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American Journal of Epidemiology Advance Access originally published online on December 7, 2006
American Journal of Epidemiology 2007 165(6):611-616; doi:10.1093/aje/kwk031
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Size at Birth and Blood Pressure in Early Adolescence: A Prospective Birth Cohort Study

Ana M. B. Menezes1, Pedro C. Hallal1, Bernardo L. Horta1, Cora L. P. Araújo1, Maria de Fátima Vieira1, Marilda Neutzling1, Fernando C. Barros2 and Cesar G. Victora1

1 Federal University of Pelotas, Pelotas, Brazil
2 Latin American Centre for Perinatology and Human Development, Pan American Health Organization/World Health Organization, Montevideo, Uruguay

Correspondence to Dr. Ana M. B. Menezes, Federal University of Pelotas, Domingos de Almeida 1146 #25, 96085-470 Pelotas, Rio Grande do Sul, Brazil (e-mail: anamene{at}terra.com.br).

Received for publication February 2, 2006. Accepted for publication July 24, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Previous studies have suggested that birth size may influence blood pressure in later life. Most of these reported inverse associations only became evident after weight or body mass index at some later age was included in the regression model. In a prospective birth cohort study in Brazil, the effect of birth size on blood pressure at age 11 years was explored. Of the 5,249 cohort members, 4,452 were interviewed. Mean systolic and diastolic blood pressures were 101.9 mmHg (standard deviation, 12.3) and 63.4 mmHg (standard deviation, 9.9), respectively. Birth weight was positively associated with blood pressure in the crude analysis, but this effect was no longer significant after adjustment for confounders. When current body mass index—a possible mediating variable—was added to the model, the association between birth weight and blood pressure tended to become negative, though not quite significant. Birth length showed a positive effect on later blood pressure regardless of the adjustments made. Head circumference, gestational age, and ponderal index were not associated with blood pressure. Children born small for gestational age had lower blood pressure values. The postulated inverse association between birth weight and later blood pressure was not confirmed in this cohort. Instead, a positive effect of birth length was detected.

birth weight; blood pressure; cohort studies; chronic disease; hypertension; infant, small for gestational age; prospective studies


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Several studies in high-income countries have investigated associations between anthropometric birth measures and chronic conditions in later life (1–14), addressing the so-called "fetal origins" hypothesis proposed by Barker et al. (15). The specific association between birth weight and blood pressure has been a frequent topic (1, 2, 4, 5, 7–15). Most early reports suggested the existence of an inverse association, but in a recent meta-analysis Huxley et al. (6) concluded that publication bias, inappropriate adjustment for current size (16, 17), and random error may explain most of these findings. Another limitation is that several studies were based on historical cohorts, relying on routinely obtained measurements and lacking information on important confounding factors. Few studies have gone beyond birth weight to investigate the role of birth length or weight/length ratios such as the ponderal index (2, 14); in addition, ascertainment of gestational age has often been missing or inaccurate. Studies from low- and middle-income countries are rare (5, 8, 9).

In this paper, we report prospective findings on a population-based birth cohort of 5,249 Brazilian adolescents born in 1993, of whom 87.5 percent were located in 2004–2005. Trained observers measured birth weight, length, and head circumference and ascertained gestational age by physical examination. Blood pressure was measured at the mean age of 11.3 years.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The study was carried out in Pelotas, a 320,000-inhabitant city in southern Brazil (18). The gross domestic product in Pelotas is below the Brazilian average, and also below the state average. In 1985, the gross domestic product of Pelotas represented 84 percent of the state mean; in 1999, this value was reduced to 70 percent, and in 2002, a further decline to 58 percent was observed (18).

In 1993, all hospital deliveries were monitored, and mothers of all live newborns were invited to join a cohort study. At that time, over 99 percent of all city deliveries occurred in hospitals. Trained interviewers applied a standardized and pretested questionnaire to mothers soon after delivery; information on weight at the beginning of pregnancy was collected retrospectively, based on maternal report.

Newborns were weighed and measured using pediatric scales (Filizola, São Paulo, Brazil) with a precision of 10 g and locally made length boards with a precision of 1 mm. Gestational age was calculated within the first 24 hours after birth by trained examiners using the method of Dubowitz et al. (19). The Dubowitz score assesses an infant for its apparent gestational age by considering both neurologic (n = 10) and external (n = 12) signs of development (19). The method of Kramer et al. (20) was used to classify children as adequate or small for gestational age; these curves provide smooth and biologically plausible means, standard deviations, and percentile cutoffs for defining small- and adequate-for-gestational-age births. Ponderal index at birth was calculated as weight in kilograms divided by length in cubic meters. Birth weight and birth length were converted into z scores using the US Centers for Disease Control and Prevention 2000 reference curves (21).

In 2004–2005, all subjects belonging to the cohort were sought. Two main strategies were used: a citywide school census and visits to the approximately 100,000 households in the city. Persons born in 1993 were linked to their cohort records and interviewed. Blood pressure was measured with an OMRON digital portable wrist monitor (OMRON, Beijing, China; margin of error: 3 mmHg) at the beginning of the interview and at its end about 60 minutes later; the mean value was used in the present analysis. It is unlikely that this small margin of error would have affected our results, because this could only have happened if measurement errors were systematic. A previous study of the validity of the monitor concluded that "the wrist monitor is not only easy to use, but also produces results very similar to those obtained by the standard indirect method" (22, p. 532). In our study, the mean difference between the first and second systolic blood pressure measurements was 2.42 mmHg; for diastolic pressure, the mean difference was 1.54 mmHg. The interquartile range was 5 mmHg for systolic pressure and 3 mmHg for diastolic pressure. Data collection, including administration of questionnaires to the adolescent and the mother, lasted approximately 60 minutes.

The fieldwork was carried out from July 2004 to March 2005. Trained interviewers conducted home visits. A random sample of 10 percent of all interviews was repeated by a supervisor for quality control purposes. Confounding variables included sex, family income in 1993, and some maternal variables: prepregnancy body mass index and smoking during pregnancy. Further information on the study methods is available elsewhere (23).

Chi-square tests were used to compare the percentages of subjects located at age 11 years according to baseline characteristics. In the crude analysis, one-way analysis of variance was used to compare mean systolic and diastolic blood pressures according to birth weight, birth length, ponderal index, head circumference, gestational age, and weight for gestational age. Multivariable analyses included linear regression using different models. The first model included sex, prepregnancy body mass index, family income, and maternal smoking during pregnancy. The second included these variables plus gestational age. Because birth measures are correlated, in the third model birth weight was also adjusted for birth length and head circumference; birth length was adjusted for birth weight and head circumference; weight for gestational age was adjusted for birth length and head circumference; and head circumference was adjusted for birth weight and length. Finally, in model 4, adjustment was also made for current body mass index (weight (kg)/height (m)2). For assessment of effect modification, these analyses were stratified by sex, weight for gestational age (small or adequate), family income (≤3, 3.1–6, or >6 Brazilian minimum wages (~US$150) per month), and skin color (White or non-White). Interaction terms were tested for significance. Models were tested for collinearity using the "vif" command in Stata (Stata Corporation, College Station, Texas).

Ethical approval was provided by the Committee for Ethics in Research of the Federal University of Pelotas Medical School, affiliated with the Brazilian Federal Medical Council. Written informed consent was obtained from mothers, and confidentiality was ensured.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
There were 5,265 livebirths in Pelotas in 1993 (23). Only 16 mothers refused to take part in the study, resulting in a cohort of 5,249 children. At the age of 11 years, 4,452 adolescents were examined. Added to the 141 persons known to have died, these adolescents represented a follow-up rate of 87.5 percent (table 1). Table 1 presents the percentages of subjects followed up in 2004–2005 according to baseline characteristics. No differences were observed for sex, birth weight, small-for-gestational-age birth, and maternal height. High family income, low birth length, preterm delivery, and normal prepregnancy body mass index were associated with slightly lower follow-up rates. In spite of these significant differences, at least 80 percent of the children in each subgroup were traced, and the highest follow-up rate (92.2 percent) was observed among those born to obese mothers.


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  		TABLE 1. Percentage of study subjects located at age 11 years, according to baseline characteristics (n = 5,249), Pelotas Birth Cohort Study, Pelotas, Brazil, 1993–2005

 
Birth weight was correlated with birth length (r = 0.76), gestational age (r = 0.50), and head circumference (r = 0.75). Other significant correlations were birth length and head circumference (r = 0.61), birth length and gestational age (r = 0.42), and head circumference and gestational age (r = 0.43). All correlation coefficients were significant at the 0.01 level.

Mean systolic blood pressure at age 11 years was 101.9 mmHg (standard deviation, 12.3), while mean diastolic pressure was 63.4 mmHg (standard deviation, 9.9). Table 2 presents mean blood pressure values according to birth weight, birth length, ponderal index, gestational age, and small-for-gestational-age birth. Systolic and diastolic blood pressure were positively associated with birth weight and birth length. Subjects with a birth weight of 3,500 g or more had a mean systolic pressure 1.5 mmHg greater than that of subjects with a birth weight under 2,500 g. The difference in diastolic pressure was 1.1 mmHg. In terms of birth length, subjects born with a length of 50 cm or more had, on average, blood pressure values 1.4 mmHg (systolic) and 0.8 mmHg (diastolic) greater than those of subjects with a birth length less than 47 cm.


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  		TABLE 2. Relation of mean blood pressure at age 11 years to birth-related and anthropometric variables in crude analyses (n = 4,452), Pelotas Birth Cohort Study, Pelotas, Brazil, 1993–2005

 
Ponderal index and gestational age were not significantly associated with blood pressure at age 11 years in this crude analysis. Adolescents who were born small for gestational age had lower mean blood pressure values (systolic: 100.5 mmHg; diastolic: 62.6 mmHg) than those born with adequate weights (systolic: 102.4 mmHg; diastolic: 63.6 mmHg). Persons born with a head circumference of 36 cm or more tended to have higher blood pressure levels, but the difference was significant only for diastolic pressure.

Table 3 presents the results of crude and adjusted analyses for systolic blood pressure. Gestational age had no effect on systolic pressure, either in the crude analysis or in the adjusted analysis. The positive association between birth weight and systolic blood pressure was reduced and no longer significant after adjustment for sex, family income, prepregnancy body mass index, and maternal smoking during pregnancy, but when gestational age was included the effect of birth weight again became significant. The regression coefficients were 0.58 in the crude model, 0.38 in model 1, and 0.46 in model 2. Additional adjustment for birth length and head circumference removed part of the effect of birth weight on systolic blood pressure (the regression coefficient in model 3 was 0.33). Extra adjustment for current body mass index produced an inverse association between birth weight and systolic blood pressure at age 11 years.


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  		TABLE 3. Relation of perinatal variables to systolic blood pressure at age 11 years (n = 4,452), Pelotas Birth Cohort Study, Pelotas, Brazil, 1993–2005

 
Birth length was directly associated with systolic blood pressure in all analyses, regardless of which covariates were included (table 3). The magnitude of the association was strengthened after adjustment for gestational age, birth weight, and head circumference.

Ponderal index was not associated with systolic blood pressure in models 1 and 2. Adjustment for current body mass index resulted in a significant inverse association between ponderal index and systolic blood pressure. The inverse association between weight for gestational age and blood pressure was consistent in models 1 and 3. Head circumference was not associated with systolic pressure (table 3).

Table 4 presents the results for diastolic blood pressure. Trends were mostly consistent with those observed for systolic blood pressure, but some differences were apparent. The association between birth length and diastolic pressure was of borderline significance in models 1 (p = 0.06) and 2 (p = 0.06) and failed to reach significance in model 3 (p = 0.10). In spite of these differences in statistical significance, the regression coefficients ranged only from 0.33 mmHg (model 1) to 0.57 mmHg (model 4). The effect of having been born small for gestational age was not significant in model 3; the regression coefficient was –0.78 mmHg, as compared with –1.09 mmHg in the crude model. There was no evidence of collinearity in the regression models presented in tables 3 and 4.


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  		TABLE 4. Relation of perinatal variables to diastolic blood pressure at age 11 years (n = 4,452), Pelotas Birth Cohort Study, Pelotas, Brazil, 1993–2005

 
All analyses were repeated after stratification by weight for gestational age. Interaction terms were tested, but none were significant at the 0.05 level. The p values for the interaction between birth weight and small-for-gestational-age birth were 0.87 for systolic pressure and 0.37 for diastolic pressure. For birth length, the respective p values were 0.29 and 0.10. Crude regression coefficients for the effect of birth weight on systolic pressure were 0.04 among small-for-gestational-age children and 0.36 among adequate-for-gestational-age children. For diastolic pressure, the respective coefficients were 0.47 and 0.72. Interactions between size at birth and sex, income, and skin color were also tested; all had p values greater than 0.25 and differences in size effects that were not relevant.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The prospective nature of this study, its population basis, the high rates of follow-up, and the use of standardized methods for birth measurements and gestational age assessment reduce the likelihood of selection and information bias. Some limitations, however, should be considered. Blood pressure was measured twice on the same day, whereas clinical recommendations involve measurements taken on different days (24). Such errors are likely to be independent of birth anthropometry. The possibility of confounding by socioeconomic status has to be considered, but no associations were found between blood pressure levels and either family socioeconomic status (at birth or current) or maternal education (data not shown). Nevertheless, to be consistent with the literature, we opted to keep family income as a covariate in the regression analyses.

Birth length was directly associated with systolic blood pressure at age 11 years, regardless of which covariates were included in the regression models. Being small for gestational age was associated with lower systolic blood pressure. The association with diastolic pressure pointed in the same direction but was not significant. Gestational age in weeks, birth weight, ponderal index, and head circumference were not consistently related to either systolic or diastolic blood pressure.

Huxley et al. (6) conducted a meta-analysis of the effect of birth weight on blood pressure, concluding that there was no clear association. Nevertheless, several studies reported an inverse association, which only became apparent after weight or body mass index at some later age was included in the regression model. However, as was discussed by Lucas and Morley (10), birth size adjusted for later size is equivalent to a measure of the effect of postnatal growth (16, 17). In the present analyses, if adjustments are made for current body mass index (model 4), both birth weight and ponderal index present significant (or nearly so) inverse associations with blood pressure. It is interesting that the positive effect of birth length would be slightly enhanced if adjustment were made for current body mass index.

The evidence on the association between birth length and blood pressure is controversial. Studies from high-income countries, where intrauterine growth restriction is rare, have either failed to report an association (2, 7, 13) or found inverse associations (1, 4, 12). On the other hand, studies from low- and middle-income settings—such as those by Kumaran et al. (8) among Indian adults and Law et al. (9) among Nigerian children—reported positive associations, in accordance with the present findings. In particular, our observation that the direct association between birth length and diastolic pressure seems to be stronger among children who underwent intrauterine growth restriction supports the presence of an effect in poor populations.

To our knowledge, only two studies have included birth weight and birth length in the same regression model (2, 14). Whincup et al. (14) reported that birth length was inversely related to blood pressure, but this association disappeared after birth weight was controlled for. Burke et al. (2) reported that neither birth weight nor birth length was associated with blood pressure when each factor was adjusted for the other. We found that the effect of birth weight was substantially reduced when birth length was included in the model, whereas inclusion of birth weight did not substantially change the effect of birth length.

The biologic mechanisms through which birth size may influence blood pressure are not clearly known. In animal studies, protein intake during pregnancy was inversely associated with blood pressure among offspring (25). In a human study, however, high maternal carbohydrate and protein intakes were positively associated with hypertension in the offspring at age 40 years (3). Further studies are needed to confirm this association and to clarify potential biologic mechanisms.

In summary, our data support a direct association between birth length and blood pressure in early adolescence and do not support an inverse association between birth weight and blood pressure in adolescence, because the negative effect of this variable on later blood pressure was apparent only after inclusion of current body mass index in the regression model—a finding that indicates an effect of postnatal growth, not of birth weight per se. As Adair and Dahly (26) mentioned in a recent systematic review, the association between birth size and later blood pressure may vary according to the level of economic development of the country of birth. Therefore, further studies from low- and middle-income countries are warranted in order to confirm or reject our findings in such settings.


   ACKNOWLEDGMENTS
 
This analysis was supported by a Wellcome Trust initiative entitled "Major Awards for Latin America on Health Consequences of Population Change." Earlier phases of the 1993 cohort study were funded by the European Union, the National Program for Centers of Excellence (Brazil), the National Research Council (Brazil), and the Ministry of Health (Brazil).

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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