Abstract
BACKGROUND/OBJECTIVES:
To investigate sex-specific associations of birth weight with body mass index (BMI), waist circumference (WC) and waist-to-hip ratio (WHR) in mid-to-late adulthood.
SUBJECTS/METHODS:
ELSA-Brasil is a multicenter cohort study of adults aged 35–74 years affiliated with universities or research institutions of six capital cities in Brazil. After exclusions, we investigated 11 636 participants. Socio-demographic factors and birth weight were obtained by interview. All anthropometry was directly measured at baseline. We categorized birth weight as low (⩽2.5 kg); normal (2.5–4 kg) and high (⩾4 kg). We performed analysis of covariance (ANCOVA) for continuous outcomes and ordinal logistic regression for categorical adiposity outcomes. We examined interaction on the multiplicative scale by sex and by race.
RESULTS:
High birth weight uniformly predicted greater overall and central obesity in men and women. However, low (vs normal) birth weight, in ANCOVA models adjusted for participant age, family income, race, education, maternal education, and maternal and paternal history of diabetes, was associated with lower BMI, WC and WHR means for men, but not for women (Pinteraction = 0.01, <0.0001 and <0.0001, respectively). In similarly adjusted ordinal logistic regression models, odds of obesity (odds ratio (OR) = 0.65, 0.46–0.90) and of being in the high (vs low) tertile of WC (OR = 0.66, 0.50–0.87) and of WHR (OR = 0.79, 0.60–1.03) were lower for low (vs normal) birth weight men, but trended higher (BMI: OR = 1.18, 0.92–1.51; WC: OR = 1.21, 0.97–1.53; WHR: OR = 1.44, 1.15–1.82) for low (vs normal) birth weight women.
CONCLUSIONS:
In this Brazilian sample of middle-aged and elderly adults who have lived through a rapid nutritional transition, low birth weight was associated with adult adiposity in a sex-specific manner. In men, low birth weight was associated with lower overall and central adult adiposity, while in women low birth weight was generally associated with greater central adiposity.
INTRODUCTION
The number of overweight and obese adults has increased from 857 million in 1980 to 2.1 billion in 2013, making this global epidemic one of the greatest public health challenges facing our generation. Rates in low- and middle-income countries seem to be rising faster than high-income countries.1 In the Brazilian scenario, 57%, or 82 million adults, have excess weight, and women are more affected than men.2
Multiple lines of evidence suggest an in utero provenance for overall and central adult obesity. Compared with adults born with normal birth weight (2.5–4 kg), those born with high birth weight (>4.0 kg) are at greater risk of becoming overweight or obese as an adult, but the association between low birth weight (<2.5 kg) and adult obesity is less clear.3 The association between low birth weight and adult obesity may be obscured by sex differences. Famine studies show that in utero caloric deprivation is associated with adult adiposity in a sex-specific manner, with stronger associations in women than in men.4–6 To the best of our knowledge, cohort studies have not comprehensively evaluated sex differences in the association of low birth weight with measures of overall and central adiposity in middle-aged and elderly adults.
To address this issue, we examined sex-specific associations of birth weight with measures of body mass index (BMI), waist circumference and waist-to-hip ratio in middle-aged and elderly Brazilian men and women, born at a time of food insecurity and now living in a notably obesogenic environment.
MATERIALS AND METHODS
Study design and population
This investigation is based on cross-sectional data from the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil), a multicenter cohort enrolling participants from 2008 to 2010 investigates diabetes, cardiovascular diseases and other related chronic conditions. We invited active and retired employees of selected public institutions of higher education and research located in six capital cities to participate, as previously detailed.7,8 From a total of 15 105 ELSA participants, we excluded 2228 lacking information on birth weight, 915 who indicated twin births or prematurity, 6 lacking waist circumference, hip circumference or BMI, and 320 lacking data on covariates, leaving 11 636 in the analytic sample. The institutional review boards of the six institutions conducting the study approved ELSA-Brasil. We obtained written informed consent from all participants.
Exposure assessment
At baseline exam, we asked participants to recall their weight at birth as ‘<2.5 kg’, ‘2.5–4 kg’, ‘>4 kg’, or as ‘I do not know’. These first three categories were defined as low birth weight, normal birth weight and high birth weight, respectively.
Covariate assessment
History of paternal diabetes was ascertained by asking participants ‘Was your father diagnosed with diabetes?’ and history of maternal diabetes as ‘Was your mother diagnosed with diabetes?’. Participants who answered, ‘I don’t know’ to either of these parental history of diabetes questions were categorized as ‘no’ for each respective covariate in this analysis. Maternal educational attainment was ascertained by asking participants ‘What was the highest level of education that your mother completed?’. Prematurity was assessed by asking participants, ‘Were you born preterm?’.
Outcome ascertainment
We obtained several anthropometric measures using internationally standardized protocols.9 Waist circumference and weight were measured when fasting and with an empty bladder at the research clinics. During measurement, participants dressed in standardized clothing without eyeglasses and other personal objects. We measured height to the nearest 0.1 cm (Seca-SE-216, Hamburg, Germany). We obtained waist and hip circumferences with a 150-cm inelastic measuring tape (Mabis-Gulick, Waukegan, IL, USA), waist circumference being obtained at the midpoint between the inferior edge of the costal border and the iliac crest, in the mid axillar line, and hip circumference at the maximum posterior protrusion of the gluteus muscles, when viewed laterally. We measured body weight with an electronic scale with maximum capacity of 300 kg (Toledo, São Bernardo do Campo, Brazil). Quality control measures were uniform across all centers.10 BMI was calculated as measured weight (kg) divided by measured height squared (m2). We defined waist-to-hip ratio as the ratio of these two circumferences.
Data analysis
We describe socio-demographic and anthropometric characteristics of participants with absolute and relative frequencies for categorical variables and means (standard deviations) for continuous ones. We compared adjusted means of adiposity measures across birth weight categories with analysis of covariance (ANCOVA). We fit ordinal logistic regression (partial proportional odds) models to evaluate the relationship between birth weight (three ordinal categories, with the middle one (2.5–4 kg) as the reference category) and adiposity measures (also three ordinal categories, with the lowest as the reference category). For overweight and obesity, we adopted conventional cutoffs established by the World Health Organization.11 For waist circumference and waist-to-hip ratio, we used tertiles as cutoffs are not consensual and even those recommended for waist circumference in the definition of the metabolic syndrome differ according to population groups.12 We tested interactions with sex and race (white vs non-white). We conducted all statistical analyses with SAS version 9.3 (SAS Institute Inc., Cary, NC, USA), and defined statistical significance at P<0.05.
RESULTS
Our sample of 11 636 participants comprised 5254 men and 6382 women. The mean age was 51.3 (s.d.: 8.8) years and net monthly family income per capita was R$1452.25 (interquartile range: R$726.13–R$2282.25). Low birth weight (<2.5 kg) was reported by 608 (5.3%) and high birth weight (>4 kg) by 911 (7.9%) participants. More than half (54.9%) of participants reported white race/skin color (the typical approach to classifying ethnicity in Brazil), while 27.1% reported brown (‘pardo’), and 15.0% black, 2.2% Asian origin and 0.9% declared themselves Amerindian. More than half of the sample (55.9%) had a university degree, while only 6.9% of their mothers reached this level of educational attainment. Maternal history of diabetes was reported by 2355 (20.2%) participants, and paternal history of diabetes by 1555 (13.4%) participants.
In Table 1, we present baseline characteristics separately for men and women according to birth weight categories. For both sexes, birth weight was positively associated with white race/skin color, participant educational attainment and the educational achievement of the participant’s mother. Participants who reported a high birth weight were more likely to have parents with a history of diabetes. Those reporting a low birth weight were more likely to have a maternal history of diabetes. Among men only, birth weight was inversely associated with age at baseline.
Table 1.
Characteristics of 11 636 adult participants from ELSA-Brasil, according to sex and birth weight
| Characteristica |
Birth weight categories |
|||||||
|---|---|---|---|---|---|---|---|---|
|
Men |
Women |
|||||||
| <2.5 kg (n = 277) | 2.5–4 kg (n = 4447) | >4 kg (n = 530) | P-value | <2.5 kg (n = 346) | 2.5–4 kg (n = 5642) | >4kg (n = 394) | P-value | |
| Age | 52.6±9.0 | 51.4±9.1 | 50.4±9.0 | 0.0049 | 51.9±8.2 | 51.3±8.7 | 51.1±8.3 | 0.3547 |
| Race/color | ||||||||
| White | 116 (41.9) | 2 478 (55.7) | 319 (60.1) | <0.0001 | 165 (47.7) | 3073 (54.5) | 232 (58.9) | 0.0299 |
| Brown | 97 (35.0) | 1301 (29.3) | 136 (25.7) | 104 (30.1) | 1427 (25.3) | 90 (22.8) | ||
| Black | 47 (17.0) | 553 (12.4) | 62 (11.7) | 66 (19.1) | 949 (16.8) | 64 (16.2) | ||
| Asian origin | 10 (3.6) | 75 (1.7) | 3 (0.6) | 11 (3.2) | 152 (2.7) | 6 (1.5) | ||
| Amerindian | 7 (2.5) | 40 (0.9) | 10 (1.9) | 0 (0.0) | 41 (0.7) | 2 (0.5) | ||
| School achievement | ||||||||
| <Complete primary | 35 (12.6) | 261 (5.9) | 28 (5.3) | <0.0001 | 17 (4.9) | 135 (2.4) | 9 (2.3) | 0.0022 |
| Primary | 42 (15.2) | 325 (7.3) | 28 (5.3) | 22 (6.4) | 248 (4.4) | 12 (3.0) | ||
| Secondary | 112 (40.4) | 1489 (33.5) | 157 (29.6) | 134 (38.7) | 1951 (34.6) | 127 (32.2) | ||
| University | 88 (31.8) | 2372 (53.3) | 317 (59.8) | 173 (50.0) | 3308 (58.6) | 246 (62.4) | ||
| Mother’s schooling | ||||||||
| <Complete primary | 190 (68.6) | 2375 (53.4) | 259 (48.9) | <0.0001 | 218 (63.0) | 3093 (54.8) | 208 (52.8) | 0.0339 |
| Primary | 40 (14.4) | 893 (20.1) | 113 (21.3) | 57 (16.5) | 1176 (20.8) | 78 (19.8) | ||
| Secondary | 40 (14.4) | 861 (19.4) | 109 (20.6) | 55 (15.9) | 981 (17.4) | 83 (21.1) | ||
| University | 7 (2.5) | 318 (7.1) | 49 (9.2) | 16 (4.6) | 392 (6.9) | 25 (6.3) | ||
| Mother had diabetes | ||||||||
| Yes | 59 (21.3) | 861 (19.4) | 128 (24.1) | 0.0282 | 76 (22.0) | 1110 (19.7) | 121 (30.7) | <0.0001 |
| Father had diabetes | ||||||||
| Yes | 16 (5.8) | 552 (12.4) | 72 (13.6) | 0.0027 | 50 (14.4) | 802 (14.2) | 63 (16.0) | 0.6223 |
| Body mass index (kg m−2) | 26.3±4.7 | 27.0±4.2 | 28.1±4.7 | <0.0001 | 27.1±5.2 | 27.0±5.0 | 28.5±5.9 | <0.0001 |
| Waist circumference | 92.4±11.5 | 95.3±11.5 | 98.2±12.5 | <0.0001 | 88.1±3.0 | 87.4±12.3 | 91.8±14.5 | <0.0001 |
| Waist-to-hip ratio | 0.94±0.07 | 0.95±0.07 | 0.95±0.07 | 0.2393 | 0.86±0.08 | 0.85±0.07 | 0.86±0.08 | <0.0001 |
Abbreviation: ELSA-Brasil, Brazilian Longitudinal Study of Adult Health.
Mean ± s.d. or N (%).
In ANOVA, we found statistically significant interactions between sex and birth weight categories (all P-values for interaction <0.05), and thus performed all additional analyses stratified by sex. We found no evidence of interaction between race/ethnicity (white vs non-white) and birth weight categories in relation to adult adiposity outcomes (Pinteraction: BMI = 0.44, waist circumference = 0.34; waist-to-hip ratio = 0.12).
Table 2 presents multivariable adjusted means of BMI, waist circumference and waist-to-hip ratio across birth weight categories. In men, we found means of all three adiposity measures increased monotonically with higher birth weight categories. Among women, instead of linearity, J- or U-shaped patterns were seen. Compared to women with normal birth weight, those with high birth weight had higher mean values for all adiposity measures. Compared to women with normal birth weight, those with low birth weight had similar BMI and waist circumference means, but a higher mean waist-to-hip ratio (Figure 1). Statistical testing demonstrated significant sex differences comparing those with low to normal weight (BMI: Pinteraction = 0.01; waist circumference and waist-to-hip ratio: Pinteraction<0.0001), but not comparing those with high to normal weight (Pinteraction ⩾ 0.18).
Table 2.
Adjusteda means (and 95% confidence intervals) of body mass index, waist circumference and waist-to-hip ratio, according to sex and birth weight categories in adults 35–70 years of age in ELSA-Brasil
| Birth weight categories | Body mass index, kg m−2 | Waist circumference, cm | Waist-to-hip ratio |
|---|---|---|---|
| Men | |||
| <2.5 kg | 26.7 (26.1–27.2) | 94.0 (92.6–95.5) | 0.95 (0.94–0.96) |
| 2.5–4 kg | 27.6 (27.4–27.9) | 97.5 (97.0–98.1) | 0.96 (0.96–0.97) |
| >4 kg | 28.9 (28.5–29.4) | 100.7 (99.6–101.8) | 0.97 (0.96–0.97) |
| Women | |||
| <2.5 kg | 27.7 (27.2–28.3) | 90.2 (88.9–91.6) | 0.87 (0.87–0.88) |
| 2.5–4 kg | 27.7 (27.5–28.0) | 89.8 (89.1 −90.4) | 0.86 (0.86–0.87) |
| > 4 kg | 29.3 (28.8–29.8) | 94.0 (92.7–95.3) | 0.87 (0.86–0.88) |
Abbreviation: ELSA-Brasil, Brazilian Longitudinal Study of Adult Health.
Analysis of covariance adjusted for study center, sex, age, family income, race, education, education of mother, mother had diabetes and father had diabetes.
Figure 1.
Adjusted mean values of BMI, waist circumference and the waist-to-hip ratio for men and women (women = black, men = gray). Values were adjusted through ANCOVA for study center, age, family income, participant race, participant education, education of participant’s mother, mother had diabetes and father had diabetes. P-value for the interaction between low birth weight and sex was on BMI = 0.01, on waist circumference <0.0001 and on waist-to-hip ratio <0.0001; and for high birth weight and sex on these same outcomes: 0.33, 0.18 and 0.42, respectively.
Similar sex-specific patterns were observed when we analyzed adiposity outcomes using ordinal logistic regression models (Table 3). Among men, greater odds of adult overall and central obesity occurred with each higher category of birth weight. Among women, however, when compared to those with normal birth weight, those with both low and high birth weight had higher odds, frequently statistically significant, of being in the highest level of each adiposity outcome, producing, again, J- or U-shaped patterns. For low birth weight women, this difference was statistically significant for waist-to-hip ratio. Figure 2 illustrates these sex-specific categorical analyses, presenting the odds of obesity (vs normal weight) and those of being in the third (vs first) tertile of waist circumference and waist-to-hip ratio. Once again, there were sex differences comparing those with low to normal weight (BMI: Pinteraction = 0.004; waist circumference: Pinteraction = 0.0008 and waist-to-hip ratio: Pinteraction = 0.005), but not comparing those with high to normal weight (Pinteraction ⩾ 0.20).
Table 3.
Associationsa of birth weight categories with body mass index (BMI), waist circumference and waist-to-hip ratio categories according to sex in adults 35–70 years of age in ELSA-Brasil
| Birth weight categories | 25≤ BMI<30 kg m−2 vs <25 kg m−2 | BMI ≥30kg m−2 vs <25 kg m−2 |
|---|---|---|
| OR (95% CI) | OR (95% CI) | |
| Men | ||
| <2.5 kg | 0.66 (0.51–0.85) | 0.65 (0.46–0.90) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| >4 kg | 1.59 (1.29–1.96) | 1.88 (1.54–2.30) |
| Women | ||
| <2.5 kg | 1.00 (0.80–1.26) | 1.18 (0.92–1.51) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| >4 kg | 1.61 (1.29–2.02) | 1.67 (1.34–2.08) |
| Waist circumference 2nd vs 1st tertile | Waist circumference 3rd vs 1st tertile | |
| OR (95% CI) | OR (95% CI) | |
| Men | ||
| <2.5 kg | 0.61 (0.47–0.79) | 0.66 (0.50–0.87) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| <4 kg | 1.42 (1.16–1.75) | 1.71 (1.41–2.06) |
| Women | ||
| <2.5 kg | 0.90 (0.71–1.14) | 1.21 (0.97–1.53) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| >4 kg | 1.48 (1.16–1.87) | 1.82 (1.48–2.25) |
| Waist-to-hip ratio 2nd vs 1st tertile | Waist-to-hip ratio 3rd vs 1st tertile | |
| OR (95% CI) | OR (95% CI) | |
| Men | ||
| <2.5 kg | 0.63 (0.49–0.83) | 0.79 (0.60–1.03) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| >4 kg | 1.08 (0.89–1.33) | 1.33 (1.09–1.62) |
| Women | ||
| <2.5 kg | 1.61 (1.24–2.10) | 1.44 (1.15–1.82) |
| 2.5–4 kg | 1 (reference) | 1 (reference) |
| >4 kg | 1.21 (0.96–1.53) | 1.21 (0.97–1.52) |
Abbreviations: CI, confidence interval; ELSA-Brasil, Brazilian Longitudinal Study of Adult Health; OR, odds ratio. Cutoffs for tertiles of waist circumference: men 90 and 99.6 cm; women 81.2 and 91.9 cm; cutoffs for tertiles of waist-to-hip ratio: men 0.919 and 0.978; women 0.812 and 0.877.
Ordinal logistic regression models adjusted for study center, age, family income, participant race, participant education, education of participant’s mother, mother had diabetes and father had diabetes. Statistically significant associations are presented in bold.
Figure 2.
Adjusted OR of obesity (BMI), high waist circumference (3rd vs 1st tertile) and high waist-to-hip ratio (3rd vs 1st tertile) for men and women (women=black, men=gray). Values were adjusted through ordinal logistic regression models for study center, age, family income, participant race, participant education, education of participant’s mother, whether the participant’s mother had diabetes and whether the participant’s father had diabetes. P-value for the interaction between low birth weight and sex was on obesity =0.004, on high vs low tertile waist circumference=0.0008 and on high vs low tertile waist-to-hip ratio =0.005; and for high birth weight and sex on these same outcomes: 0.43, 0.64 and 0.54, respectively.
In sensitivity analyses that excluded 87 participants (48 obese, 27 overweight and 12 with normal BMI) who reported having undergone bariatric surgery, the results were not appreciably different from the main results including these participants.
DISCUSSION
In this sample of middle-aged and elderly Brazilians 35–74 years, born from 1936 to 1973, we found a sex-specific pattern of associations of low but not high birth weight with adult measures of overall and central adiposity. In men, low birth weight was generally associated with lower overall and central adult adiposity, while in women low birth weight was generally associated with higher levels of adiposity. Those with high birth weight, consistent with findings from a large systematic review,13 had greater odds of adult overweight and obesity (57–87% greater), and these associations were generally similar for men and women.
The sex-specific association between low birth weight and adult overall and central adiposity has not, to our knowledge, been comprehensively reported in cohorts of middle-aged or elderly adults. A systematic review reported a decreased odds of overweight/obesity (odds ratio (OR) = 0.67; 95% confidence interval (CI) = 0.59–0.76) for those with low birth weight (<2500 g).13 However, in sensitivity analyses of only those studies with adult participants, lower odds for future excess weight were not seen (OR = 0.97; 95% CI = 0.79–1.20). In this systematic review, results in adults were not presented separately by sex. In fact, we could find no reports in the literature investigating sex-specific adiposity outcomes of low birth weight for middle-aged and elderly adults, the age range at which overall and central obesity are usually associated with their common cardiometabolic complications.
An investigation of 3 72 542 middle-aged UK women, but no men, showed a U-shaped relationship between birth weight and obesity at middle age.14 In comparison to those with normal birth weight, those with low birth weight had 26% greater odds of obesity (OR = 1.26; 95% CI = 1.23–1.29) and those with high birth weight had 33% greater odds of obesity (OR = 1.33; 95% CI = 1.30–1.37). A Brazilian birth cohort that followed participants until 30 years of age found that women with low birth weight, but not men, had greater visceral fat content.15 A study of Chinese adolescents found a U-shaped association of birth weight with BMI and waist circumference, the latter being statistically significant only in girls.16 Adolescent Spanish girls presented smaller associations of birth weight, assessed as weight for gestational age, with measures of body composition than boys, although only linear relationships across the entire birth weight spectrum were reported.17
Our findings suggest sex-specific responses to intrauterine adversity that influence the development of overall and central obesity. Similar to our findings, sex differences have been reported from several studies of survivors of famines. Middle-aged women conceived during the Dutch Famine of 1944–1945,4 the Nigerian Biafran Famine,5 the Great Depression in Reykjavik (1930–1934)6 and the Great Chinese Famine18,19 have a greater prevalence of overweight and obesity than men.
In terms of biologic mechanisms that may underlie the associations we report, growing evidence shows that intrauterine adversity not only restricts fetal growth but also alters gene expression in a manner that may increase future risk of adiposity and metabolic diseases.20 Consistent with our findings, the current literature suggests that these epigenetic marks are sex specific.21–24
These sex-specific findings may also be interpreted within a larger framework of sexually-dimorphic, species-specific gestational strategies to cope with environmental adversity.25–27 This framework suggests that our findings may represent the long-term effects of fetal programming evolved through natural selection to produce alternative survival strategies for boys and girls in the setting of intrauterine growth restriction. In a number of non-human mammalian species, a greater fraction of females are born in gestations complicated by poor nutrition or a poor habitat.28 Some29–31 but not all32 studies of famine also report a drop in the male-to-female ratio of births. A Brazilian study of low birth weight infants showed neonatal mortality in boys to be 67% greater than that in girls.33
There are limitations to our study that merit mention. Birth weight was ascertained by interview through self-report. However, if an ELSA participant was uncertain about his or her birth weight, he or she was encouraged to investigate it further and report back later to the clinic. Additionally, care was taken to limit low birth weight to causes related to intrauterine growth restriction (for example, those reporting premature or twin birth were excluded from analyses), and several cohort studies have shown moderate correlations between estimated and recorded birth weight (r = 0.64–0.83).34–36 A subsample of the Nurse’s Health Study II found that 70% of referred values fell into the correct birth weight categories written in birth certificates.37 Another limitation is missing data; we were only able to conduct analyses in the 84% of participants self-reported their birth weight. Although potential confounders, such as maternal educational attainment, were controlled for in our multivariable analysis, we also cannot rule out influence from unmeasured or residual confounding. Finally, as our study participants were recruited from higher education institutes they may be of higher socioeconomic status than other contemporary Brazilian adults.
Our study also has several strengths, including its generalizability to populations in low- and middle-income countries. The majority of the world’s population is currently undergoing a rapid nutritional transition. ELSA participants were born between 1930 and 1970, and thus lived through the mid-1900s during which food insecurity was common, as well as through the more recent period in which obesity has been highly prevalent. This study is the first, to our knowledge, to examine the association of birth weight with measures of obesity in middle-aged and elderly adults within this context of a rapid nutritional transition. Additionally, adult anthropometry in ELSA was carefully measured following internationally standardized techniques.
In conclusion, birth weight was associated with measures of overall and central adiposity in a sex-specific manner, suggesting a positive linear association in men and J- or U-shaped associations in women. Sex stratification in future studies of fetal programming may help to uncover novel sex-dependent responses to the in utero environment that may lead to adult metabolic disease.
ACKNOWLEDGEMENTS
This work was supported by the Brazilian Ministry of Health (Science and Technology Department) and the Brazilian Ministry of Science and Technology (Financiadora de Estudos e Projetos - FINEP and the National Council for Scientific and Technological Development - CNPq) (grant numbers 01 06 0010.00 RS, 01 06 0212.00 BA, 01 06 0300.00 ES, 01 06 0278.00 MG, 01 06 0115.00 SP, 01 06 0071.00 RJ).
Footnotes
CONFLICT OF INTEREST
The authors declare no conflict of interest.
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