Previous - Next
We hypothesized that
nutritional supplementation in early childhood would affect
positively skeletal maturation status at adolescence.
Specifically, we hypothesized that subjects supplemented with the
high energy, high protein Atole would be advanced in maturation
at adolescence compared with subjects who received the low
energy, no protein Fresco supplement. As further support of the
supplementation effect, we hypothesized that maturation at
adolescence would show a dose-response to the amount of
supplemental energy ingested in the first 3 y of life. We found
only minimal support for these hypotheses. Atole-Fresco
differences in maturation status were small (0.4 y) and
restricted to the youngest cohort of girls between 11 and 14 y of
age; also, these weak effects were attenuated after controlling
for SES. No linear dose-response to individual supplemental
energy intake was observed in the only group suitable for testing
this relationship: Cohort 2 males from the Atole villages. These
findings differ to some extent from those of Khan et al. (1995)
who found that the mean age at menarche was similar in Atole
(13.75 ± 1.22 y) and Fresco (13.74 ± 1.75 y) villages. Thus,
taken together, the studies of skeletal maturation and of
menarche suggest that the effect of improved nutrition in
childhood on maturation in adolescence is weak to absent.
As the results differ in some respects from our expectations, it is necessary to seek an explanation of our findings by examining both our original hypotheses and the various factors that may have caused the nonsignificant results of this study: sample size, study design and the influence of negative confounders.
The indicator of biological maturation chosen for this study was skeletal maturation, which is sensitive to the effects of early undernutrition. Martorell et al. (1979) reported a significant impact of the INCAP nutrition intervention (of both type and amount of supplementation) on skeletal maturation, measured by the number of hand-wrist ossification centers present in early childhood (12-36 mo). We measured skeletal maturation by the RUS option of the TW2 method,which can be used over the entire developmental period and is a more accurate and precise measure of variation in maturation at adolescence than alternative atlas methods, such as that of Greulich and Pyle (1959). The TW2 system allows for population variation in the pattern of maturation (Shakir and Zaini 1974), is robust to minor assessment problems (Van Venrooij and Van Ipenburg 1978) and assessment is neither agenor sex-dependent (Wenzel et al. 1984). In addition, the use of the RUS option allows the exclusion of the carpal bones, problematic in the adolescent age range corresponding to this sample (Johnston and Jahina 1965).
Sample sizes for Cohorts 1 and 2 of males were 220 and 223, respectively, and 220 for Cohort 1 females. SD for the mean deviation in maturation (SA deviation) of the three groups were 1.80, 1.32, and 1.41 y, respectively. Using a statistical power (1 - b) of 0.90 and a P value (a) of 0.05 to estimate z = 6.6 for a twotailed test (Snedecor and Cochran 1980), we can calculate the minimum difference (d) in SA deviation that could have been detected in this study. Solving the equation
separately for males and females of each cohort shows that sample size was sufficient to detect significant differences in the delay of maturation between the Atole and Fresco groups as small as 0.43 and 0.32 y in males of each cohort and 0.30 y in females of Cohort 1. This suggests that sample sizes within each cohort by sex group were marginally adequate to detect differences of biological significance (0.3-0.5 y).
It is probable that CA is acting as a negative confounder of the effects of early supplementation on adolescent skeletal maturation at the time of follow-up, as the age range of the subjects is 11-18 y. In wellnourished populations, skeletal maturity is reached around the age of 16 in females and 18 in males. As the skeleton approaches full maturity, SA converges with CA to reach zero difference at the completion of maturation. The variation in relative maturation status (SA deviation) used as an outcome in this study therefore decreases with age. This may explain the failure to show any dose-response in the older cohort of males. For the test of Atole-Fresco differences in each cohort, CA, along with other potential confounding factors such as village size and sex, are controlled in each analysis. But lack of variation in SA deviation in the older cohort cannot be corrected by controlling for confounders.
Cohort 1, the youngest group, had shorter, although variable, exposure to the nutrition intervention than Cohort 2 and was not expected to provide strong evidence of supplement effects on maturation at adolescence. Therefore, it is somewhat surprising that the only significant supplementation effect was seen in this younger cohort. However, it is also likely that even a limited exposure to the Atole supplement has a significant effect on skeletal maturation. Martorell et al. (1979) found a significant difference in the number of hand-wrist ossification centers between Atole and Fresco male infants as young as 12 mo of age and female infants as young as 24 mot Considering that the better test of any supplementation effect is likely to be in younger rather than older adolescents because of the age confounding effect discussed above, the carryover into early adolescence of the early supplementation effects seen in the first 2 y is plausible.
The interaction between village size and supplement group is statistically significant (P = 0.016) for Cohort 2 boys but weaker in Cohort 1 boys (P = 0.22). A significant interaction also is seen in Cohort 1 girls (P<0.001). We observed a greater positive effect of Atole supplementation in large compared with small villages. Large villages were more delayed in skeletal ma turity than small villages (Table 2). This might be interpreted as a greater potential for the intervention to have been effective in groups where the maturation process was more delayed. We have no explanation for the apparent negative effect of Atole in the small villages, especially in Cohort 2 males.
The possible persistence into adolescence of a small and selective effect of supplementation on skeletal maturity while the supplementation effects on height remain about the same as seen at 3 y (Rivera et al. 1995) suggests that the effect of delaying maturity to allow more time for catch-up growth is minimal in this population.
In conclusion, we found that type of early nutritional supplementation significantly affected skeletal maturation at adolescence, but its effect was restricted to females <14 y of age and in large villages. It is probable that the interpretation of results of this study are obscured by the advanced age of most of the subjects at the time of the measurement of skeletal maturation in adolescence. A study with a similar research design and that follows up youth and adolescents at a somewhat younger age would help to establish whether early nutritional supplementation affects maturation at adolescence. Given the central importance of maturation status in explaining variation in physical growth and performance, particularly at adolescence, and the possibility that maturation acts as a mediator of long-term nutritional effects on such outcomes, the relationship of early nutrition to later biological maturation is worthy of further attention.
ACKNOWLEDGMENTS
We thank
Hilda Castro, Elizabeth Conlisk, Edward Frongillo, Jr., John
Himes and Kimberly Suriano.
Alvear, J., Artaza, C.,
Vial, M., Guerrero, S. & Muzzo, S. (1986) Physical growth and
bone age of survivors of protein-energy malnutrition. Arch. Dis.
Child.61: 257-262.
Bailey, S. M., Gershoff, S. N., McGandy, R. B., Nondasuta, A., Tantiwongse, P., Suttapreyasri, D., Miller, J. & McCree, P. (1984) A longitudinal study of growth and maturation in rural Thailand. Hum. Biol.56: 539-557.
Billewicz, W. Z. & MacGregor, l. A. (1982) A birth-to-maturity study of heights and weights in two West African (Gambian) villages, 1951-1975. Ann. Hum. Biol. 9: 309-320.
Greulich, W. W.& Pyle, I. (1959) Radiographic Atlas of Skeletal Development of the Hand and Wrist. Stanford University Press, Stanford, CA.
Hauspie, R. C., Das, S. R., Preece, M. A. & Tanner, J. M. (1980) A longitudinal study of the growth in height of boys and girls of West Bengal (India) aged six months to 20 years. Ann. Hum. Biol. 7: 429-441.
Himes, J. H. (1978) Bone growth and development in proteincalorie malnutrition. World Rev. Nutr. Diet.28: 143-187.
Johnston, F. E. & Jahina, S. B. (1965) The contribution of the carpal bones to the assessment of skeletal age. Am. J. Phys. Anthropol.23: 349-354.
Khan, A. D., Schroeder, D. G., Martorell, R. & Rivera, J. A. (1995) Age at menarche and nutritional supplementation. J. Nutr.125: 1990S-1096S.
Marks, G. C., Habicht, J.-P. & Mueller, W. H. (1989) Reliability, dependability and precision of anthropometric measurements. The Second National Health and Nutrition Examination Survey 1976-1980. Am. J. Epidemiol.130: 578-587.
Martorell, R., Habicht, J.-P. & Rivera, J. A. (1995) History and design of the INCAP longitudinal study (1969-77) and its follow-up (1988-89). J. Nutr.125: 1027S-1041S.
Martorell, R., Rivera, J. A. & Kaplowitz, H. (1990) Consequences of stunting in early childhood for adult body size in rural Guatemala. In: Annales Nestle: Long Term Consequences of Nutrition in Infancy and Childhood. Vol 48 (International Committee of Pediatricians, eds.), Nestec Ltd., Vevey, Switzerland, pp.85-92.
Martorell, R., Yarbrough, C., Klein, R. E. & Lechtig, A. (1979) Malnutrition, body size and skeletal maturation: interrelationships and implications for catch-up growth. Hum. Biol.51: 371-389.
Rivera, J. A., Martorell, R., Ruel, M., Habicht, J.-P. a Haas, J. (1995) Nutritional supplementation during the preschool years and body size and composition in Guatemalan adolescents. J. Nutr. 125: 1078S-1089S.
SAS Insitute Inc. (1985) SAS Users Guide: Statistics, Version 5 ed. SAS Institute, Inc., Cary, NC.
Satyanarayana, K., Naidu, A. N. & Rao, B. S. A. (1980) Adolescent growth spurt among rural Indian boys in relation to their nutritional status in early childhood. Ann. Hum. Biol. 7: 359-365.
Satyanarayana, K., Radhaiah, G., Mohan, K. R. M., Timmayammma, B. V. S., Rao, N. P., Rao, B. S. N. & Akella, B. (1989) The adolescent growth spurt in height among rural Indian boys in relation to childhood nutritional background: an 18 year longitudinal study. Ann. Hum. Biol.16: 289-300.
Schrader, R. E. & Zeman, F. J. (1973) Skeletal development in rats as affected by maternal protein deprivation and postnatal food supply. J. Nutr.103: 7792-7801.
Schroeder, D. G., Martorell, R., Rivera, J. A., & Ruel, M. T. (1995) Age differences in the impact of supplement on growth. J. Nutr. 125: 1060S-1067S.
Shakir,A.&Zaini,S. (1974) Skeletal maturation of the hand and wrist of young children in Baghdad. Ann. Hum. Biol. 1: 189-200.
Snedecor, G. W. & Cochran, W. G. (1980) Statistical Methods, 7th ed. The lowa State University Press, Ames, IA.
Spurr, G. B., Reina, J. C. & Barac Nieto, M. (1983) Marginal malnutrition in school aged Colombian boys: anthropometry and maturation. Am. J. Clin. Nutr. 37: 119-132.
Tanner, J. M., Whitehouse, R. H., Cameron, N., Marshall, W. A., Healy, M. J. R. & Goldstein, H. (1983) The assessment of skeletal maturity and the prediction of adult height (TW2 method), 2nd ed. Academic Press, London, U.K.
Van Venrooi), M. E. & Van Ipenburg, A. (1978) Mixed longitudinal data on skeletal age from a group of Dutch children living in Utrecht and surroundings. Ann. Hum. Biol.5: 359-380.
Wenzel, A., Droschl, H. & Melsen, B. (1984) Skeletal maturity in Austrian children assessed by the GP and TW2 methods. Ann. Hum. Biol. 11: 173-178.
Yarbrough, C., Habicht, J.-P., Klein, R. E. & Roche, A. F. (1973) Determining the biological age of the preschool child from a handwrist radiograph. Invest. Radiol.8: 233-243.
