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Discussion


The hypothesized effect of early nutritional supplementation on work capacity at adolescence was observed, particularly in males. Atole males have significantly greater VO2max values (L/min) at all ages or cohorts, while Atole females have significantly greater values only in Cohort 1. The Atole-Fresco differences in Cohort 2 males persist after controlling for SES, village size, age and level of participation in the supplementation trial.

In Cohort 2 Atole males' VO2max was significantly related to the amount of supplement consumed. This positive dose-response relationship appears to be partially, but not totally, mediated by body size, which is also responsive to the amount of supplement consumed. The unexpected negative dose-response seen in girls is difficult to explain. Because Atole-Fresco differences in VO2max are not significant in females in Cohort 2, this may represent a spurious relationship. On the other hand, this may be evidence for self-selection bias related to unmeasured characteristics of the girls who consume higher amounts of Atole.

The subjects who participated in the physical performance testing were meant to be a random subsample of all possible subjects. After two rounds of random sampling, 84 and 77% of the selected subjects in Atole and Fresco villages, respectively, consented to the performance testing. The best response rate was found in the younger subjects (<18 y) who were still in school or working around the home. These included Cohort 1 and most of Cohort 2, the groups most likely to reflect a treatment effect due to their early age at the time of supplementation. Evidence for the subsample being representative of the follow-up sample can be seen in a comparison of anthropometry and amount of supplement ingested. The small biases that occur, although not statistically significant, contribute to greater Atole vs. Fresco differences in height in the subsample than was observed for the follow-up sample. The greater heights in the subsample of Atole subjects may be due to overrepresentation of adolescents from Atole villages who consumed high quantities of supplement as young children. Thus, the subsample measured may not be a true random subsample of the follow-up sample. Therefore, the internal validity of the supplementation effect can be questioned. Appropriate statistical control for unequal participation can remove some of this disproportionate representation of Atole subjects. Supplement participation and other confounding variables (e.g., age and SES) were controlled through statistical procedures and the results in favor of better performance among Atole subjects remained significant.

Physical work capacity is affected by maturation (Bouchard et al. 1976; Kemper and Verschuur 1987). However, skeletal maturity does not differ between Atole and Fresco villages, thus disqualifying it as a confounder in this analysis. When skeletal age is used as a covariate (in place of CA) to test for Atole-Fresco differences, as done by Rivera et al. (1995) in analyses of body size and composition data, the results are unchanged.

Other individual confounders were not controlled in this analysis, but indirect evidence suggests that they probably did not play an important role in explaining the reported supplementation effects. Most prominent of these is physical activity. Evidence that this is not a serious confounder in this sample was demonstrated by Novak et al. (990) who studied physical activity patterns by questionnaire and heart rate monitoring in a subsample of 132 subjects drawn from the same subjects reported here. Males were significantly more active than females, but there was no effect of early childhood nutritional supplementation on time spent at levels of physical exertion sufficient to raise heart rates to 75% of maximum.

Another potentially important confounder is iron deficiency anemia. Preliminary analysis of hematological and iron status data for the exercise subsample indicates a very low prevalence (<5%) of anemia severe enough to compromise work capacity, and there are no differences in mean hemoglobin concentration, prevalence of anemia or prevalence of iron deficiency between Atole and Fresco villages.

The results reported here generally are consistent with those reported by other researchers examining the relationship between anthropometric status and work capacity in adolescents. The values for height and VO2max (L/min and mL/kg FFM min-) for Atole males and females are similar to those reported by Spurr and Reina (1989) for Colombian subjects who were underweight (<95% of Colombian reference for weight for-age and weight-for-height). Both the Colombian underweight children and the Atole adolescents of both sexes and all ages are below normal weight Colombian children in height and V02max (L/min). The Fresco subjects are well below the Colombian underweight children in V02max regardless of age or sex. These two study samples differ when VO2max is expressed per kg FFM (Fig. 4). Spurr and colleagues (1983, 1989) and others (Desai et al. 1984, Satyanarayana et al. 1979) consistently have reported that the differences in work capacity (VO2max in L/min) between subjects with small body size and those with normal size are eliminated when work capacity is expressed per body weight, and often the trend is reversed in favor of the smaller subjects when VO2max is expressed per kg FFM. The results from this study indicate that the differences in work capacity, although reduced, remain significant in favor of the Atole subjects after controlling for FFM. Thus, the conclusion of other investigators that the effects of small body size on work capacity are mediated through muscle mass is supported only partially in this sample of Guatemalan adolescents. Several factors could explain these differences.

FIGURE 4 Relationship between maximum oxygen consumption (VO2Wax) and fat-free mass (FFM) for subjects from all cohorts. Thickest and thinnest lines represent regression equations for each sex and nutrition group of Guatemalan subjects and corresponding symbols represent means for each of three cohorts. Lines for Call males and females represent regression equations reported for Colombian adolescents by Spurr and Reina (1989). Trends for Atole males and Colombian males are nearly identical and greater than Fresco males at any level of FFM. Atole females have lower VO2max for a given FFM than Colombian girls but higher than Fresco females. The statistical analysis for Atole-Fresco differences are reported in Table 3.

The relationship between previous nutritional status and work capacity may be nonlinear with the strongest effect seen below a threshold of nutritional status as suggested by a study of Indian male adolescents (Satyanarayana et al. 1979). Relative to the Colombian adolescents studied by Spurr and Reina (1989), the Guatemalan subjects show evidence of a greater degree of growth retardation perhaps as a result of more severe undernutrition in early life.

Another difference between the Colombian and Guatemalan studies is the way subjects were classified. The Colombian subjects, as well as those studied for similar effects in Brazil (Desai et al. 1984) and East Africa (Davies 1977), were classified by current anthropometric indicators of past and/or recent undernutrition. Because current height and weight are only proxies of past nutritional status and are themselves highly correlated to current FFM, the expression of work capacity per kg of weight and FFM would logically lead to a reduction in group differences in uncorrected VO2max (L/min). The results reported by Satyanarayana et al. (1979) are more consistent with ours, possibly because they classified nutritional status based on height during the preschool period rather than retrospectively at adolescence.

Yet another difference between the Colombian and Guatemalan studies that might explain the contrasting results is the method used to estimate FFM. By applying prediction equations for FFM developed specifically for this population, most of the bias in the equations used by other authors is reduced. Whatever differences might exist between studies in estimating FFM, they appear to be small. From Figure 4 it is clear that the slopes for the relationship between VO2max and FFM are nearly identical among the three groups (Atole, Fresco, Call) for each sex, suggesting a common effect of FFM on VO2max across different populations. However, the group differences in VO2 for a given FFM persist.

What explains the fact that differences in work capacity between Atole and Fresco subjects persist after controlling for FFM? Unfortunately, no data were collected to address this question. Future research might consider what role early malnutrition plays in the development of muscle fiber (Bedi et al.1982, Saltin and Gollnick 1983) and its oxidative capacity in later life.

The reduced VO2max of Fresco males compared with Atole males appears not to be related to differences in pulmonary ventilation during maximum exertion. Atole subjects have a significantly lower ventilatory equivalent (VE/VO2) than Fresco subjects (Table 2), which implies that less ventilation is required for a given amount of oxygen consumed. Also, because maximum heart rates are similar between Atole and Fresco groups, the oxygen pulse is significantly greater in Atole compared with Fresco subjects (Table 2). The exact mechanisms to explain how early chronic undernutrition affects respiratory or circulatory function is not known for human subjects. Future research should focus on the possible long-term or lifelong effects of early malnutrition on development of the lungs, heart and skeletal muscle.

The effects of early nutritional supplementation are much clearer in males than females, both with regard to main effects and to dose-response relationships. This does not seem to be related to differential participation in the supplementation trial or in the physical performance testing. It may be related to different levels of physical activity. Novak et al. (1990) have shown that females in this sample of adolescents are much less active than males and that the sex differences become greater with increasing age, perhaps because of culturally prescribed changes in sex roles associated with biological and social maturation. Spurr and Reina (1989) also observed similar reductions in VO2max among Colombian girls as they matured through adolescence and suggest that age changes in physical activities (Spurr and Reina 1988) might account for this pattern.

Although the results reviewed above indicate that nutrition in early childhood influences adolescent physiological status, little is known about the biological mechanisms through which malnutrition affects oxygen uptake and utilization. Also, not much is known about the practical implications of these results to everyday functioning of individuals living in developing countries.

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