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close this bookChronic Energy Deficiency : Consequences and Related Issues (International Dietary Energy Consultative Group - IDECG, 1987, 201 pages)
close this folderA critical view of three decades of research on the effects of chronic energy malnutrition on behavioral development
View the document(introductory text...)
View the document1. Background
View the document2. The main-effect model
Open this folder and view contents3. Deficiencies of the main-effect model
View the document4. Suggestions for future research
View the documentReferences

(introductory text...)

E. POLLITT*.

* Department of Applied Behavioral Sciences, University of California, Davis, CA 95616, U.S.A.

1. Background

Three decades of research have passed, involving costly, lengthy and elaborate attempts to test the hypothesis that early chronic protein energy malnutrition influences cognitive and social-emotional development. A cursory review of this research provides a gloomy view of its accomplishments. Without an in-depth analysis, the data gathered in the last 30 years are, at best, inconclusive; admittedly, not a single study can be cited that satisfies all the requirements of experimentation and at the same time provides a clear and distinct picture of the effects of early chronic undernutrition on mental development. Serious attempts to test the hypothesis in question failed because of conceptual and methodological problems in the criteria that define the subjects to be studied, in the sampling procedure, in the delivery of the experimental treatment, or in other aspects of research design. For example, intervention studies included subjects not likely to be nutritionally at risk (RUSH, STEIN and SUSSER, 1980); in others, the frequency of the treatment was hopelessly confounded with self-selection in the sample (KLEIN, et al., 1976), or the treatment represented not only a nutritional intervention, as intended, but a potent social intervention as well (CHÁVEZ and MARTÍNEZ, 1982).

This dim view of the past three decades brightens, however, when the studies are pooled and the evidence is examined in the light of new relevant theoretical and empirical work in developmental biology and developmental psychology. This paper examines critically and synthesizes the conceptual approaches used and the data derived from studies on undernutrition and behavioral development- particularly cognitive development1. This critique takes advantage of current thinking on the nature of behavioral development and of the role attributed to biological risk factors in shaping cognitive function. A final objective is to underline what are in my view the most important findings on which we can draw, and point to new approaches that can lead future research in this area.

1 Most research on the developmental consequences of early chronic protein and energy deficiency has focused on aggregate measures of intelligence (e.g., IQ) or specific measures of cognitive development (e.g., attention; POLLITT, 1984). There are some notable exceptions that have focused on social-emotional development, or mother-child interaction, or school behavior, among others (see references). These are, however, exceptions.

2. The main-effect model

Early studies of the effects of prenatal and early postnatal undernutrition on behavioral development were guided by a static main-effect model, which has its roots in the biomedical model of disease causation. In its simplest form the biomedical model is a reductionistic approach in which agent and disease are conceptualized as causally and linearly related (ENGEL, 1979). A simple version of this model in relation to the hypothesis of an adverse effect of early protein energy malnutrition on mental development is represented in the following bivariate equation:

BD = f (NR)

where BD = behavioral deviation and NR = nutritional risk factor (e.g., wasting during the second six months of life). That is, the probabilities of a delay in behavioral development will vary as a function of severity and timing of the nutritional disorder.

This main-effect model can be traced in the developmental literature to the early-trauma, later-deficit hypothesis, which goes back to the mid-19th century (LITTLE, 1982). A basic assumption is that exposure to biological risk factors2 during critical periods of brain growth results in structural lesions in the brain, which in turn leave sequelae such as mental retardation. The emphasis is on the measurement of an input (e.g., chronic fetal hypoxia) and an output (e.g., IQ; see, for example NAEYE, 1987). Besides epidemiological studies using large sample sizes and establishing bivariate correlations, clinical trials and the measurement of a dose-response are sharp expressions of this conceptual and methodological approach.

2 In the present context risk is defined as the probability of an individual's developing a given disease or experiencing a health-status change over a specified period of time (KLEINBAUM, KUPPER and MORGENSTERN, 1982). Biological risk factors are adverse environmental circumstances or events that occur in pregnancy (e.g., intra-uterine growth retardation), at birth (e.g., hypoxia), during lactation, or during the preschool period (e.g., lead intoxication) and increase the probability of diverting a child's growth and developmental trajectory from a course typically followed when physiological and emotional needs are adequately met.

The main-effect model does not account for either the social context in which development occurs, for the previous and subsequent health history of an individual, or for the interactions3. Most importantly, the model, within the context of developmental research, has failed to incorporate two critical developmental characteristics: plasticity and canalization (MCCALL, 1981). Plasticity refers to the notion that, within the limits of individual differences and structural functional capacities, the organism has the elasticity or flexibility to be influenced by, and adapt to, new environmental contingencies (KUO, 1967; GOLLIN, 1981). Canalization refers to the organism's characteristic of following a species-specific developmental path that allows it to withstand a great amount of environmental stress before any significant deviation is observed4.

3 There are, among others, two categories of interactions that have been identified in human developmental research (RUTTER, 1983). One refers to the interactions (synergistic or antagonistic) between variables outside the organism that affect developmental outcome. The other (ordinal interactions) refers to interactions between an environmental variable and an organismic variable that determine different effects from similar experiences in different people, or from similar experiences in the same people at different ages.

4 At least three different definitions of canalization have been advanced (see GOTTLIEB, 1983). In the present context reference is made to canalization as defined by the developmental geneticist WADDINGTON (1971).

The main-effect model guided correlational and experimental (or quasi-experimental) research in the field and in the laboratory. Correlational studies measured the associations between retardation in physical growth and delays in mental development (i.e., DQ or IQ; KLEIN et al., 1972) or in tests of specific cognitive function (CRAVIOTO, DELICARDIE and BIRCH, 1966). Height-forage, weight-for-age or weight-for-height were taken as indicators of present nutritional status or of nutritional history. Statistically significant correlations between, for example, height-for-age and low intelligence test performance were interpreted to mean that exposure to undernutrition increased the probabilities of developmental risk. Experimental studies of nutrition supplementation measured the variance in developmental outcome accounted for by the variance in dietary intake (Jogs and POLLITT, 1984).

A striking illustration of the influence of the main-effect model on the conduct and interpretation of research on undernutrition and behavior was the calculation of regression coefficients to measure the changes in protein intake presumably required for a given change in an intelligence quotient (TAYLOR and SELOWSKY, 1973). This econometric analysis might not be representative, but it does convey the flavor of the conceptual approach that dominated the field.

Animal and basic research, and influential theoretical concepts such as the critical period of behavioral development (SCOTT, 1962) 5, strengthened the face validity 6 of the main-effect model. The critical period hypothesis in connection with a nutritional insult predicted that protein and energy malnutrition during a time of accelerated brain growth (i.e., the first 24 months of life) resulted in a deviation from the normal trajectory of central nervous system development (DOBBING and SANDS, 1979). Implicit in this definition is the idea that past a certain "critical point" (duo, 1967), there is little chance for rehabilitation from the insult produced by undernutrition. A corollary is that past such critical point of brain growth the presence of undernutrition would not have severe developmental consequences.

5 A critical period is defined as a limited period during development in which a particular stimulus will have a profound effect upon the organism. The same stimulation before or after this interval will have little or no effect upon the organism.

6 Face validity is a subjective evaluation by judges as to what a measuring device appears to measure.

Experimental and basic research data in part supported the main-effect model and fed into the critical period hypothesis. Experimentally-induced malnutrition in early life on laboratory rodents (BARNES et al., 1966; FRANKOVA and BARNES, 1968) and pigs (BARNES, MOORE and POND, 1970) adversely affected learning in later development. Early undernutrition in rats retarded the division process of every type of proliferating brain cell and delayed migration of cells and myelination (WINICK and NOBLE, 1966). Curtailment of brain cell division was also documented in infants who died of severe undernutrition (WINICK and ROSSO, 1969).

(introductory text...)

The results of correlational and supplementation research studies in humans and experimentation in animals, however, were insufficient to justify the main-effect model. Gradually, most investigators recognized that a bivariate approach of simple linear causality was not conducive to an understanding of the developmental effects of undernutrition among poor children (POLLITT and RICCIUTI, 1969; RICHARDSON, 1974, 1980; RICCIUTI, 1981; RUSH, 1984; GBANTHAM-MCGREGOR, 1984). It became apparent that undernutrition was a multifactorially determined human condition, far too complex to be reduced to the blueprint of the main-effect model. The model constricted the alternatives for the recognition and measurement of factors that coexisted and interacted (see footnote 3) with protein and energy malnutrition and contributed to the nature of the final developmental outcome. In other words, the model lacked the sensitivity to account for what was observed in the field as well as for some of the findings of studies on human populations. Some of these findings are reviewed below, underscoring the basic issues that evidenced the need to drop the main-effect model and pointed in the direction of a new paradigm. The review is primarily intended to uncover contradictions in the findings of different types of studies, which reveal the inadequacies of the bivariate model. Three main issues will be addressed:

1. discrepancy in the findings between the developmental outcome of primary and secondary malnutrition;

2. effects of favorable and unfavorable social environmental circumstances in the developmental outcome of undernourished children; and

3. the differences in the effects produced by nutritional supplementation with and without health care and education stimulation.

3.1. Outcomes of primary and secondary malnutrition

There is a striking contradiction between the results from behavioral studies of children with a history of malnutrition living in economically impoverished environments in developing countries, and those from studies of children whose malnutrition is secondary to an organic illness in developed countries. The former consistently showed an association between undernutrition in early life and later developmental delay (see reviews in GALLER, 1984; BROZEK and SCHÜRCH, 1984; POLLITT and THOMSON, 1977). Conversely, studies on children with organic illness generally showed that these were not developmentally delayed. In these cases, chronic undernutrition in early life, independent of socioeconomic deprivation, did not correlate with poor developmental or intelligence test quotients or else the correlations found were very low (BEARDSLEE, et al., 1982; BERGLUND and RABO, 1973; KLEIN, FORBES and NADER, 1975). Similarly, a study in Holland on the effects of famine during World War II showed no effects of early undernutrition on performance on a non-verbal IQ test at age 18 (STEIN, et al., 1975).

One of the suggestions derived from this contradiction in the nature of the findings from these two types of studies is that undernutrition in early life did not leave developmental sequelae. The developmental delays observed among the undernourished children in developing countries were due to the contextual factors in which malnutrition occurs. An alternative explanation is that the environment of children with secondary malnutrition acted as a buffer and neutralized the effects of the nutritional deficiency.

3.2. Effects of the environment and experience

Evidence of potent advantageous and disadvantageous effects of the social environment and of experience on behavioral development has confirmed the inadequacy of the main-effect model (MCKINNEY, 1986). This evidence has accumulated gradually from different sources and in relation to different biological risk factors (see FARRAN and MCKINNEY, 1986). Children with similar types of early trauma differed in their developmental outcomes according to the nature of their social and familial environment (WERNER, 1986). Early signs of intellectual impairment associated with biological trauma such as intra-uterine growth retardation disappeared in some circumstances because of favorable qualities of the environment and the educational experiences to which children were exposed (SAMEROFF and CHANDLER, 1975).

Findings from studies on undernutrition and cognitive function concurred with the behavioral observations on other biological risk factors. Social-environmental conditions determined large variability in the developmental outcome of children with similar histories of early nutritional deficiencies (RICHARDSON, 1980). Moreover, the magnitude of the differences between the intelligence test scores of children with and without a history of malnutrition varied as a function of social-environmental factors. Under comparatively favorable environmental conditions the differences were small (e.g., 2 IQ points); on the other hand, under unfavorable environmental conditions, these differences were relatively large (e.g., 10 IQ points; RICHARDSON, 1980). Similarly, environmental conditions that met the developmental needs of children protected against, and in some instances remedied, the cognitive delays associated with the nutritional deficiency (WINNICK, MEYER and HARRIS, 1979; GBANTHAM-MCGREGOR, 1984, 1984a). Thus, early malnutrition, even during so-called critical periods of brain growth, was not a sufficient condition to fix a developmental trajectory 7.

7 Based on data from a long-term follow-up of severely malnourished (marasmic) children on the island of Barbados, GALLER (1984a) has argued strongly that, after controlling for social-environmental variables, malnutrition accounts for a large and significant portion of variance in intelligence test measures, school behavior and school attainment. Her measures of graduated parameters of social structure are illustrated by assessments of household items, quality of housing or father's work. Because of the retrospective nature of the study process variables relevant to the time of the nutritional deficiency, could not be assessed.

Galler's work is indeed commendable because of the amount of follow-up information she has collected and the variety of behavioral measures obtained. However, given the nature of her study design, I fully agree with RICCIUTI'S (1981) comments related to the issue of looking for the effects of malnutrition, controlling for socioeconomic factors: "From this reviewer's perspective, these kinds of analyses are heuristically useful up to a point, but they are of rather limited value in advancing our understanding of the interactive influence of nutritional and socioenvironmental variations on intellectual development. First the indices of nutritional status and of the family and home environment are typically quite simplistic and hence may be capturing only a small portion of the developmentally relevant variations in each domain. Moreover, obtained estimates of the independent contribution of nutritional versus socioenvironmental factors will vary greatly depending on various characteristics of the samples employed such as age, homogeneity or heterogeneity with respect to environmental and nutrition variation and also depending on the particular outcome measures utilized." (p. 402).

Moreover, there was strong evidence of a synergism between nutritional history and social-environmental conditions in connection with developmental outcomes.

The corrective process, determined in part by social-environmental circumstances and related experiences, illustrated the plasticity of the organism in behavioral adaptation. Likewise, the shift toward a normal developmental trajectory following early developmental deviations could be considered akin to canalization, namely, a propensity to move in the direction of a species-typical path toward which its members tend to develop (see WADDINGTON, 1971).

Conversely, cognitive developmental deficits increased as children grew older and were continuously exposed to environments that did not meet their physiological, emotional and educational needs. Evidence from different sources confirmed the validity of the so-called "cumulative deficit hypothesis" (SACO-POLLITT, POLLITT and GREENFIELD, 1985). This pervasive effect of the environment was explained by the fact that under ordinary circumstances key components of such environment remain invariant across time. People tend to remain poor under conditions where the opportunities for change rarely exist, and the support systems required for such a change are scarce.

The high frequency of illness among children who were undernourished and living in economically impoverished environments (MATA, 1978) was also noted by investigators concerned with the effects of undernutrition on cognition. Behavioral observations were made that infection and diarrhea result in anorexia, affect the biological homeostasis of children and limit motor activity (BEATON, 1983). In one study (POLLITT, 1983), a significant relationship was observed between frequency of respiratory and gastrointestinal illness during the first six months of life and mental and motor development scores at eight months of life. The explanation given was that a demand for biological homeostasis leads an organism that is frequently ill to reduce activity and decrease energy expenditure.

Environmental conditions will determine to a large extent the direction of the developmental trajectory of children with a history of malnutrition. They can potentiate the effects of the nutritional deficit or, conversely, remedy or prevent adverse effects. Whenever there is a relationship between undernutrition and developmental delay, it is not likely to have been a simple, linear causal relationship. Unfortunately, however, with some notable exceptions (CRAVIOTO and DELICARDIE, 1979) little research has been done to define the nature of the environmental contingencies that will determine final outcomes for malnourished children.

3.3. Outcomes of monofocal and multifocal interventions

The third source of information pointing to the inadequacies of a bivariate model is the difference between the results of studies on nutritional supplementation with and without a health and an education component. Nutritional supplementation of pregnant and lactating women, and of infants and preschool children, yielded mild effects on developmental outcomes. On the other hand, multifocal interventions which included nutrition supplementation, health care delivery, and educational stimulation resulted in impressive developmental benefits.

The Table (from JOOS and POLLITT, 1984) presents in summary form the main developmental test findings of four supplementation studies conducted in Bogota, Colombia; Guatemala; Harlem, New York; and Sui Lin, Taiwan8. The brief review of these four studies that follows, illustrates that food supplementation alone, among nutritionally at risk women and young children, had mild, albeit statistically significant developmental effects.

8A detailed report of the components of each one of these interventions and a comparative analysis of the findings are reported in JOOS and POLLITT (1984). See also references for each study for specific information regarding research design and findings.

The results (see Table) for the study conducted in Bogota, Colombia, are the mean scores on the general quotient (GQ) of the Griffiths test9 in the three groups that received only supplement and the untreated control group (WABER et al., 1981). The analyses up to 18 months showed independent effects of nutritional supplementation primarily in the subscales that reflect motor functioning (Locomotor and Performance) and the GQ. Comparison of the mean GQ and subscale scores of the supplemented and control groups shows that, while the supplemented groups have higher mean scores than the control group, these differences are not statistically significant for any subscales at any one age. Statistically significant differences were restricted to intergroup comparisons across ages. Also, there was no independent effect of nutrition on the Albert Einstein Scale of Sensory Motor Intelligence10. A subsequent analysis up to three years of age yielded essentially the same findings, except that the nutrition treatment had a significantly greater effect on scores of the females than of males.

9 For a review of the methods used for the behavioral assessment of the consequences of malnutrition see POLLITT (1984).

10 In contrast to most other psychometric techniques used in most other empirically-based studies of undernutrition and behavior, the Albert Einstein Scale of Sensory Motor Intelligence was constructed on the basis of Piaget's epigenetic theory of intelligence.

The second set of scores presented in the Table are the mean scores in the mean and motor subscales of the Composite Infant Scales used in a supplementation study conducted in Guatemala (KLEIN et al., 1976). At six months of age, the differences between low, medium and high supplementation groups were statistically significant only for the mental subscale. At 15 and 24 months the absolute differences were greater and significant for both subscales. Item analyses suggested that the impact of supplement ingestion was more associated with motor and manipulative items within each scale than with the more cognitive or linguistic items. As in the Bogota study, effects were more apparent in the motor subscales, though the absolute differences were more pronounced in the Guatemala data. No sex differences were found11.

11 Social behavior may represent an exception to the effects of the supplementation restricted to the preschool period. Among children B to 10 years old from three of the tour villages participating in this supplementation study, several aspects of social behavior (personal interactions with peers and adults, activity levels, response to the physical environment and affect) appeared to be related to nutrition in early childhood (BARRETT, YARROW and KLEIN, 1982). Controlling for socioeconomic status, high levels of supplementation between birth and two years of age were predictive of high levels of social involvement, happy and angry affect, and moderate levels of activity, while low supplementation was associated with passivity, dependency on adults, and anxious behavior.

A serious methodological problem in this Guatemalan study is the self-selection in the sample to determine frequency of participation in the supplementation program. Participation was likely to be influenced by the subjects' motivation to take advantage of the available supplement. This social behavioral variable could have determined, at least in part, the variations observed in social development (BARRETT, 1984).

Table. Mean scores on developmental scales




Ages in months




4

6

8

12

15

18

24

Bogotaa

General

S1

103.6

100.7


98.6


97.7

100.4e


Quotient

S2

103.5

101.6


100.4


97.6

99.5



S3

106.1

102.0


98.0


96.3

88.8



U

100.4

97.0


97.6


95.1

98.8

Guatemalab

Mental

L


73.8*



62.9**


61.6**



M


76.3*



67.8**


65.5**



H


77.8*



72.3**


68.1**


Motor

L


70.0



73.8**


67.5**



M


70.6



77.2**


74 4**



H


72.7



82.6**


78.9**

New Yorkc

Mental

S




98.97






C




98.65





Motor

S




45.78






C




45.79






U




45.81




Taiwand

Mental (modified)

S



4.48







U



4.49






Motor (modified)

S



3.80***







U



3.31***





a S1 = Supplemented during pregnancy and infancy; S2 = Supplemented after 6-months old; S3 = Supplemented during pregnancy and until 6-months old; U = Unsupplemented controls.
b L = Low supplement intake (<5000 kcal/quarter for 14 quarters); M = Medium supplement intake (5000 to 10,000 kcal); H = High supplement intake (>10,000 kcal).
c S = "Supplement" group; C = "Complement"; U = Unsupplemented controls.
d S = High calorie and protein supplement; U = Placebo supplement.
e Average of male and female scores, Table 2, WABER et al., 1981.
*(p<.05) (F-test); ** (p<.01) (F-test); *** p = <.06 (2-tail t-test).

A third supplementation study was conducted in Harlem, New York (RUSH, STEIN and SUSSER, 1980). As indicated in the Table, there were no differences between the supplement, complement and control groups on either the mental or motor scales of the Bayley test at 12 months of age included in this study. The fourth and last study was carried out in the township of Sui Lin in Taiwan (JOOS et al., 1983). Treatment group differences in mental and motor scores (i.e., Bayley Scales) were tested with males and females combined and separated. The overall mental scores of the supplemented and the control group infants were not significantly different from each other. The motor scores of the supplement group (both sexes combined) were higher (p<.05) than those of the controls. However, analyses of the motor scores by sex did not show statistically significant differences between supplemented and unsupplemented children. Further, there were no significant correlations of volume of intake at any point in time (i.e., pregnancy and lactation) with any of the Bayley Scale scores.

This consistency of results in the four studies is striking considering that the selection of study sample, type of nutrition intervention, behavioral scales and ages at testing differed across the studies. Accordingly, the evidence from intervention studies suggests that the magnitude of developmental variability accounted for by nutritional variability alone is small, albeit statistically significant. These effects disappear in the school period and after terminating the supplementation program. The possibility of dormant effects that could be detected in later life still exists. Dormant effects were observed in early intervention studies among educationally disadvantaged children in the United States (Consortium for Longitudinal Studies, 1983).

In contrast to the mild effects of interventions restricted to nutrition supplementation, interventions that included health care and educational stimulation plus nutrition supplementation had major developmental effects (MCKAY et al., 1977). A study in Cali, Colombia, involving moderately to severely malnourished preschool children living in an impoverished urban community showed that the effects on cognitive developmental measures after four years of treatment were as large as .50 to .75 of a standard deviation. The size of these effects were particularly surprising because the children were enlisted when they were 42 months old. At this age they had already past the time of the so-called critical period of brain growth.

The difference in the magnitude of the effects between monofocal and multifocal interventions should not be surprising. The greater the improvements in the environmental conditions, the greater the developmental advantages for children. At issue here, however, is not the difference in itself but its magnitude, since it points to either additive or interactive effects. The former refers to the co-action of different inputs, whereas the latter reveals a synergistic effect, namely, that the health care and educational stimulation would potentiate the effects of the nutritional supplementation and vice versa. Unfortunately, the data available in the published reports are insufficient to allow for a comparative statistical analysis of the studies to determine the precise nature of the difference. In my view, the size of the effects in the Cali study is too large in comparison to that of the other studies to assume that they are simply additive.

An intervention study in Mexico (CHÁVEZ and MARTÍNEZ, 1982) is enlightening at this point because of the strong developmental effects obtained in the context of a study design that called for a nutritional supplement without additional inputs. The intervention began in pregnancy and continued throughout early childhood. The benefits were observed in cognitive measures in infancy and in the preschool period and later on in school attainment (CHÁVEZ and MARTÍNEZ, 1982a).

The investigators, as previously noted, intended to limit the experimental treatment to a nutritional supplement, but their reports strongly suggest that the experiment became a major social intervention. The conditions under which the supplement was delivered intensified the social interactions of the families and broadened their social contacts. In addition, the children that received the "treatment" acquired prestige or prominence within the community. The final outcome was that the intended intervention and the contextual response resulted in potent effects that, even in the absence of statistical comparisons between studies, were significantly greater than the effects observed in the other nutrition supplementation studies. It is thus reasonable to generalize that the differences already discussed between the benefits derived from the monofocal and the multifocal interventions are not determined only by the differences in the additive effect of the number of inputs. The interactions between nutrition and environmental factors are more likely to lie behind such differences, but these interactions have escaped the main-effect model.

In summary, the evidence presented on the three issues listed above indicates that the main-effect model is not conducive to an understanding of the developmental outcomes of children with a history of undernutrition. The direction in the trajectory of development of a child with a history of undernutrition depends not only on the nutritional history but on the environmental circumstances (e.g., attenuating circumstances, other risk factors) to which the organism is exposed, and the nature of its health history. Further, the notion of irreversible damage to brain function because of malnutrition during a so-called critical period is no longer tenable, as it is also no longer tenable in other areas of developmental psychobiology (GOTTLIEB, 1983). In fact, strong evidence points to the conclusion that unless "major and irreparable physiological insults" (HOROWITZ, 1987) have occurred, environmental conditions can modify the developmental effects of any biological or social risk factor to which the child is exposed in early life.

4. Suggestions for future research

For the purposes of this paper, a developmental risk factor was defined (see footnote 1) as a circumstance or event occurring in an early life period that increases the probability of diverting a child's growth and developmental trajectory from a course typically followed by children when physiological and emotional needs are met. Although the main-effect model has failed to give a conclusive answer to the issue of whether or not early undernutrition is a developmental risk factor, the evidence on the synergism between undernutrition and social-environmental factors strongly supports this contention. Through its interactions with illness and adverse family and socioeconomic conditions, undernutrition increases the probability of diverting the trajectory of mental development, a hazard not encountered by other children living under similar environmental and economic conditions who do not experience undernutrition. Moreover, and perhaps more importantly, undernutrition shapes behavioral adaptation into forms that are different from those of well-nourished children.

The evidence also points in the direction of research that integrates nutritional variability and context along a time dimension. Endemic infant and childhood malnutrition is a tragic manmade condition that provides a unique natural experiment to understand the biological basis of human behavior. Behaviorally-oriented research among chronically undernourished children has generally defined this condition as a biological insult, disregarding the behavioral implications of its long-term effects on the energy balance equation. A likely outcome of low energy expenditure, to maintain homeostasis, is reduction in activity, an important component of the behavioral repertoire of infants and young children (GOLDSMITH et al., 1987). As such, low energy expenditure is likely to shape interactions between the organism and the immediate environment (GRAVES, 1976, 1978; RICCUTI, 1981; BEATON, 1983; VALENZUELA and ARAYA, 1987), it would be of particular developmental interest to determine the ways in which the undernourished organism establishes transactions12 with caretakers, that is, the ways in which the energy-deficient child influences behaviors of "others" so that the energy demands are in keeping with its energy balance.

12 For present purposes I use the term transaction following RUTTER's definition (1983): "Transactional effects differ from all the interaction effects considered thus far in that it is not a question of one variable potentiating, reducing, or altering the effect of some other variable or outcome, but rather of one variable changing the other" (p. 305).

On the other hand, if research interest stems from consideration of applied issues (public health) then the greatest payoff lies in questions aimed at identifying and operationalizing those environmental factors that, in conjunction with undernutrition, increase children's developmental risk. Evidence from research on other biological risk factors suggests that cumulative risk through the additive and interactive effects of social and biological risk factors in time might be the best predictor of final outcome. Accordingly, there could be significant public health payoff in the identification of family or community "risk" variables13.

13 These could be conceptualized as time-independent or time-dependent. The former refers to structural variables, such as parental illiteracy, which are not likely to change throughout the child's infancy and early childhood. Time-dependent variables vary as the child grows older. These variations could occur in a systematic way. For example, rainy seasons with higher demands on maternal work could be considered a time-dependent variable that varies systematically within a 12-month period and represents a growth risk to infants and young children (ADAIR and POLLITT, 1985). Increases in family size do not follow a specific schedule; they generally result in caretaking practices within the household which could have adverse consequences for young children.

A recognition that it is necessary to change from bivariate to multivariate models is not a guarantee that the main effect model and bivariate equations will not be the prescriptions used in research on undernutrition and behavioral development. It does, however, provide a conceptual umbrella to understand better the developmental meaning of the data that are generated from research with different conceptual and methodological approaches.

References

ADAIR, L., POLLITT E.: Outcome of maternal nutritional supplementation: A comprehensive review of the Bacon Chow study. Am. J. Clin. Nutr., 41, 948-978 (1985).

BARNES, R.H., CUNNOLD, S.R., ZIMMERMAN, R.R., SIMMONS H., McLEOD, R.B., KROOK L.: Influence of nutritional deprivations in early life on learning behavior of rats as measured by performance in a water maze. J. Nutr., 89, 399409 (1966).

BARNES, R.H., MOORE, A.U., POND, W.G.: Behavioral abnormalities in young adult pigs caused by malnutrition in early life. J. Nutr., 100, 144-155 (1970).

BARRETT, D.E.: Methodological requirements for conceptually valid research studies on the behavioral effects of malnutrition. In: Nutrition and Behavior. Human Nutrition: A Comprehensive Treatise, Vol. 5, J. GALLER (Ed.). Plenum, New York, NY, 1984.

BARRETT, D.E., YARROW, M.R., KLEIN, R.E.: Chronic malnutrition and child behavior: effects of early calorie supplementation on social and emotional functioning at school age. Dev. Psychol., 18, 541-556 (1982).

BEARDSLEE, W.R., WOLFF, P.H., HURWITZ, I., PARIKH, B., SHWACHMAN H.: The effects of infantile malnutrition on behavioral development: a follow-up study. Am. J. Clin. Nutr., 35, 1437-1441 (1982).

BEATON, G.: Energy in human nutrition: perspectives and problems. Nutr. Rev., 41, 325-340 (1983).

BERGLUND, G., RABO, E.: A long-term follow-up investigation of patients with hypertropic pyloric stenosis - with special reference to the physical and mental development. Acta Paediatr. Scand., 62, 125-129 (1973).

BROZEK, J., SCHÜRCH, B. (Eds.): Malnutrition and Behavior: Critical Assessment of Key Issues. Nestle Foundation Publication Series, Lausanne, Switzerland, 1984.

CHÁVEZ A., MARTÍNEZ, C.: Growing up in a developing community. Instituto Nacional de Nutrición, Mexico City, Mexico, 1982.

CHÁVEZ, A., MARTÍNEZ, C.: School performance of supplemented and unsupplemented children from a poor rural area. In: Proceedings of the Xll International Congress of Nutrition, Alan R. LISS (Ed.), New York, NY, 1982a.

The Consortium for Longitudinal Studies: As the twig is bent... Lasting effects of preschool programs, L. ERLBAUM (Ed.), New Jersey, NJ, 1983.

CRAVIOTO, J., DELlCARDlE, E.R., BIRCH, H.G.: Nutrition, growth and neurointegrative development. An experimental and ecologic study. Pediatrics, 28 (supplement) (1966).

CRAVIOTO, J., DELICARDlE, E.R.: Nutrition, mental development and learning. In: Human Growth 3, Neurobiology and nutrition, F. FALKNER, J.M. TANNER (Eds.). Plenum Press, New York, NY, 1979.

DOBBING, J., SANDS J.: Comparative aspects of the brain growth spurt. Early Hum. Dev., 3, 79-83 (1979).

ENGEL, G.L.: The biomedical model: A procrustean bed? Man and medicine, 4, No. 4, 257-275 (1979).

FARRAN, D.C., McKINNEY, J.D. (Eds.): Risk in intellectual and physchosocial development. Academic Press, New York, NY, 1986.

FRANKOVA, S., BARNES, R.H.: Eftect of malnutrition in early life on avoidance conditioning and behavior of adult rats. J. Nutr., 96, 485-493 (1968).

GALLER, J. (Ed.): Nutrition and behavior. Human Nutrition: A Comprehensive Treatise. Plenum Press, New York, NY, 1984.

GALLER J.: The behavioral consequences of malnutrition in early life. In: Nutrition and Behavior. Human Nutrition: A Comprehensive Treatise. Plenum Press, New York, NY, 1984a.

GOLDSMITH, H.H., Buss, A.H., PLONIN, R., ROTHBART, M.K., THOMAS, A., CHESS, S., HINDE, R.A., MCCALL R.B.: Roundtable: What is temperament? Four approaches. Child Dev., 58, 505-529 (1987).

GOLLIN, E.S.: Development and plasticity. In: Developmental Plasticity. Behavioral and Biological Aspects of Variations in Development, E.S. GOLLIN (Ed.). Academic Press, San Francisco, CA, 1981.

GOTTLIEB, G. The psychobiological approach to developmental issues. In: Handbook of Child Psychology, P. MUSSEN (Ed.) Vol. 2, 4th Edition. Infancy and developmental psychobiology, M.M. HAITH, J.J. CAMPOS (Eds.), Wiley, New York, NY (1983).

GRANTHAM-McGREGOR, S.: Rehabilitation following clinical malnutrition. In: Malnutrition and Behavior: Critical Assessment of Key Issues, J. BROZEK, B. SCHÜRCH (Eds.), pp. 358-374. Nestlé Foundation Publication Series, Lausanne, Switzerland, 1984.

GRANTHAM-McGREGOR, S.: Social background of childhood malnutrition. In: Malnutrition and Behavior: Critical Assessment of Key Issues, J. BROZEK, B. SCHÜRCH (Eds.). Nestlé Foundation Publication Series, Lausanne, Switzerland, 1984a.

GRAVES, P.L.: Nutrition, infant behavior and maternal characteristics: a pilot study in West Bengal, India. Am. J. Clin. Nutr., 29, 305 (1976).

GRAVES, P.L.: Nutrition and infant behavior: a replication study in Katmandu Valley, Nepal. Am. J. Clin. Nutr., 31, 541 (1978).

HOROWITZ, F.D.: Exploring developmental theories: towards a structural behavioral model of development, L. ERLBAUM (Ed.), New Jersey, NJ, 1987.

JOOS, S.K., POLLITT, E.: Effects of supplementation on behavioral development in children up to the age of two years: a comparison of four studies. In: Malnutrition and Behavior: Critical Assessment of Key Issues J. BROZEK, B. SCHÜRCH (Eds.), pp. 507-519. Nestlé Foundation Publication Series, Lausanne, Switzerland (1984).

JOOS, S.K., POLLITT, E., MUELLER, W.H., ALBRIGHT D.A.: The Bacon Chow study: maternal nutritional supplementation and infant behavioral development. Child Dev., 54, 669-676 (1983).

KLEIN, P.S., FORBES, G.B., NADER P.R.: Effects of starvation in infancy (pyloric stenosis) on subsequent learning abilities. J. Pediatr., 87, 8 (1975).

KLEIN, R.E., FREEMAN, H.E., KAGAN, J., YARBROUGH, C., HABICHT, J.P.: Is big smart? The relation of growth to cognition. J. Health Soc. Behav., 13, 219-225 (1972).

KLEIN, R.E., ARENALES, P., DELGADO, H., ENGLE, P., GUZMAN, G., IRWIN' M., LASKY, R., LECHTIG R., MARTORELL, R., PIVARAL, V., RUSSELL, P., YARBROUGH C.: Effects of maternal nutrition on fetal growth and infant development. Bull. Pan. Am. Health Organ., 10, 301-316 (1976).

KLEINBAUM, D.G., KUPPER, L.L., MORGENSTERN H.: Epidemiologic Research: Principles and Quantitative Methods. Lifetime Learning Publications, Belmont, CA, 1982.

Kuo, Z.: The Dynamics of Behavior Development. An Epigenetic View. Random House, New York, NY, 1967.

LITTLE W.J.: On the influence of abnormal parturition, difficult labours, premature birth, and asphyxia neonatorum on the mental and physical condition of the child, especially in relation to deformities. Trans. Obstet. Soc. Lond., 3, 293-344 (1862).

MATA, L.J.: The Children of Santa Maria Cauque. MIT Press, Cambridge, MA, 1978.

MCCALL, R.B.: Nature-nurture and the two realms of development: a proposed integration with respect to mental development. Child Dev., 52, 1-12 (1981).

McKay H., SINISTERRA, L., McKay A., GOMEZ, H., LLOREDA, P.: Improving cognitive ability in chronically deprived children. Science, 200, 270-278 (1978).

McKINNEY, J.D.: Reflections on the concept of risk for developmental retardation: A summary. In: Risk in Intellectual and Psychosocial Development, DC, FARRAN J.D. McKINNEY (Eds.), pp. 121-125. Academic Press, New York, NY, 1986.

NAEYE, R.L.: Antenatal hypoxia and low 10 values. Am. J. Dis. Child., 141, 50-54 (1987)

POLLITT, E.: Morbidity and infant development: a hypothesis. Int. J. Behav. Dev., 6, 461-475 (1983).

POLLITT, E.: Methods for the behavioral assessment of the consequences of malnutrition. In: Methods for the Evaluation of Impact of Food and Nutrition Programmes, D.E. SAHN, R. LOCKWOOD, N.S. SCRIMSHAW (Eds.), pp. 179203. The United Nations University, Tokyo, Japan, 1984.

POLLITT, E., RICCIUTI, H.N.: Biological and social correlates of stature among children in the slums of Lima, Peru. Am. J. Orthopsychiatry, 39, 735-747 (1969).

POLLITT, E., THOMPSON, C.: Protein-calorie malnutrition and behavior: a view from psychology. In: Nutrition and the Brain, Vol. 2, R.J. WURTMAN, J.J. WURTMAN (Eds.). Plenum Press, New York, NY, 1977.

RICCIUTI, H.N.: Developmental consequences of malnutrition in early childhood. In: The Uncommon Child: Genesis of Behavior, M. LEWIS, L.A. ROSENBLUM (Eds.), VOl.3. Plenum Press, New York, NY, 1980.

RICHARDSON, S.A.: The background histories of school children severely malnourished in infancy. Adv. Pediatr., 21, 167 (1974).

RICHARDSON, S.A.: The long range consequences of malnutrition in infancy: a study of children in Jamaica, West Indies. In: Topics in Pediatrics 2. Nutrition in Childhood, B. WHARTON (Ed.). Pitman Medical, Tunbridge Wells, England, 1980.

RUSH, D.: The behavioral consequences of protein-energy deprivation and supplementation in early life: an epidemiological perspective. In: Nutrition and Behavior. Human Nutrition: A Comprehensive Treatise, J. GALLER (Ed.). Plenum Press, New York, NY, 1980.

RUSH, D., STEIN, Z., SUSSER, M.: Diet in Pregnancy: A Randomized Controlled Trial of Nutritional Supplements. Alan R. LISS, New York, NY, 1984.

RUTTER, M.: Statistical and personal interaction: facets and perspectives. In: Human Development. An Interactional Perspective, D. MAGNUSSON, V.L. ALLEN (Eds.). Academic Press, San Francisco, CA, 1983.

SACO-POLLITT, C., POLLITT, E., GREENFIELD, D.: The cumulative deficit hypothesis in the light of cross-cultural evidence. Int. J. Behav. Dev., 8, 75-97 (1985).

SAMEROFF, A., CHANDLER, M.J.: Reproductive risk and the continuum of caretaking casualty. In: Review of Child Development Research, F.D. HOROWITZ, M. HETHERINGTON, S. SCARR-SALAPATEK, G. SIEGEL (Eds.), Vol. 4. The University of Chicago Press, Chicago, IL, 1975.

SCOTT, J.P.: Critical periods in behavioral development. Science, 138, 949-958 (1962).

STEIN, Z., SUSSER, M., SAENGER, G., MAROLLA, F.: Famine and Human Development. The Dutch Hunger Winter of 1944/1945. Oxford University Press, New York, NY, 1975.

TAYLOR, L., SELOWSKY M.: The economics of malnourished children: an example of disinvestment in human capital. Econ. Dev. Cult. Change, 22, 17-20 (1973).

VALENZUELA, M., ARAYA, M.: Attachment and developmental status of chronically undernourished infants. Paper presented at the biennial meeting of the Society for Research in Child Development. Baltimore, MD, April, 1987.

WABER, D. P., VUORI-CHRISTIANSEN, L., ORTIZ, N ., CLEMENT, J.R., CHRISTIANSEN, N . E., MORA, J.O., REED, R.B., HERRERA, M.G.: Nutritional supplementation, maternal education, and cognitive development of infants at risk of malnutrition. Am. J. Clin. Nutr., 34, 807-813 (1981).

WADDINGTON, C.H.: Conceptsof development. In :The Biopsychologyof Development, E. TOBACH, L.R.ARONSON, E. SHAW(Eds.).Academic Press, NewYork, NY, 1971.

WERNER, E.: A longitudinal study of perinatal risk. In: Risk in Intellectual and Psychosocial Development, D.C. FARRAN, J.D. McKINNEY (Eds.). Academic Press, New York, NY, 1986.

WINICK, M. NOBLE, A.: Cellular response in rats during malnutrition at various ages. J. Nut., 89, 300-306 (1966).

WINICK, M., Rosso, P.: Head circumference and cellular growth of the brain in normal and marasmic children. J. Pediatr., 74, 774-778 (1969).

WINICK, M. MEYER, K.K., HARRIS, R.C.: Malnutrition and environmental enrichment by early adoption. Science, 190, 1173-1175 (1979).

ZESKIND, P.S., GOFF, D.M., HUNTINGTON, L.: A developmental approach to the study of behavioral effects of early malnutrition. In: Malnutrition and Behavior: Critical Assessment of Key Issues, J. BROZEK, B. SCHÜRCH (Eds). Nestle Foundation Publication Series, Lausanne, Switzerland, 1984.