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The following section describes how the strategy for investigating the relationship between undernutrition and cognitive development has changed and is continuing to evolve. Also discussed are some of the problems in defining the nutritional and outcome variables of interest and how biological and environmental factors can modify the effects of undernutrition.

Assessing nutrition

Protein and energy. In the 1960s, when researchers and policymakers were becoming increasingly concerned that early PEM could result in permanent impairment of intellectual development, it was widely accepted that protein was the limiting nutrient in the diet of populations at risk. During the next decade, however, dietary energy was held to be the more critical factor (McLaren, 1974). It was understood that to provide undernourished children with protein without also providing sufficient energy was futile, because the dietary protein would be used to supply energy rather than essential amino acids.

Iron, iodine, and zinc. Accompanying the new focus on energy was a recognition that, in most circumstances, energy deficiency may be closely linked to political and socioeconomic problems not easily addressed by simple nutritional intervention. Such political complexity and the fact that dietary energy is inextricably confounded with a mix of nutrients were two of numerous reasons that led subsequent research and policy interest to shift from the study of PEM effects to the effects of specific nutrients, especially Vitamin A, iron, iodine, and zinc. Whereas iron deficiency was known to be a cause of anemia, zinc deficiency a cause of growth retardation, and iodine deficiency a cause of goiter and cretinism, studies established further that deficiencies in these nutrients have broader systemic effects that lead to multiple threats to child health and development (United Nations ACC/SCN, 1993).

Complexities of deficiencies. Mild-to-moderate protein-energy malnutrition is difficult to diagnose, because it does not produce a specific set of symptoms and signs. It also coexists with other nutrient deficiencies. The same foods, particularly those from animal origin (from meat, fish, and poultry), are often sources of energy, protein, and distinct micronutrients (e.g., iron and zinc). Children that do not have access to these foods are at risk of multiple nutritional deficiencies. Further, some constituents of a habitual diet can limit the absorption of some important nutrients. This is the case, for example, with phytates, tea, and coffee which inhibit the absorption of non-heminic iron. Dietary quality² is critically important, requiring diversity and, to the extent possible for a family, the inclusion of foods of animal origin.

Where food is scarce and dietary quality is poor, diets consist primarily of staples such as cereals and legumes. Such diets typically contain few animal products, fresh fruits, or vegetables, and are therefore associated with low intakes of certain vitamins and minerals, high intakes of phytates and fiber, and poor bioavailability³ (Allen, 1993). Moreover, bioavailability is reduced when the supply of nutrients that enhance absorption is low. Finally, when food availability and quality are inadequate, the incidence of morbidity is usually high, with several nutrients simultaneously depleted through anorexia, malabsorption, and/or diarrhea with its associated inflammatory responses (Chen, 1983; Martorell & Yarbrough, 1983; Sahni & Chandra, 1983).

Thus, with both the nature of nutritional deficiency and the relationship among nutrients unclear, it remains a challenge not only to understand effects but to utilize findings in designing intervention strategies. In populations where general undernutrition is common, supplementation with a single nutrient, with the exception perhaps of iodine, will often be ineffective because as one deficiency is ameliorated, others may become limiting.

Measuring outcome

Investigations of both the nature and range of effects of undernutrition on intellectual development have been limited by the restricted nature of the psychological tests commonly used to assess children's cognitive development. Availability and convenience of the test seem to have been the dominant criteria for test selection, rather than considered theory and well-defined hypotheses that would test the psychological processes most likely to be affected. Consequently, it is possible that deficits in specific cognitive functions, e.g., attention, have not been adequately assessed by IQ or achievement tests, and may have been underestimated or missed entirely (Diamond et al., 1992). This concern is borne out by suggestive evidence of impaired attentiveness in previously undernourished children (Galler, Ramsey, Solimano, & Lowell, 1983).

Effects of undernutrition on social and emotional development have been generally disregarded. The few researchers who have investigated such effects have observed that social and emotional development is sensitive to undernutrition (Barrett, 1984; Espinosa, Sigman, Neumann, Bwibo, & McDonald, 1992) and can moderate effects on other processes. Detriments in these domains, observed repeatedly in animal studies (Levitsky & Strupp, 1995), may well have significant effects on the child's ability to adapt to the educational and social environment.

The traditional approach of focusing exclusively on cognitive development, independent of other psychological processes and systems, contradicts both current understanding of psychological development and the results of experimental studies based on animal models. Such a restricted approach also gives the mistaken impression that the effects of undernutrition on cognition are direct. Current data indicate strong reciprocal interactions between cognitive and emotional development so that changes in one may contribute to changes in the other (Rothbart, Derryberry, & Posner, 1994; Steinmetz, 1994).

Incorporating the context

Adopting a contextual approach acknowledges that we can not interpret the contributions specific biological or psychosocial factors to development independent of the individual's specific environment. Within this framework, the study of nutritional influences on development must account for not just the biological but also the psychosocial stressors that accompany undernutrition (Horowitz, 1989; Pollitt, 1987; Ricciuti, 1981, 1993). Available evidence clearly demonstrates that undernourished individuals have a higher probability of simultaneous exposure to other risk factors (Golden, 1991; Grantham-McGregor, 1984; Pollitt, 1987), including

(1) biological factors (e.g., morbidity, parasitic infection, lead exposure);
(2) psychosocial factors (e.g., child neglect, poor-quality schools);
(3) socioeconomic factors (e.g., parental underemployment, lack of access to medical care).

Conversely, the detrimental impact of an adversity may be attenuated (though not necessarily eliminated) by protective factors, such as maternal education (Rutter, 1983; Zimmerman & Arunkumar, 1994). For example, in one study among impoverished rural communities in Guatemala, maternal education ensured that the children benefited from a nutrition program. Independent of the distance between home and the center where the foods were distributed, the mothers with higher levels of education took the children to the center to eat the food distributed without charge. This was not the case among children of mothers with low levels of education: these children were likely to be taken to the center only if they lived nearby (Carmichael, Pollitt, Gorman, & Martorell, 1994).

Traditionally, environmental influences have been regarded as complicating nuisances, to be controlled for by elements of the research design or statistical procedures. But this view has tended to oversimplify or obscure inherent complexities of causation that can only be captured if the most relevant biological, psychosocial, and socioeconomic factors (the covariates) are an integral part of the research plan (Lozoff, 1990).