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© 2006 American Society for Nutrition J. Nutr. 136:473-478, February 2006


Community and International Nutrition

Early Life Factors Are Determinants of Female Height at Age 19 Years in a Population-Based Birth Cohort (Pelotas, Brazil)1

Denise P. Gigante*,2, Bernardo L. Horta*, Rosângela C. Lima*, Fernando C. Barros*,{dagger} and Cesar G. Victora*

* Post-Graduate Program in Epidemiology, Universidade Federal de Pelotas, CP 464, 96001-970, Pelotas, RS, Brazil and {dagger} PAHO/WHO Latin-American Center for Perinatology and Human Development, Montevideo, Uruguay

2 To whom correspondence should be addressed. E-mail: denise{at}epidemio-ufpel.org.br.


    ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The purpose of this study was to investigate the influence of biological and social background on height of adolescent girls at age 19 y in the city of Pelotas, Southern Brazil. In 2001, a sample of the urban census tracts was visited and adolescent girls who were part of the Pelotas 1982 Birth Cohort Study were located. Standardized questionnaires were administered to the adolescents and their mothers. Height was measured using locally manufactured stadiometers; standardized protocols were employed. The information obtained in 2001 was combined with data collected in earlier phases of the study. The follow-up rate was 69% and 473 girls were studied in 2001. Multiple linear regressions were used to analyze the determinants of height. The height of the 19-y-old adolescents was 161.2 ± 6.3 cm. The significant determinants of height were family income, maternal pregestational weight, maternal height, smoking during pregnancy, birth weight, height gain, and age at menarche. Birth weight was a more important predictor than weight gain during infancy or height gain between the ages of 2 and 4 y. Each 100 g in birth weight was associated with an increase of ~0.2 cm in the adolescent's height (P = 0.001). The current findings reinforce the importance of early life factors in the determination of adult height.


KEY WORDS: • height • adolescence • cohort study

Adult height has been found to be inversely related to mortality, but this association is influenced by social background (1). Considering that the adult height attained is determined in part by factors acting during pregnancy, infancy, and childhood, the association between height and mortality is consistent with the effects of early life factors on morbidity and mortality in adulthood (2).

In a recent review, Silventoinen (3) wrote that in modern Western societies, ~20% of the variation in adult body height was due to environmental factors, whereas in poorer environments, this proportion is probably larger, with socioeconomic factors playing a greater role. The most important nongenetic factors affecting growth and adult body height are nutrition and diseases. This review concluded that body height is a good indicator of childhood living conditions, not only in developing countries but also in modern Western societies.

Even though the influence of genetic factors on adult height is known, the secular trend toward increased height observed in many countries (4) was assumed to result from improvements in nutritional intakes and reductions in infectious disease in childhood (5). Studies across 2 generations in Guatemala showed that nutritional supplementation in childhood has positive effects on both the supplemented persons and their offspring (6).

Environmental factors, such as social class, parental education, maternal smoking during pregnancy, prenatal and postnatal growth have all been related to height (711). British birth cohorts studied biological and social determinants of adult height (10,11), whereas the Guatemalan longitudinal study (9) analyzed only biological factors (prenatal and postnatal components). Although environmental and social effects on size at birth and during childhood are well described (1214) their influence on adult height is less clear. In addition, there is no study that examined both physiological and behavioral determinants of adult height in the developing world.

In Pelotas, a southern Brazilian city, a population-based birth cohort has been studied since 1982 (15). The association between anthropometric variables in early life and overweight in adolescence was investigated. Rapid growth in childhood was associated with increased prevalence of overweight in adolescence (16). In another analysis, teenage pregnancy was associated with shorter stature and higher BMI, after adjustment for previous anthropometric status, social, and biological characteristics (17).

The objective of this study was to investigate the influence of biological and social background variables on the height of 19-y-old adolescent girls. The explanatory variables under study included family income and maternal schooling indicating socioeconomic level; maternal height as an indicator of genetic potential; prenatal factors, i.e., birth weight, gestational age, maternal weight gain, and smoking during pregnancy; postnatal factors, including breast-feeding, nutritional status, and hospitalization at age 2 and 4 y; and age at menarche.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
In 1982, 5914 live-born infants were recruited and included in the Pelotas Birth Cohort Study. These children were visited several times; the latest follow-up was carried out in 2001. The methods used in the early phases of the cohort study were described elsewhere (15,18,19). In 2001, a 27% sample of census tracts in the city was visited and adolescent girls who were born in 1982 and belonged to the cohort were identified. In 70 census tracts from the Pelotas urban area, 496 eligible adolescents were identified. There were 5% losses (n = 20) or refusals (n = 3) and 473 girls had full information. Standardized questionnaires were applied to these adolescents and their mothers. The information obtained in 2001 was combined with data collected in earlier phases of the study.

Height was measured using locally manufactured stadiometers, by trained interviewers who followed standardized techniques (20).

Data on explanatory variables were obtained in different phases of the study. Information collected in 1982 included socioeconomic variables (monthly family income in minimum wages and schooling of the adolescents' mother), maternal characteristics during pregnancy (weight gain and smoking defined as smoking at least 1 cigarette/d at any time during pregnancy) and characteristics at birth (age, height and pregestational weight of the adolescents' mother, gestational age, and birth weight). Information on breast-feeding and hospitalizations was obtained at the 1983, 1984, and 1986 follow-ups. The earliest available information was used in this analysis. Total breast-feeding time was reported in months and days. Starting in wk 1 of life, almost all children received herbal teas or water. Duration of predominant breast-feeding recorded the age at which foods other than breast milk or teas or water were introduced. Children were weighed using portable scales (CMS Weighing Equipment) and their supine length (1984) or height (1986) was measured using locally manufactured boards according to international specifications (AHRTAG). Nutritional indices were expressed as a Z-score of the NCHS reference (21). Children who presented weight for height index greater than +2 Z-score were classified as overweight. Height for age and weight for age deficits were defined by a Z-score below –2.

Age at menarche was obtained in 2001 by asking the adolescent. This information was also collected in early phases of the study for a subsample of girls. Comparisons between the 1997 and 2001 follow-ups showed excellent agreement between the 2 results. The variable was analyzed as continuous or dichotomous (<13 y vs. ≥13 y).

ANOVA was used to compare means (F-test and linear trend for ordinal variable). Values are means ± SD. Linear regression was used in the crude and adjusted analyses. Multiple linear regression analysis of the determinants of attained height was carried out in accordance with a hierarchical conceptual model (Table 1), in which variables in the same level were adjusted for others or higher levels. This approach takes into account both the level of statistical significance (P < 0.2) as well as postulated hierarchical relations between the explanatory variables to identify potential confounders that required adjustment (22). The first level included socioeconomic variables (family income and maternal schooling); variables that had a P-value ≤ 0.2 were included in the next level of the analysis. Biological maternal characteristics before pregnancy (age, weight, and height) were analyzed in the second level, whereas weight gain, smoking during pregnancy, and gestational age were in the third level. Birth weight and breast-feeding duration were included in the next 2 levels. Each one was adjusted for others in higher levels. The sixth and seventh levels included anthropometrical variables and hospitalization at age 2 and 4 y, respectively. Finally, age at menarche was included in the last level.


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TABLE 1 Hierarchical model of the determinants of the height of adolescent girls at age 19 y (Pelotas, 1982–2001)

 
The effects of weight and height gains during childhood were also investigated through multiple linear regression analysis incorporating birth weight and other possible confounders. Weight gain was assessed from birth up to age 4 y and height gain between age 2 and 4 y, because information on birth length was not collected.

The proposal was approved by the Ethical Research Committee of the Federal University of Pelotas. Written informed consent was obtained from all participants.


    RESULTS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The follow-up rate, based on the number of girls born in 1982 who were expected to live in the 70 census tracts included in the study, was 69%. The height of the 473 girls was 161.2 ± 6.3 cm; the median was 161.0 cm and the range was 142.2–180.8 cm. In 2001, these girls were 18.7 ± 0.3 y old; the median was also 18.7 y and the range was 18.1–19.4 y.

The crude results (Table 2) showed a positive linear association between socioeconomic variables and height at age 19 y. Girls who belonged to poor families and whose mothers were in the lowest schooling category were ~4 cm shorter than girls from rich families whose mothers had ≥9 y of schooling. The height of the girls increased with increases in their mothers' age, pregestational weight, and height in 1982. Girls whose mothers had smoked during pregnancy were ~2 cm shorter than the others. A positive linear association was also observed between maternal weight gain during pregnancy and height at age 19 y, but gestational age did not affect height (Table 2).


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TABLE 2 Heights of 19-y-old adolescent girls according to socioeconomic and maternal characteristics (Pelotas, 1982–2001)12

 
Height increased with birth weight, and adolescents born weighing ≥4000 g were 9 cm taller than those who had a low birth weight (166.3 ± 6.1 and 157.2 ± 5.8, respectively; Table 3). Girls who were small for gestational age at birth were ~5 cm shorter than all others. Height was not associated with either total or predominant breast-feeding.


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TABLE 3 Height of 19-y-old adolescent girls according to birth and breast-feeding variables (Pelotas, 1982–2001)12

 
Adolescents who were stunted or underweight at age 2 or 4 y were 8 cm shorter at age 19 y (P < 0.05). Otherwise, adolescents who were overweight at age 4 y were taller than those who were not, but the association was significant only at 4 y of age. Adolescents who were hospitalized during childhood were shorter than those who were not hospitalized, and a borderline association was observed between age at menarche and height at age 19 y (P = 0.05). Girls who had early menarche (< 13 y) were 1 cm shorter than girls who had menarche at age 13 y or later (Table 4).


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TABLE 4 Height of 19-y-old adolescent girls according to childhood characteristics (Pelotas, 1982–2001)12

 
Results of the multiple linear regression analyses are shown in Table 5. Each independent variable was adjusted for other variables at the same or higher levels of determination (Table 1) to avoid adjustment for possible mediating factors. Among socioeconomic variables, only family income in 1982 remained associated with the subjects' height at age 19 y in the adjusted analysis, and it was included in the next level of the analysis. The apparent influence of maternal age disappeared when adjusted for family income and maternal anthropometry (height and pregestational weight). Each centimeter of maternal height was associated with a 0.5-cm change in height at age 19 y (P < 0.001) and each kilogram of maternal prepregnancy weight with a 0.1 cm change in adolescent height (P = 0.005). Compared with adolescents whose mothers smoked during pregnancy, daughters of nonsmokers were almost 1.5 cm taller at age 19 y (P = 0.03), after adjustment for family income and maternal anthropometry. On the other hand, neither maternal weight gain during pregnancy nor gestational age were associated with adolescents' height. However, gestational age (P < 0.2) was included in the next level of the analysis. The strong association between birth weight and height remained significant in the adjusted analysis. Each kilogram of birth weight changed height at age 19 y by >3 cm. Breast-feeding duration was not associated with height. The effects of hospitalization at age 2 and 4 y on adolescent's height disappeared after adjustment. Negative confounding may have occurred in the association between age at menarche and height at age 19 y when adjusted for family income; although the crude analysis showed a nonsignificant association between these variables (P = 0.14), each year of delayed menarche led to an increase of 0.5 cm in height at age 19 y, in the adjusted analysis (P = 0.003).


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TABLE 5 Linear regression analysis for height of 19-y-old adolescent girls according to socioeconomic, maternal, and childhood variables (Pelotas, 1982–2001)

 
The effects of weight and height gains during childhood are shown as a life-course plot (Fig. 1). The y-axis shows the result of multiple linear regression carried out to analyze the effects of weight and height gains during childhood on height at age 19 y adjusted for family income, maternal height, pregestational weight, gestational age, smoking during pregnancy, and predominant breast-feeding as possible confounders. Although each kilogram in birth weight increased height by 2.1 cm at age 19 y, weight gain between the ages 2 and 4 y was not associated with adolescent height. Otherwise, a positive effect of height gain was evident; each centimeter in height at age 4 y increased the adolescent's height by ~8 cm.


Figure 1
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FIGURE 1  Regression coefficient and 95% CI of weight (A) and length/height (B) obtained during childhood on height of 19-y-old adolescent girls (n = 352) after adjusting for family income, maternal height, pregestational weight, smoking during pregnancy, gestational age, and duration of predominant breast-feeding (Pelotas, 1982–2001).

 

    DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Two periods of intense activity characterize growth after birth. Height gain is greatest during infancy. During adolescence, height velocity rises sharply to a peak that equals approximately one-half of the velocity during infancy, then declines rapidly and reaches zero in adulthood. Young adults may still grow 2–3 cm between the ages of 19 and 20 y (23); therefore, our study included girls who had not necessarily completed their linear growth.

The secular trend in increased adult height was also observed in developing countries (6,24). In a prospective study, 267 children from 4 Guatemalan villages have been followed since 1969 (6). Birth weight, length at 15 d of age, and length at 2 y of age were positively associated with adult height, whereas ponderal index was not a significant predictor. Prenatal and postnatal growth were equally important determinants of height.

The literature shows that short stature in adults is associated with poorer educational status and lower socioeconomic level. This is due mainly to family background, but other environmental factors in childhood may also contribute to this association (3). The present study showed an association between socioeconomic background in childhood and height at age 19 y. In addition, the influence of maternal nutrition may represent a combination of genetic and socioenvironmental factors.

The most important nongenetic factors affecting growth and adult height are nutrition and disease. In our adjusted analyses, no association was observed between hospitalizations and height at age 19 y, but we did not have detailed information on disease episodes that did not lead to hospital admissions. Two other Brazilian studies showed that height decreased with hospitalization in childhood, but their outcome measure was height among children < 5 y old (25,26). It is possible that such an effect is no longer apparent in late adolescence.

Considering maternal height and birth weight, our results were similar to those of the 1958 British birth cohort (10), which found that parental height was positively associated with adult height in the offspring. In addition, midparental height captured the joint effects of both parents and had a stronger effect than that of either parent's height. Birth weight was also positively associated with adult height in the British cohort. Unlike in our study, the association between maternal smoking during pregnancy and height at 33 y of age disappeared after adjustment for parental height, birth weight, family size, and social class. However, the hierarchical conceptual approach used in our analyses (22,27) states that birth weight is not a true confounder of the association between smoking in pregnancy and height of the offspring; rather, it is a mediating factor. Therefore, adjusting for birth weight may lead to an underestimation of the true effect of maternal smoking. In the present study, the association between maternal smoking and height at age 19 y remained significantly associated after adjustment for family income, maternal age, weight, and height.

In the present study, breast-feeding was not associated with height at age 19 y, but the possibility of lack of power must be considered. Results of an analyses of a larger sample of 2250 adolescent men in our cohort showed that the association between total breast-feeding and height at age 18 y tended to be significant (P = 0.06), although the actual size of the effect was small (28). Longitudinal data from Israeli infants showed that despite their slower growth rate, breast-fed children reached the same final height and adult BMI as formula-fed children (29). In a 1958 British birth cohort, the effect of breast-feeding was substantially weakened in the adjusted analyses (10).

The 1958 British birth cohort showed that adult height, measured at 33 y, was accurately predicted by height measured at ages 7, 11, 16, and 33 y (30). Menarche also played a role. For example, girls with onset of menarche by age 11 y (1.62 m) were significantly shorter than those with onset after this age (1.63 m) in the 1958 British birth cohort. In the present study, height at age 19 y was 1.61 ± 0.06 m for girls with onset of menarche before age 13 y and 1.62 ± 0.06 m for those with later onset. In addition, after adjustment for confounding, the effect of age at menarche on height at age 19 y was stronger.

Our study had limitations. Losses during follow-up represented about one-third of all girls who should have been found in 2001. Analysis of the background characteristics of those who were lost to follow-up showed that there were no differences in maternal schooling, but losses were more common among girls who belonged to low-income families. Considering that adolescents from poor families were shorter, an increased effect of family income on height could be expected. On the other hand, the proportion of girls identified did not vary markedly according to birth weight. Therefore, it is unlikely that the association between birth weight and adult height is due to selection bias. Unfortunately, birth length was not collected by the study team and the first measure of length was not obtained until age 2 y. Although length at birth was not associated with BMI 20 y later in a cohort of Danish men (31), a positive association between birth length and adult height was stronger than between birth weight and adult weight in men from Norway (32).

Adult height has been positively associated with cancer risk (33), whereas an inverse association between height and cardiovascular disease was described (34). Genetic factors may be a plausible explanation; however, the associations maybe simply be a reflection of environmental factors affecting childhood growth and chronic disease. For instance, birth weight, infant feeding, diet, and parental smoking may influence both adult height and cardiovascular disease. In this study, maternal height was strongly associated with offspring height; however, environmental variables were also associated with adult height.

In conclusion, the main determinants of height at age 19 y in adolescent girls were family income, maternal pregestational weight, maternal height, smoking during pregnancy, birth weight, height gain, and age at menarche. These analyses showed that birth weight was a stronger predictor of height than weight gain during infancy taking into account negative effects of weight at ages 2 and 4 y when adjusted for birth weight. On the other hand, an adjusted effect of height at age 4 y on height at age 19 y suggests that height gain between 2 and 4 y is also important. Results from developed countries suggest that social inequalities in height are substantially reduced in subsequent generations, in parallel with economic development (35). These findings, as well as the present results, highlight the continued importance of socioeconomic and early life factors in promoting healthy long-term growth.


    FOOTNOTES
 
1 Supported by the Wellcome Trust's initiative entitled "Major Awards for Latin America on Health Consequences of Population Change." Earlier phases of the 1982 cohort study were funded by the International Development Research Center (Canada), the World Health Organization (Department of Child and Adolescent Health and Development, and Human Reproduction Programme), the Overseas Development Administration (United Kingdom), the United Nation's Development Fund for Women, the National Program for Centers of Excellence (Brazil), the National Research Council (Brazil) and the Ministry of Health (Brazil). Back

Manuscript received 26 June 2005. Initial review completed 2 August 2005. Revision accepted 17 November 2005.


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