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This paper's analyses, which relate supplement consumption to growth rates in individuals, should be considered jointly with others reviewed by Habicht, Martorell and Rivera (1995). Even though care was taken to control for potentially confounding factors, the present results, by themselves, are open to criticism because they rely on associations involving individual, ad-libitum consumption. Elsewhere, Habicht, Martorell, and Rivera (1995) provide results using the randomized design, with village as the unit of analysis, and show that the nutrition intervention caused the changes in physical growth observed. The present analyses, as well as others reviewed by these authors that involved explorations of "dose-response", complement the randomized design analysis and add strength to a causal inference. Moreover, the present analyses add important information about the age differences in the relationship between supplement intake and growth rates, aspects that could not have been explored with the data available using the randomized design.
Nutritional supplementation of Guatemalan children had the greatest impact on growth in the first 36 mo of life. Consumption of an additional 100 kcals/d of supplement resulted in ~4-9 mm additional gain in length during the first 3 y of life with greatest benefit seen in the first year. Between 3 and 7 y of age, nutritional supplementation had no significant impact on linear growth. Impact on weight gains was greatest during the first 2 y with little benefit thereafter.
If supplement was expressed as a percent of the recommended dietary allowances, the impact of 10% of RDA consumed as supplement during any of the first 3 y of life was approximately the same as consuming 100 kcal of supplement per day. Again, no significant impact on growth was observed after three years of age. Similar patterns were seen if the impact of supplement (either kilocalories/day or as percent of RDAs) was measured as the percent of expected, rather than actual, velocity.
The results of this study are similar with others that have reported a stratified analysis of the impact of nutritional supplementation by age. Gopalan et al. (1973) found that 1- to 2-y-old Indian children who received ~170 kcal/d of supplement in the form of a sweet cake grew 2.8 cm more during 14 months compared with unsupplemented children. This difference was 1.7 cm for 2- to 3- and 3- to 4-year olds and 1.1 cm for 4- to 5 year olds. Lutter et al. (1990), comparing supplemented and unsupplemented Colombian children and examining generally shorter intervals, found that responsiveness of length and weight to supplementary feeding coincided with the initiation of weaning (3-6 mo of age) and the peak prevalence of diarrhea (9-12 mo). Using the same dataset used in the present analyses, Burger (1992) examined all 3-mo age intervals under two years and found that the 3-to 6-mo age interval was associated with the greatest impact of supplement on length gain.
The most likely explanations for these findings are associated with the relative magnitude of: growth potential as proxied by reference data, deficits in required energy intakes as proxied by the recommended energy intakes and infectious diseases, particularly diarrhea, during these years.
Linear velocity of well-nourished children is greatest during the first year of life at ~20 cm per year (Baumgartner et al. 1986). By the second and third years of life, the rate has declined to ~12 and 9 cm per year, respectively. Between the fourth and seventh years of life, healthy children grow at ~7 cm per year.
Though the lengths of the Guatemalan children in this study were near the 50th percentile at 15 d (Martorell et al. 1995), growth velocities were much less than the reference until age 36 mot The magnitude of the deficits in length gain per year coincided with rates of greatest expected growth, with the biggest difference during the first year and diminishing until the third year. After age 36 mo, length velocities were approximately as expected. As seen in Figure 2, though consumption of Atole was able to make up some of the growth deficit during the first years of life, the majority of the deficit remained.
The deficits in growth velocity seen during the first 3 y of life are likely due, in part, to inadequate nutrient intakes. Investigations from other developing countries find that the complementary foods given during the weaning period are often insufficiently dense (Ashworth and Draper 1992) or too bulky (Ljungqvist et al. 1981) to provide adequate calories and nutrients to achieve proper growth. In the current study, the fact that supplementation with Atole had an impact on growth is evidence that nutrient deficiencies were limiting growth in this population. The other primary cause of reduced growth velocity seen during these ages is infectious disease.
The negative impact of infectious disease, particularly diarrhea! illness, on growth has been well described (Black et al. 1984a, Martorell et al. 1975). In this, as in many populations in the developing world, the highest prevalence of diarrhea coincides with the weaning period when children are first exposed to pathogen containing foods (Black et al. 1982). In this population, children spent on average ~ 10-12 of every 100 d during their first 2 y with diarrhea, a rate that declined to ~ 5 d per 100 by the third year of life and about 1 d per 100 by age 7 y (Figure 6).
The effect of these high rates of diarrhea! illness on supplement intakes and growth as well as the reverse relationships are complex. Though good nutritional status has been associated with slightly decreased duration (Black et al. 1984b; Tomkinset al. 1989) of diarrhea, previous analyses of these data did not find that supplementation itself decreased diarrhea prevalence (Rose and Martorell 1992). Nutritional supplementation has, however, been found to partially (Martorell et al. 1990), and nearly completely (Luster et al. 1989), offset the negative effect of diarrhea! illness on linear growth. A similar protective effect of supplementation against growth faltering was found in relation to measles (Gopalan et al. 1973).
The results from the current study, as well as those reported from Colombia (Luster et al. 1990), suggest that supplementation is most efficacious in very young children. The issue then arises of what the lower age limit for recommending supplementation should be. In an analysis of the same Guatemalan data used here, Burger (1992) found that supplementation before 3 mo of age was associated with higher rates of diarrhea whereas children, especially girls, who began receiving supplement at between 3 and 6 mo had better growth rates compared with those who began receiving supplement after 6 mot Though both this study as well as that from Colombia (Luster et al. l 990) report benefits for children 3-6 mo of age, it is important to reiterate that these results are based on the use of supplements prepared and served under very hygienic conditions. Large-scale programs that provide supplement under less-controlled conditions may have different results.
The analyses presented here focus on a single component of nutritional supplement (energy) and anthropometric outcomes. Analyses were also carried out that use volume of supplement consumed to explore whether the effects observed could have been due to the nutrients added in equal concentration to the Atole and Fresco (i.e., iron, fluoride, thiamin, riboflavin, niacin, ascorbic acid and vitamin A; see Habicht et al. 1995 for greater details). When volume of supplement consumed was added to the regression models used to generate the combined Atole and Fresco results presented in Table 2, the statistical significance of the variable representing energy from supplement was far greater than that for volume during the first three yearly intervals. Only in the 60- to 72-mo age interval did the variable for volume show a similar level of impact relative to energy. Though these analyses are suggestive that the effects observed are more likely to have been caused by energy as opposed to the other nutrients in the supplements, the issue as to which nutrient or combination of nutrients were responsible remains unsettled. Protein, which the Atole but not the Fresco contained, also could have caused the changes observed. There is little evidence that the Fresco had a nutritional effect (Table 3) which enhances the case for a protein effect. However, the results could be ascribed just as easily to energy; so little energy was contributed by Fresco in the first 3 y of life that an effect would be unlikely, even if energy provided the explanation. Clearly, the fact that energy intakes from both supplements were not similar in children precludes the type of convincing analyses carried out in pregnant women where it was shown that energy and not protein provided a better explanation for the effects on birthweight (Habicht 1995). Additional discussion of the difficulty of differentiating the contribution of energy and other nutrients is found elsewhere in this volume (Habicht et al. 1995). Although there is uncertainty about the nutrient or nutrients responsible for the effects observed, the analyses presented here, together with those given by Habicht, Martorell and Rivera (1995), leave no doubt that ingestion of the Atole c aused children to grow better.
Linear growth was of most interest in these analyses because the Guatemalan population is heavily stunted but not wasted. Patterns of wasting and stunting vary drastically throughout the world (Victora 1992); age-specific responsiveness to nutritional supplementation is also likely to vary. In populations where wasting is the main concern, analyses may prioritize examining the age-specific impact of nutritional supplementation on weight gain.
Finally, there are certainly other benefits of nutritional supplementation besides growth (Beaton 1993). Supplementation has been shown to positively affect functional capabilities such as activity level, literacy, and school performance (Pollitt and Gorman 1990) - outcomes that might be most responsive to nutritional supplementation in older rather than younger childhood.
The authors thank Dr. Edward Frongillo of Cornell University for his assistance in developing the analytical strategy used in this paper.
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