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ORIGINAL RESEARCH COMMUNICATION |
1 From the Division of Biological and Biomedical Sciences, Nutrition and Health Sciences Program, Emory University, Atlanta (HL, ADS, UR, and RM), and the Departments of International Health (ADS, UR, and RM) and Biostatistics (HXB), Rollins School of Public Health, Emory University, Atlanta.
2 Supported by grants from the NIH (HD-29927) and the Nestlé Foundation, Lausanne, Switzerland.
3 Address reprint requests to R Martorell, Department of International Health, Rollins School of Public Health, Emory University, 1518 Clifton Road, NE, Atlanta, GA 30322. E-mail: rmart77{at}sph.emory.edu.
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ABSTRACT |
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Objective: We assessed associations between prenatal and postnatal growth (0–2 y of age) and ABSC.
Design: We included 267 singletons from a prospective study carried out between 1969 and 1977 in 4 ladino Guatemalan villages. We used data from that study and from a follow-up study conducted in 1998–1999 (when the subjects were 21–27 y of age) to determine associations of birth weight, length at 15 d of age, ponderal index, and length at 2 y of age with adult height, weight, fat-free mass (FFM), fat mass, percentage of body fat, and waist-to-hip ratio. Multivariate linear regression analyses with mixed models were carried out to account for sibling clustering. Two-stage least-squares analyses were used to separate specific effects of prenatal and postnatal growth.
Results: Birth weight, length at 15 d of age, and length at 2 y of age were positively associated with height, weight, and FFM in both sexes (P < 0.05). Prenatal growth and postnatal growth were equally important determinants of height, weight, and FFM. Weak positive associations of postnatal growth with adult fat mass and percentage of body fat were found in both sexes, whereas similar associations for prenatal growth were found in women only. Growth in early childhood was not related to waist-to-hip ratio.
Conclusions: Growth retardation in early childhood was associated with shortness and less FFM in adulthood. Preventing growth failure in utero and preventing growth failure during the first 2 y of life are equally important for ABSC.
Key Words: Stunting • early childhood • prenatal growth • postnatal growth • adulthood • body size • body composition • longitudinal study • Guatemala
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The effect of growth in early childhood on adult body size and composition has been the subject of much study in the past 2 decades. Most investigators agree that linear growth retardation or stunting in early life increases the risk of shortness in adulthood and results in low fat-free mass (FFM) (13–20). Undernutrition in early life may play a role in promoting chronic metabolic diseases (the "early origins" hypothesis) (21). However, evidence that stunting in early childhood increases fatness later in life remains inconclusive (22).
Most of the studies linking growth in early childhood to later body size and composition were carried out in developed countries. A Guatemalan study of subjects born in 4 rural villages is among the few conducted in a developing country (13). That study focused on assessing the consequences of intrauterine growth retardation for adult body size and found that the differences between subjects with or without intrauterine growth retardation (ie, 
5 cm in height and 5 kg in weight) were similar to those found in studies from developed countries. However, a limitation of this Guatemalan study was that it included subjects as young as 11 y of age at the time of measurement, which required adjustment for maturation and thus added complexity to both the analysis and the interpretation of results. A problem not addressed adequately to date by any study is quantification of the relative importance of prenatal and postnatal growth for adult body size and composition. The current study is an extension of the prior Guatemalan report (13). We analyzed the most recent follow-up data collected when the subjects were 21–27 y of age. The objectives were to estimate the overall associations between growth in early childhood and adult body size and composition and to assess the relative importance of prenatal and postnatal growth for adult body size and composition.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Exclusions
Participants who had missing data on adult body size and composition, birth length (BL; length at 15 d of age), or confounders (gestational age, maternal height, socioeconomic status in early childhood, age at follow-up, physical activity, residency, or smoking status) were excluded from the analysis. We also excluded participants with missing data on length at 2 y of age, which could not be imputed by the multiple imputation technique (described below). The final sample for analysis consisted of 267 subjects (136 males and 131 females), or 75% of the eligible subjects.
Measurements and variables
Trained field workers used standard methods to obtain all measurements (23). The quality of collected data was closely monitored (25).
The 1969–1977 longitudinal study focused on women during pregnancy and on preschool children. BW, BL, and ponderal index were selected as indicators of prenatal growth. Length at 2 y of age (L2y) was selected to indicate growth in early childhood. Weight-for-age or length-for-age z scores were calculated according to the recently revised 2000 CDC Growth Charts (26). Before z score calculation, 1 cm was subtracted from the length values of children aged ≥ 24 mo to make the values equivalent to height values (27). Data on gestational age, maternal height, and socioeconomic status during childhood from the original 1969–1977 study were also included in the analyses. The 1998–1999 follow-up study provided information on age at follow-up, adult lifestyle habits (physical activity, urban or rural residency, and smoking status), and adult body size and composition, including height, weight, FFM, fat mass (FM), percentage of body fat (%BF), and waist-to-hip ratio (WHR). FFM, FM, and %BF were estimated with the use of predictive equations from hydrostatic weight measurements in a similar population (M Ramirez, unpublished data, 2002). The variables selected are listed in Table 1
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Model development
Multivariate linear regression analyses were used to test associations between growth in early life and adult body size and composition. All final models for weight, FFM, FM, %BF, and WHR were adjusted for confounders in early childhood and in adulthood. Models for height were adjusted for factors in early childhood only because adult height is unlikely to be affected by factors in adulthood (age of young adults and lifestyle habits). Because some subjects were siblings (33 males and 26 females), mixed-effect models were used to account for clustering. Two-stage least-squares analyses were conducted to separate the contributions of prenatal and postnatal components to each adult outcome. Because prenatal growth influences postnatal growth, the measure of postnatal growth needed for our analyses had to be adjusted to remove this influence. In other words, for appropriate assessment of the influence of each component, the measure of postnatal growth used had to be independent of prenatal growth. Specifically, L2y was modeled on BL to estimate predicted L2y. Then the residual (observed L2y - predicted L2y) was calculated. In regressions, BL was used as the measure of prenatal growth, and the residual, which is independent of the prenatal component, was used as the measure of postnatal growth. The relative contributions of the prenatal and postnatal components to each adult outcome were examined by using Student’s t test, and the means and 95% CIs of the ß estimates were compared.
Adult body size and composition were also compared between the following 4 groups categorized by BL and postnatal increment in length (changes between ages 15 d and 2 y): SS, BL and postnatal increment in length below their respective medians; SL, BL below the median but postnatal increment in length above the median; LS, BL above the median but postnatal increment in length below the median; and LL (the reference group), BL and postnatal increment in length above their respective medians. All analyses were carried out for males and females separately with the use of SAS software (version 8.2; SAS Institute Inc, Cary, NC).
Effect size
In regression analysis, effect size can be defined as the absolute change in SD units in the outcome variable per 1-SD change in a predictor (31). Effect size is a useful concept both for presenting results and for performing power analyses. Although 2 predictors, such as BL and L2y, have the same units, it is difficult to compare relative effects directly from the variables estimated (changes in the outcome per 1-unit change in the predictor) from the model because their SDs differ (eg, 1 SD for males: BL, 2.3 cm; L2y, 3.8 cm). Expressing effects in SD units eliminates this problem. Furthermore, using effect size allowed us to compare not only effects (on the same outcome) of predictors with similar units but different SDs (eg, BL compared with L2y) but also effects (on the same outcome) of predictors with different units (eg, length compared with head circumference) or even effects on different outcomes (eg, effects on adult height compared with effects on FFM). In power analysis, effect sizes of magnitudes 0.1, 0.3, and 0.5 are considered small, medium, and large, respectively (31).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Eleven percent of the newborns were stunted (length-for-age z score ≤ -2). During the first 2 y of life, length-for-age z scores decreased rapidly until 18–24 mo of age, when 75% of the children were stunted (data not shown). The males and the females were equally stunted and did not differ significantly in any variable during early childhood. Age at follow-up was between 21 and 27 y for both the males and the females. The subjects who were excluded from the analysis (41 males and 48 females) did not differ significantly from our analytic population (136 males and 131 females) in size at birth, at 2 y of age, and during adulthood; in factors in early childhood (gestational age, maternal height, and socioeconomic status during childhood); in factors during adulthood (age at follow-up, physical activity, residency, and smoking status); and in the percentage of males (data not shown). Subjects who had imputed L2y data (15 males and 10 females) also did not differ significantly from those with measured L2y (121 males and 121 females) in any of the variables selected (data not shown). Results are presented in 2 parts: 1) associations of growth during early childhood with adult body size and composition and 2) relative contributions of the prenatal and postnatal components.
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. The corresponding effect sizes are shown in Table 4.
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Relative contributions of prenatal and postnatal components
Specific absolute changes in adult outcomes associated with sample-specific 1-SD increments in prenatal (BL) or postnatal (residual) components are presented in Table 5. Both the prenatal and postnatal components were positively associated (P < 0.05) with adult height, weight, and FFM in the males and the females. The postnatal component was also positively associated (P < 0.05) with FM and %BF in both the males and the females, whereas the prenatal component was a significant predictor (P < 0.05) of FM and %BF in the females only. Neither the prenatal nor the postnatal component was associated with WHR in the males or the females either before (Table 5) or after adjustment for adult body mass index (BMI; in kg/m2) or %BF (data not shown). Mean specific effect sizes (and 95% CIs) for adult body size and composition per 1-SD increments in prenatal and postnatal components are shown in Figure 1. For adult height, weight, and FFM, both the prenatal and postnatal components had positive, medium effect sizes in both the males and the females. For FM and %BF, both the prenatal and postnatal components had small effect sizes among the females; but among the males, only the postnatal component had such effects.
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. Within each sex, the subjects in the SS, SL, and LS groups were significantly shorter and lighter (P < 0.05) than the subjects in the LL group and had significantly less FFM (P < 0.05) than did the subjects in the LL group. The subjects in the SS group were the shortest and lightest and had the least amount of FFM among the 4 groups, whereas the SL and LS groups were similar to each other and intermediate between the SS and LL groups. In the males, no significant differences were found between the 4 groups in FM, %BF, and WHR. The females in the SS, SL, and LS groups had less fat (FM and %BF) than did those in the LL group (P < 0.05 for both).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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2 y of age. z Scores changed little after this age.
The current study also used more appropriate methods and statistical techniques than were used in the previous study (13). First, the recently revised 2000 CDC Growth Charts (26) were used to characterize growth in this study. These charts are considered more appropriate because they were developed on the basis of recently available comprehensive national data and improved statistical procedures (32). Second, the multiple imputation technique was applied to increase statistical power by imputing L2y when L2y was missing and thereby increasing sample sizes 10%. Third, compared with the analyses in the earlier study, the analyses in the current study were based on linear regression with BW and BL as continuous variables, which increased statistical power. Fourth, the PROC MIXED procedure, rather than general linear regression analysis, was used to correct for sibling clustering. Finally, we used two-stage least-squares analyses to appropriately evaluate the relative contribution of prenatal and postnatal growth to adult outcomes.
The findings from the current study about the importance of stunting in early childhood for adult body size and composition are consistent with those of the previous follow-up study (13). Stunting resulted from growth retardation in utero and during the first 2 y after birth. The median length of both the male and the female Guatemalan newborns was 2 cm less than that of the newborns in the reference population (ie, 1 SD below the reference means). By 2 y of age, the difference increased to 9 cm (2.5–2.7 SDs below the reference means). On the other hand, on the basis of the third National Health and Nutrition Examination Survey (NHANES III; 33), Mexican Americans, who are similar to Guatemalans in ancestry, are slightly taller at these ages than the subjects in the reference population. Our study suggests that a 1-SD increment in L2y (3.8 cm in males and 3.1 cm in females), which can be viewed as the sum of both the prenatal and postnatal components, results in increments of 3.6 cm in height, 3.4 kg in weight, and 3.5 kg in FFM in males and of 2.6 cm in height, 4.2 kg in weight, and 1.9 kg in FFM in females. Correspondingly, the effect sizes were around 0.3 and are considered medium in magnitude.
Our results do not show that retardation in length during early childhood increases fatness later in life, as some have reported (20, 34–38). Rather, our findings suggest that subjects, particularly females, who are growth retarded during early childhood are thinner as adults. Among children with better growth in early childhood, the possible tradeoffs between increased fatness and increased height and FFM in adulthood need to be considered. This is more of an issue among women. In the current study, the effects of growth during early childhood on adult fatness were greater and more consistent among the women than among the men. In addition, the men were relatively lean, whereas many of the women were overweight (BMI > 25). The mean (± SD) BMI values in the men and the women were 22.2 ± 2.4 and 23.8 ± 4.0, respectively; 10.3% of the men and 29.0% of the women were overweight. The tradeoff for women would pit the health risks of overweight against the benefits of greater stature and FFM for reproductive outcomes. In addition, survival to adulthood, which is enhanced by greater growth during early childhood, needs to be considered (39). We also found that the prenatal and postnatal (first 2 y of life) periods are equally important for adult height, weight, and FFM and that these effects are of medium size. Among the women, both the prenatal and postnatal components were also positively associated with fatness (FM and %BF), but the corresponding effect sizes were much smaller than those for height. Among the men, only the postnatal component showed these associations with fatness. In other words, the prenatal component had no effect on fatness in the men. Neither the prenatal nor the postnatal component was significantly associated with fat patterning, as measured by the WHR, among the men or the women, and this was the case either before or after adult BMI or %BF was taken into account.
Our findings suggest that growth retardation during gestation and the first 2 y of life has powerful influences on adult body size and composition. The men who were below the median in growth in length during both the prenatal and postnatal periods (ie, the SS group) were 9 cm shorter and 6.4 kg lighter than those who were above the median value during both periods (ie, the LL group) and had 6.5 kg less FFM than did the subjects in the LL group (Table 6
). For the women, the corresponding differences were 5 cm in height, 11.8 kg in weight, and 4.9 kg in FFM. These differences are very large and are likely to have important functional implications. All of the difference in weight between the men who were growth retarded during gestation and early childhood and those who were not was accounted for by FFM, whereas in the women, the difference was attributable to both FFM and FM. On the basis of the work edited by Barker (21), one would predict greater fatness in subjects with consistently poor growth during prenatal and postnatal periods or with poor prenatal growth and good postnatal growth than in those with consistently good growth (the SS or SL group compared with the LL group, Table 6). However, we found no differences among the males in either comparison but less fatness among the females in the SS and SL groups than in the LL group. Our findings support the notion that in countries where maternal and child malnutrition are common, pregnant women and young children should be the priority groups for program targeting and interventions.
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ACKNOWLEDGMENTS |
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This article is an extension and refinement of previous work performed by a group led by RM. HL developed the analytic plan with assistance from HXB, UR, ADS, and RM. RM, ADS, and UR contributed to data collection and supervision. Data analyses were executed by HL. HL and RM had primary responsibility for writing, but all the authors provided substantive and editorial comments on several drafts. None of the authors had any financial or personal conflict of interest with respect to the material reported in this article.
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REFERENCES |
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
; females, 
) or postnatal (males, 
; females, 
) components. PROC MIXED was used to account for sibling clustering. Sample-specific SDs were as follows: prenatal component (birth length), 2.3 and 1.9 cm for the males and the females, respectively; postnatal component (residual = observed length at 2 y of age - predicted length at 2 y of age), 3.5 and 2.8 cm for the males and the females, respectively. Height was adjusted for socioeconomic status during early childhood, maternal height, and gestational age. All other adult outcome variables were adjusted for socioeconomic status during early childhood, maternal height, gestational age, age at follow-up, physical activity, smoking, and residency.