reported that 49% of lactating mothers in Guatemala City and 68% of their breast-feeding infants have low or deficient plasma vitamin B12 concentrations at 12 months of age (6). The fact that infant nutritional depletion can occur in breast-fed infants in no way contraindicates the recommendation for exclusive breast-feeding during the first 6 months of life, but rather indicates the need to improve maternal micronutrient status during pregnancy and lactation. Even the breast milk of well-nourished women does not contain sufficient iron and zinc to meet an infant's requirements after the first 6 months of life, so that after this age additional intake from micronutrient-rich or -fortified complementary foods or supplements is required (5). However, commonly breast-feeding ends too early and breast milk is substituted by complementary food of inadequate quality.
PERIOD OF COMPLEMENTARY FEEDING
During the transition from breast-feeding to complementary feeding, breast-feeding should be continued while gradually adding complementary foods. Because the intake of breast milk falls with age, it is evident that the amount and percent of nutrients required from complementary foods increase with age. By 9 to 11 months old, the average breast-fed baby in low-income countries needs to obtain about 50% to 90% of its vitamin and mineral requirements from complementary foods (7). The energy intake of the child depends on the number and energy density of meals. It has been estimated that at 1 to 2 years old, assuming the average amount of breast milk that is consumed at this age in low-income countries, if two complementary feeds are given daily, then the energy density of the meals needs to be at least 1.5 kcal/g; for 3 meals per day it needs to be 1.0 kcal/g and for 4 meals, 0.74 kcal/g (8). Children more than 8 months old probably need about 3 meals per day.
To evaluate how well nutrient requirements are met by complementary feeding in developing countries, food intake data were analyzed from Guatemala City, Bangladesh and Malawi (8). The analysis revealed that families can prepare complementary foods that have an adequate energy density, and can feed them often enough to meet their childrens' energy needs, but about one third of the children in the different countries were given meals with insufficient energy density for the number of meals provided. Moreover, the amounts of food consumed by the children were much less than their gastric capacity. Intakes of energy (when expressed per kilogram of body weight), protein and fat were adequate. However, the intake of many micronutrients was inadequate, especially the B vitamins, iron, zinc, calcium (if dairy product intake is low), and vitamin A (in Bangladesh). In fact, the authors concluded that it would be difficult for these children to meet their recommended micronutrient intakes from food, and iron and zinc needs would be met only if large amounts of liver were to be included in the diet. If the amount recommended by the World Health Organization (1 rounded tablespoon per day) were to be consumed routinely, however, vitamin A intakes would be 20 times greater than recommended. An additional problem is that the per-capita amounts of meat, liver and egg available in Guatemala, Bangladesh and Malawi were estimated to be less than the amounts required to meet the iron requirements of infants ages 6 to 11 months, pointing to the need for young children to receive iron-fortified foods or iron supplements.
ADEQUACY OF ENERGY INTAKE
In places with food shortages, there is clearly a risk of inadequate energy intake and low weight-for-height (wasting). Usually the adequacy of energy intake per se is difficult to determine because a low intake of many other nutrients will occur if food intake is inadequate. Interpretation of energy intervention trials is also often difficult because supplemental energy can displace the usual diet. Using a more sophisticated experimental design, Krahenbuhl et al. compared the effects of a high-fat versus a high-carbohydrate energy supplement against a nonintervention placebo group in rural Gambian children with stunting (9). The supplemented children, ages 68 ± 21 months, were provided with a high-fat or a high-carbohydrate biscuit for 12 months. They were moderately stunted and wasted at the start of the intervention. Their usual diet was low in fat (17% of energy) but adequate in protein (11%). Energy intake was only 80% of that recommended, but adequate on a per kilogram body weight basis. The high-fat biscuit increased energy intake by 1551 kJ (378 kcal), and the high-carbohydrate biscuit increased energy intake by 1659 kJ (404 kcal). In spite of these substantial increases in energy intake, the supplements had no effect on growth in length or weight or on resting metabolic rate. The high-fat biscuit produced a small increase in fatness. Interestingly, weight gain during the 3-month harvest season was about 3 to 10 times as much as it was during the other seasons, perhaps indicating the importance of the other nutrients in food.
Dietary diversity can be defined as the number of foods or food groups consumed in a defined period, such as 1 day or 1 week. Using Demographic and Health Survey data from 11 countries, Arimond and Ruel compared the prevalence of stunting to diet diversity in children ages 6 to 23 months (10). Dietary diversity was a 7-point score based on the number of groups of nutritionally important foods/food groups that the child had consumed on ≥3 days in the previous week; starchy staples, legumes, dairy products, other ASF, vitamin A–rich fruits and vegetables, other fruits and vegetables, and foods made with oil, fat or butter. After adjusting for the age of the child, maternal height and body mass index, the number of children in the household <5 years old and 2 health and welfare factor scores, there remained a significant correlation between dietary diversity and the prevalence of stunting in all but 1 of the countries.
IMPORTANCE OF ASF
In most developing countries, the intake of ASF is too low to provide the population with sufficient amounts of nutrients such as vitamin B12, bioavailable iron and zinc, riboflavin and calcium. For example, ASF provide <5% of total dietary energy in many sub-Saharan countries, 5% to 10% in most other African countries and southern Asia, 10% to 15% in most of eastern and northern Asia and >20% in wealthier regions such as the United States and Europe.
The ASF intake of preschoolers tends to parallel the general availability of milk, eggs and meat for the population. About 10 years ago, a multicountry study of preschoolers 18 to 30 months old in Egypt, Mexico and Kenya showed that children in all 3 countries consumed about 66 kcal/d in dairy products, but that meat plus egg intake provided 85 kcal/d in Egypt, 60 kcal/d in Mexico and only 6 kcal/d in Kenya (11). These low intakes of ASF were accompanied by low intakes of vitamins (12) and minerals (13) but not protein (14) and a high prevalence of micronutrient deficiencies.
More recently the investigators in the Kenya project returned to the same location to assess the effects of increasing ASF intake of schoolchildren ages 7 to 12 years in the same communities. The children's diets had not improved, and they consumed only an average of 12 kcal/d from meat and 52 kcal/d from milk; most of the energy was from maize and beans. Using food intake data from this study, we asked the question whether the intake of specific food groups or the overall diversity of the diets was the strongest predictor of the micronutrient adequacy of the children's diets (15). The outcome variable was the mean probability that a child would consume his or her estimated adequate requirement for 15 micronutrients. The analyses revealed that the average number of food groups consumed daily was associated with a gradual increase in micronutrient adequacy across the range examined, from 2 to 7 groups per day. However, increasing the number of servings of ASF from 0 to 3/d had only a small impact on micronutrient intake at baseline because the usual intake of ASF was so low, only 17 g/d. When ASF intake was increased to 52 g/d on average by supplements of meat or milk, the incremental benefits of increasing intake from 0 to 3 servings per day was much greater. Thus, it was concluded that ASF certainly improve childrens' abilities to meet their micronutrient requirements, but that their impact on micronutrient adequacy of the diet is limited until intake is greater than a minimal amount. Also, it was apparent that increasing dietary diversity is especially important in cases in which the usual intake of ASF is low. It should be noted, however, that even the small amounts of ASF usually consumed by children in developing countries have been reported to make a positive difference to mental and motor function (16,17). The usual intake of ASF by Kenyan preschoolers 18 to 30 months old was the main predictor of their subsequent cognitive scores at age 5 years (18).
INTERVENTIONS WITH ASF
A review of the efficacy of various interventions for improving child growth elicited the following conclusions (19). Energy supplements tend to increase body weight but not length. Protein supplements provide little benefit to improve growth. In contrast, supplements containing dried skim milk as at least 1 component improved the growth of children in 12 of 15 trials. When families of Dutch macrobiotic preschoolers increased their children's intake of milk or fish, their linear growth improved more than those of the other macrobiotic children (20). In contrast, adding dry fish to complementary foods did not affect the growth of infants ages 6 to 12 months in Ghana (21).
The benefits of adding supplemental meat to Kenyan children's diets have been tested in a recent study and compared with those of adding milk (22). On a per-kilocalorie basis, meat tends to be higher in available iron and zinc and vitamin B12 than does milk, whereas the latter contains more riboflavin, folate and calcium. Details of the study design and results have been provided elsewhere (22,23). Basically, the children, ages 7 to 12 years, were given 1 of 3 types of snacks daily in school while school was in session for 2 years. The 3 equicaloric groups were: an “energy” supplement in the form of 250 kcal as the traditional food githeri, primarily maize and beans, plus oil; a meat supplement (ie, githeri plus 60–80 g of ground beef); or a milk supplement (ie, githeri plus 1 cup of milk). Households in a nonintervention control group received a goat at the end of the study. In general the meat supplement produced greater improvements in cognitive function assessed using Raven's progressive matrices and arithmetic scores, resulted in the highest levels of physical activity, caused the biggest increase in initiative and leadership behavior, and provided the largest increment in muscle mass (22,24–26). The latter may have been the cause or the result of the greater physical activity. Milk supplementation significantly increased the growth of the shorter children.
Vitamin B12 is found only in ASF and the high global prevalence of this vitamin deficiency is becoming recognized (27,28). At baseline, 69% of the children had a deficient or marginal plasma cobalamin concentration, and the latter was significantly correlated with the usual total intake of ASF (r = 0.308), or of meat, eggs or milk. Children in the lowest tertile of ASF consumption had a 6.3 times greater risk of having a deficient or marginal plasma cobalamin concentration, even though usual intakes of ASF were very low (E. McLean, MD, and colleagues, unpublished data). Both the meat and milk supplements significantly reduced the prevalence of vitamin B12 deficiency, with the meat increasing the plasma cobalamin concentration by ≈200 pg/mL and the meat increasing it by ≈125 pg/mL at the end of the study.
In many resource-limited households, it still may be possible to provide young children with larger amounts of ASF than they are receiving. Caregivers often need to be taught about the importance of these foods for the nutrition of children and their mothers. Dairy products or fish may be more affordable than meat in some locations, and cheaper types of meat including concentrated nutrient sources such as liver could be targeted in small amounts to children and mixed with beans, fruits or cereal staples. Tougher meats may need grinding or chopping to encourage younger children to consume them.
When addressing the role of inadequate diet as a cause of malnutrition in preschool children, it is important to recognize that many children in developing countries will already be nutritionally depleted by the end of the first year of life because of the poor nutritional status of their mothers. During the period of transition to complementary feeding, energy deficiency may occur if food is short or if the energy density of the diet is low and not compensated for by an adequate number of meals. However, energy supplements generally tend to slightly increase weight but not height, even where there is seasonal food shortages. The amount of ASF consumption is a critical determinant of children's nutritional status (especially vitamin B12 status) and development. The development community needs to appreciate the importance of ASF for nutritional status (29) and normal development in low-income countries, especially in the common situation that fortified foods and micronutrient supplements are not sufficiently available. Newer concepts concerning the feasibility and merits of livestock production in developing countries (30) and novel approaches to increasing the availability of ASF for children (31) should receive greater attention if the prevalence of undernutrition in this age group is to be reduced.
1. Michie CA, Raffles A. Iron supplementation in the preterm or low birthweight infant. Arch Dis Child 1990; 65:559.
2. De Pee S, Bloem MW, Sari M, et al
. The high prevalence of low hemoglobin concentration among Indonesian infants aged 3–5 months is related to maternal anemia. J Nutr 2002; 132:2215–2221.
3. Allen LH. Vitamin B12 metabolism and status during pregnancy, lactation and infancy. Adv Exp Med Biol 1994; 352:173–186.
4. Allen LH. Impact of vitamin B-12 deficiency during lactation on maternal and infant health. Adv Exp Med Biol 2002; 503:57–67.
5. Allen LH, Graham JM. Assuring micronutrient adequacy in the diets of young infants. In: Delange FM, West KPH, editors. Micronutrient Deficiencies in the First Six Months of Life. Basel: Vevey/S. Karger AG; 2003. pp. 55–88.
6. Jones KM, Ramirez-Zea M, Zuleta C, et al. Highly prevalent vitamin B-12 deficiency in Guatemalan infants aged 12 months is predicted by maternal B-12 deficiency and infant diet. J Nutr
7. Brown KH, Dewey KG, Allen LH. Complementary Feeding of Young Children in Developing Countries: A Review of Current Scientific Knowledge. Geneva: World Health Organization; 1998.
8. Brown K, Peerson J, Kimmons J, et al
. Options for achieving adequate intake from home-prepared complementary foods in low income countries. In: Black R, Michaelsen K, editors. Public Health Issues in Infant and Child Nutrition. Philadelphia: Lippincott Williams & Wilkins; 2002. pp. 239–256.
9. Krahenbuhl JD, Schutz Y, Jequier E. High fat versus high carbohydrate nutritional supplementation: a one year trial in stunted rural Gambian children. Eur J Clin Nutr 1998; 52:213–222.
10. Arimond M, Ruel MT. Dietary diversity is associated with child nutritional status: evidence from 11 demographic and health surveys. J Nutr 2004; 134:2579–2585.
11. Allen LH. Malnutrition and human function: a comparison of conclusions from the INCAP and nutrition CRSP studies. J Nutr 1995; 125:1119S–1126S.
12. Calloway DH, Murphy SP, Beaton GH, et al
. Estimated vitamin intakes of toddlers: predicted prevalence of inadequacy in village populations in Egypt, Kenya, and Mexico. Am J Clin Nutr 1993; 58:376–384.
13. Murphy SP, Beaton GH, Calloway DH. Estimated mineral intakes of toddlers: predicted prevalence of inadequacy in village populations in Egypt, Kenya, and Mexico. Am J Clin Nutr 1992; 56:565–572.
14. Beaton GH, Calloway D, Murphy SP. Estimated protein intakes of toddlers: predicted prevalence of inadequate intakes in village populations in Egypt, Kenya, and Mexico. Am J Clin Nutr 1992; 55:902–911.
15. Ruel ME, Graham JM, Murphy SP, et al. Validating simple indicators of dietary diversity and animal source food intake that accurately reflect nutrient adequacy in developing countries. Report to the Global Livestock CRSP, University of California Davis; 2004.
16. Allen LH. The nutrition CRSP: what is marginal malnutrition, and does it affect human function? Nutr Rev 1993; 51:255–267.
17. Marquis GS, Habicht JP, Lanata CF, et al
. Breast milk or animal-product foods improve linear growth of Peruvian toddlers consuming marginal diets. Am J Clin Nutr 1997; 66:1102–1109.
18. Sigman M, McDonald MA, Neumann C, et al
. Prediction of cognitive competence in Kenyan children from toddler nutrition, family characteristics and abilities. J Child Psychol Psychiatry 1991; 32:307–320.
19. Allen LH, Gillespie SR. What Works? A Review of the Efficacy and Effectiveness of Nutrition Interventions. Geneva: ACC/SCN/ADB; 2001.
20. Dagnelie PC, van Dusseldorp M, van Staveren WA, et al
. Effects of macrobiotic diets on linear growth in infants and children until 10 years of age. Eur J Clin Nutr 1994; 48:S103–S111.
21. Lartey A, Manu A, Brown KH, et al
. A randomized, community-based trial of the effects of improved, centrally processed complementary foods on growth and micronutrient status of Ghanaian infants from 6 to 12 mo of age. Am J Clin Nutr 1999; 70:391–404.
22. Neumann CG, Bwibo NO, Murphy SP, et al
. Animal source foods improve dietary quality, micronutrient status, growth and cognitive function in Kenyan school children: background, study design and baseline findings. J Nutr 2003; 133:3941S–3949S.
23. Murphy SP, Gewa C, Liang LJ, et al
. School snacks containing animal source foods improve dietary quality for children in rural Kenya. J Nutr 2003; 133:3950S–3956S.
24. Whaley SE, Sigman M, Neumann C, et al
. The impact of dietary intervention on the cognitive development of Kenyan school children. J Nutr 2003; 133:3965S–3971S.
25. Grillenberger M, Neumann CG, Murphy SP, et al
. Food supplements have a positive impact on weight gain and the addition of animal source foods increases lean body mass of Kenyan schoolchildren. J Nutr 2003; 133:3957S–3964S.
26. Sigman M, Whaley SE, Neumann CG, et al
. Diet quality affects the playground activities of Kenyan children. Food Nutr Bull 2005; 26:S202–S212.
27. Allen LH. Folate and vitamin B12 status in the Americas. Nutr Rev 2004; 62:S29–S34.
28. Stabler SP, Allen RH. Vitamin B12 deficiency as a worldwide problem. Annu Rev Nutr 2004; 24:299–326.
29. Murphy SP, Allen LH. Nutritional importance of animal source foods. J Nutr 2003; 133:3932S–3935S.
30. Brown DL. Solutions exist for constraints to household production and retention of animal food products. J Nutr 2003; 133:4042S–4047S.
31. Allen LH. Interventions for micronutrient deficiency control in developing countries: past, present and future. J Nutr 2003; 133:3875S–3878S.