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Epidemiology and Population Health

Women’s reproductive health factors and body adiposity: findings from the UK Biobank

Abstract

Objective:

To conduct a comprehensive examination of the association between women’s reproductive health factors and measures of body adiposity in a contemporary Western population.

Methods:

A cross-sectional analysis of 502 664 individuals from the UK Biobank was conducted. Multivariable linear regression models were used to examine the association of age at menarche, age at first birth, parity and age at menopause with measures of general and central body adiposity, adjusted for age, smoking and socioeconomic status. The association between number of children and body adiposity in men was also assessed.

Results:

Age at menarche was inversely associated with body mass index (BMI); adjusted mean BMI was 29.0 kg m–2 in women with menarche before the age of 12 years, compared with 26.5 kg m–2 in those who had menarche after 14 years of age. Age at first birth was linearly and inversely associated with BMI: 0.16 kg m–2 lower BMI per year increase in age of first birth. Each additional live birth or child fathered was associated with a 0.22 kg m–2 higher BMI in women and a 0.14 kg m−2 higher BMI in men. There was no evidence for an association between age at menopause and BMI. Corresponding associations for other markers of general or abdominal adiposity were similar to those for BMI. Findings were broadly similar in analyses stratified by age, smoking status, socioeconomic status, ethnic background, and history of diabetes or cardiovascular disease.

Conclusions:

In women from a contemporary Western population, earlier age at menarche and age at first birth, and higher number of total live births were associated with higher levels of body adiposity. Prospective evaluations of the association between reproductive health factors, adiposity and the onset of cardiometabolic diseases are needed to assess causality, and to explore the mechanisms involved.

Introduction

Excess body weight poses an increasingly large burden on the world's population: more than two billion (35%) individuals globally are either overweight or obese, and the prevalence is expected to further increase over coming decades.1 The adverse health consequences of excess body weight are indisputable and wide ranging and consequently, overweight and obesity were estimated to be responsible for 3.4 million deaths worldwide in 2010.2

While dietary habits and physical inactivity are the fundamental drivers of excess body weight, with effects possibly accelerated by heritable factors, there is accruing evidence that reproductive health factors may also be determinants of body adiposity.3, 4, 5 Age at menarche, in particular, has shown to be associated with body weight, with the majority of studies demonstrating an inverse relationship between age at menarche and body size.5 It is uncertain whether the observed association between early menarche and adult body size is mediated by childhood adiposity. Also, the strength of the relationship tends to vary across populations, which may partially be a reflection of the secular trends in age at menarche (generally downwards) that has been observed in many populations.6, 7, 8 Furthermore, although most studies on the association between reproductive factors and adiposity used body mass index (BMI) as their measure of adiposity, some studies also used body fat percentage, waist circumference, waist-to-height ratio or the waist-to-height ratio.4, 9 Plausibly, these might show different relationships with reproductive health factors. Evidence on the relationship of other reproductive health factors, such as age at first birth and age at menopause, with excess body weight is more limited,3, 10 and small study sizes have hampered identification of clinically important differences in the association between reproductive health factors and of body adiposity across population subgroups. Moreover, although some studies found a link between parity and excess body weight,11, 12, 13 the evidence is inconsistent, fuelling the discussion as to whether the association is the result of physiological effects of pregnancy or due to socioeconomic and lifestyle factors associated with family size and child rearing. Comparison between men and women provides a useful method to distinguish between these biological processes, and socioeconomic and lifestyle factors associated with childbearing and child rearing, not all of which are necessarily captured by statistical adjustment.

Using data on over 500 000 women and men from the UK Biobank, we sought to overcome these limitations to conduct the most comprehensive examination to date of the association between reproductive health factors and measures of body adiposity in a contemporary Western population.

Subjects and methods

Study population

Cross-sectional data were used from the UK Biobank, a large, prospective, population-based cohort study established to examine the lifestyle, environmental and genetic determinants of a range of diseases of adulthood.14, 15 Between 2006 and 2010, more than 500 000 women and men aged 40–69 at baseline attended one of the 22 centres across the UK for detailed assessment that included collection of extensive questionnaire data and physical measurements.

Reproductive health factors and adiposity measures

Study participants provided self-reported information about reproductive factors at study baseline. For women this included questions about age at menarche, age at first birth, number of live births and menopausal status. Men were asked how many children they had fathered. Standing height was measured using a Seca 202 height measure and weight and body fat percentage were measured using the Tanita BC-418 MA body composition analyser. Waist and hip circumference were measured using a Wessex non-stretchable sprung tape measure. All measurements were done once by trained technicians while participants were wearing light clothes and no shoes. BMI was derived by dividing weight (kilogram) by the square of the standing height (square metres). The waist-to-hip ratio was derived by dividing the waist circumference by the hip circumference, and the waist-to-height ratio was obtained by dividing the waist circumference by the standing height.

Statistical analyses

Baseline characteristics are presented as means (s.d.) for continuous variables and as percentages for categorical variables. Linear regression analyses, adjusted for age, socioeconomic status (SES) and smoking status, were used to examine the association between reproductive health factor and measures of adiposity. Least-squares means were obtained and plotted against categories of the specific reproductive health factor. The primary analyses used BMI as the measure of adiposity. Subgroup analyses were conducted by age at study baseline, SES (in thirds of the Townsend material deprivation score in England, derived from the 2001 Census),16 and self-reported smoking status, ethnicity, history of diabetes and history of cardiovascular disease. In a secondary analysis, we examined the association between adiposity and reproductive health factors when evaluated through waist circumference, body fat, waist-to-hip ratio and waist-to-height ratio. R version 2.15.3 was used for all analyses.

Results

The mean age of study participants was 56 (s.d. 8) years, 94% were white and 51% were from the most socioeconomically advantaged third of the UK population (Table 1). Mean BMI was 27 (s.d. 5) kg m–2 in women and 28 (s.d. 4) kg m–2 in men, and mean waist circumference was 85 (s.d. 13) cm in women, and 97 (s.d. 11) cm in men. Secular patterns in reproductive health factors are shown in Supplementary Figure S1. Mean age at menarche was 13 (s.d. 2) years, with little evidence of temporal trends across birth cohorts. There was a continuous decrease in parity and the number of children across birth cohorts, yet about 80% of all women and men had at least one child. Age at first birth increased steadily across birth cohorts; women born before 1940 were on average 24 years when they had their first live birth, as compared with 27 years in women born after 1965. Mean age at menopause was 50 (s.d. 5) years, with no indication of temporal changes.

Table 1 Baseline characteristics of study participants

Age at menarche

Women who had their menarche before the age of 12 years had an average BMI of 29.0 kg m–2 as compared with 26.5 kg m–2 in women who had their menarche after the age of 14 years, after adjustment for age, smoking and SES (Figure 1). Mean BMIs were consistently lower in women in higher SES groups, with a white background, and without a history of diabetes or cardiovascular disease (Figure 2). Nevertheless, the pattern of decreasing BMI with increasing age at menarche was apparent in all subgroups. The associations between age at menarche and other markers of general or abdominal adiposity were similar to those observed for BMI (Supplementary Figure S2).

Figure 1
figure1

Mean body mass index by age at menarche, age at first birth, number of children or live births* and age at menopause. Analyses are adjusted for age, socioeconomic status and smoking status. Boxes represent the mean body mass index with sizes inversely proportional to the variance of the mean. Vertical lines represent 95% confidence intervals. *Number of children was used in men, and number of live births was used in women.

Figure 2
figure2

Mean body mass index by age at menarche in subgroup analyses. Analyses are adjusted for age, socioeconomic status and smoking status.

Age at first birth

There was an inverse relationship between age at first birth and BMI; every year increase in age at first birth was associated with a 0.16 kg m–2 lower BMI (Figures 1 and 3). There was slight variation in the association between age at first birth and BMI across certain subgroups, with subgroup effects ranging from a 0.09 kg m–2 lower BMI per year increase in age at birth for current smokers to a 0.25 kg m–2 lower BMI in women with a history of diabetes. Analyses of the association between age at first birth and other markers of adiposity found similar patterns (Supplementary Figure S3).

Figure 3
figure3

Mean change in body mass index per year increase in age at first birth and age at menopause in subgroup analyses. Analyses are adjusted for age, socioeconomic status and smoking status. Boxes represent the mean body mass index with sizes inversely proportional to the variance of the mean. Horizontal lines represent 95% confidence intervals.

Number of live births and number of children

An increasing number of live births among women and number of children fathered among men were associated with higher levels of BMI (Figure 1). Mean BMI was 1.3 kg m–2 higher in women with four or more live births than in nulliparous women. Men who had fathered four or more children had an average BMI that was 0.8 kg m–2 higher as compared with their counterparts without children. Every additional live birth or child fathered among those who had any children was associated with a 0.22 kg m–2 higher mean level of BMI in women and a 0.14 kg m–2 higher mean level of BMI in men (Figure 4). Associations were comparatively weaker in women from younger birth cohorts, with a higher SES, with a white ethnic background and in women with a history of diabetes as compared with their counterparts. The strength of the association appeared weaker among men with a history of diabetes or cardiovascular disease than in those without. Results were similar in the analyses using different measures of adiposity (Supplementary Figures S4 and S5).

Figure 4
figure4

Mean change in body mass index per additional live birth or per additional child fathered*. Analyses are adjusted for age, socioeconomic status and smoking status. Boxes represent the mean body mass index with sizes inversely proportional to the variance of the mean. Horizontal lines represent 95% confidence intervals. *Number of children was used in men, and number of live births was used in women.

Age at menopause

In the analyses that were restricted to postmenopausal women, there was minimal evidence for an association between age at menopause and BMI, both overall and across subgroups (Figures 1 and 3). Similarly, there was no relationship when waist circumference, body fat, waist-to-hip ratio or waist-to-height ratio were used as markers of adiposity (Supplementary Figure S6).

Discussion

This present study provides a comprehensive examination of the cross-sectional associations between reproductive health factors and a range of measures of body adiposity in a contemporary Western population. The study confirms the previously reported inverse association between age at menarche and subsequent levels of body adiposity in women several decades later. Moreover, findings from the current study add to the evidence base by demonstrating that the relationship is similar across a range of subgroup analyses, and is apparent irrespective of the measure of body adiposity used. Age at first birth was also linearly and inversely associated with body adiposity in later life, whereas there was little evidence for an association between age at menopause and body adiposity. Furthermore, there was a positive association between parity in women and the number of children fathered in men, suggesting that the association between parity and adiposity is more likely to be due to the adverse lifestyle and socioeconomic factors associated with child rearing than due to the biological effects of childbearing.

Most previous studies on the association between reproductive health factors and body adiposity have used BMI as the metric of adiposity, with comparatively few studies examining whether other markers of body adiposity—in particular, central obesity, such as waist circumference and waist-to-hip ratio—are similarly associated. In the present analyses, there was no indication that the associations between reproductive health factors with adiposity differed according to the measure used, and similarly, that any of the other measures of adiposity were more informative than BMI.17

Age at menarche

The inverse association between age at menarche and body adiposity reported here is in agreement with the findings from a recent meta-analysis of 10 cohort studies which showed that early menarche (<12 years of age) was associated with higher adult BMI, with a mean BMI difference of 0.34 kg m−2 between women who experienced early menarche versus those who experienced menarche at 12 or more years of age.5 Excess body weight is a strong risk factor for a range of disease outcomes;17, 18, 19 under the assumption of causality, an inverse association between age at menarche and adiposity might therefore suggest that women with an early menarche are at increased risk of obesity-related disease outcomes later in life. Evidence for the long-term consequences of age at menarche on chronic disease outcomes generally supports this hypothesis, and shows that early menarche is associated with an increased risk of a range of conditions including type II diabetes,20 cardiovascular diseases5, 21 and all-cause mortality.5 Nonetheless, the magnitude and shape of the relationship varies across populations, and the possible biological pathways for an association of early age at menarche, body adiposity and subsequent chronic diseases merits further examination, taking account of the roles of heritable factors, dietary habits and physical inactivity throughout life. Genome-wide association studies of age at menarche have identified several obesity-related variants to be associated with earlier menarche,22, 23 indicating that there are complex genetic relationships between adiposity and age at menarche in normal trajectories of growth and development, which could influence disease risk throughout the life course.

Age at first birth and number of live births or children

Parity has dropped and the age at which a woman has her first child has increased across successive generations in many populations.6, 7, 8 Evidence on the association between age at first birth and body adiposity is limited to that from a study among Swedish women, which reported that older age at first birth was associated with a lower level of BMI 30 years later.3 In the present analyses, we confirmed these findings and showed that older age at first birth was associated with lower levels of body adiposity later in life, with some indication that the effect was stronger among women with a lower SES as compared with women with a higher SES. There was also evidence of a positive association between the number of live births and body adiposity, which is in agreement with previous findings on the association between parity and body adiposity.11, 12, 13 The Million Women Study showed that women with four or more births had a 1.7 kg m–2 higher BMI as compared with nulliparous women, which is comparable to the 1.3 kg m–2 difference in BMI reported here.12 A novel finding of the current analyses is that the latter association is also present in men; men who had fathered four or more children had a 0.8 kg m–2 higher BMI as compared with men without children. This suggests that a significant proportion of the association between parity and later adiposity may be attributed to behavioural risk factors associated with child rearing including an increased likelihood of adverse dietary habits, accumulated financial and physical pressures, and mental depletion.

Age at menopause

A few small studies have examined the association between age at menopause and body adiposity. A report from 522 women in the Framingham Heart Study did not detect differences between menopausal age and several measures of body composition, including BMI and waist circumference.4 Similarly, results from a Japanese study among 1022 women found no differences in BMI by age at natural menopause.10 The present study included nearly 200 000 postmenopausal women from the UK Biobank robustly confirms the findings of previous studies, and most definitely shows the lack of a cross-sectional association between age at menopause and adiposity.

Strengths and limitations

The very large sample size and well characterised nature of participants within UK Biobank has permitted the most detailed evaluation on the cross-sectional association between reproductive health factors and body adiposity in a contemporary Western population. Our findings are generally in agreement with previous research, but considerably expand the evidence base with the additional consideration of a range of measures of body adiposity, evaluation of multiple key reproductive health factors and more detailed subgroup analyses. Inclusion of men enabled us to demonstrate that the association between parity and body adiposity in women is more likely to be driven by lifestyle factors associated with parenthood than with the biological factors of pregnancy. The present analysis also has some limitations. First, the cross-sectional design of our analyses does not allow us to make causal inferences about the association between reproductive health factors and excess body weight, nor about the potential contribution of reproductive health factors in the development of chronic disease outcomes. Second, body adiposity was measured in adulthood and data on levels of body adiposity earlier in life were not available. We were, therefore, unable to separate the potential biological effects of reproductive health factors, especially age at menarche, on body adiposity from their potential role as confounders or mediators in the association between excess body weight early in life and excess body weight later in life. Third, information on reproductive health factors was self-reported and was therefore subject to misclassification. This particularly might have affected the information on age at menarche recalled decades after the onset of menarche. Previous studies, however, have indicated that women recall age at menarche with reasonable accuracy.24, 25, 26

Conclusion

The present study provides robust evidence for an association between a range of reproductive health factors and body adiposity in a contemporary Western population. We report inverse relationships of age at menarche and age at first birth in women, and positive relationships between parenthood with body adiposity in both sexes. Prospective evaluations are needed to assess causality and to explore the complex interface of mechanisms involved in the association between reproductive health factors, adiposity and the onset of cardiometabolic diseases.

References

  1. 1

    Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 766–781.

    Article  Google Scholar 

  2. 2

    Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380: 2224–2260.

    Article  Google Scholar 

  3. 3

    Newby PK, Dickman PW, Adami HO, Wolk A . Early anthropometric measures and reproductive factors as predictors of body mass index and obesity among older women. Int J Obes 2005; 29: 1084–1092.

    CAS  Article  Google Scholar 

  4. 4

    Trikudanathan S, Pedley A, Massaro JM, Hoffmann U, Seely EW, Murabito JM et al. Association of female reproductive factors with body composition: the Framingham Heart Study. J Clin Endocrinol Metab 2013; 98: 236–244.

    CAS  Article  Google Scholar 

  5. 5

    Prentice P, Viner RM . Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Biomed Res Int 2013; 37: 1036–1043.

    CAS  Google Scholar 

  6. 6

    Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sorensen TI et al. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 2008; 121 (Suppl 3): S172–S191.

    Article  Google Scholar 

  7. 7

    Lewington S, Li L, Murugasen S, Hong LS, Yang L, Guo Y et al. Temporal trends of main reproductive characteristics in ten urban and rural regions of China: the China Kadoorie biobank study of 300 000 women. Int J Epidemiol 2014; 43: 1252–1262.

    Article  Google Scholar 

  8. 8

    Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ . Secular trends in age at menarche in women in the UK born 1908-93: results from the Breakthrough Generations Study. Paediatr Perinat Epidemiol 2011; 25: 394–400.

    Article  Google Scholar 

  9. 9

    Chen L, Zhang C, Yeung E, Ye A, Mumford SL, Wactawski-Wende J et al. Age at menarche and metabolic markers for type 2 diabetes in premenopausal women: the BioCycle Study. J Clin Endocrinol Metab 2011; 96: E1007–E1012.

    CAS  Article  Google Scholar 

  10. 10

    Akahoshi M, Soda M, Nakashima E, Tsuruta M, Ichimaru S, Seto S et al. Effects of age at menopause on serum cholesterol, body mass index, and blood pressure. Atherosclerosis 2001; 156: 157–163.

    CAS  Article  Google Scholar 

  11. 11

    Cohen SS, Larson CO, Matthews CE, Buchowski MS, Signorello LB, Hargreaves MK et al. Parity and breastfeeding in relation to obesity among black and white women in the southern community cohort study. J Womens Health (Larchmt) 2009; 18: 1323–1332.

    Article  Google Scholar 

  12. 12

    Bobrow KL, Quigley MA, Green J, Reeves GK, Beral V . Persistent effects of women's parity and breastfeeding patterns on their body mass index: results from the Million Women Study. Int J Obes (Lord) 2013; 37: 712–717.

    CAS  Article  Google Scholar 

  13. 13

    Koch E, Bogado M, Araya F, Romero T, Diaz C, Manriquez L et al. Impact of parity on anthropometric measures of obesity controlling by multiple confounders: a cross-sectional study in Chilean women. J Epidemiol Community Health 2008; 62: 461–470.

    CAS  Article  Google Scholar 

  14. 14

    Allen N, Sudlowa C, Downey P, Peakman T, Danesh J, Elliott P et al. UK Biobank: Current status and what it means for epidemiology. Health Policy Technol 2012; 1: 123–126.

    Article  Google Scholar 

  15. 15

    Sudlow C, Gallacher J, Allen N, Beral V, Burton P, Danesh J et al. UK biobank: an open access resource for identifying the causes of a wide range of complex diseases of middle and old age. PLoS Med 2015; 12: e1001779.

    Article  Google Scholar 

  16. 16

    Townsend material deprivation score for output areas in England - based on Census 2001, 2004. http://www.erpho.org.uk/viewResource.aspx?id=9070.

  17. 17

    Wormser D, Kaptoge S, Di Angelantonio E, Wood AM, Pennells L, Thompson A et al. Separate and combined associations of body-mass index and abdominal adiposity with cardiovascular disease: collaborative analysis of 58 prospective studies. Lancet 2011; 377: 1085–1095.

    Article  Google Scholar 

  18. 18

    Parr CL, Batty GD, Lam TH, Barzi F, Fang X, Ho SC et al. Body-mass index and cancer mortality in the Asia-Pacific Cohort Studies Collaboration: pooled analyses of 424,519 participants. Lancet Oncol 2010; 11: 741–752.

    Article  Google Scholar 

  19. 19

    Whitlock G, Lewington S, Sherliker P, Clarke R, Emberson J, Halsey J et al. Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet 2009; 373: 1083–1096.

    Article  Google Scholar 

  20. 20

    Janghorbani M, Mansourian M, Hosseini E . Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol 2014; 51: 519–528.

    Article  Google Scholar 

  21. 21

    Charalampopoulos D, McLoughlin A, Elks CE, Ong KK . Age at menarche and risks of all-cause and cardiovascular death: a systematic review and meta-analysis. Am J Epidemiol 2014; 180: 29–40.

    Article  Google Scholar 

  22. 22

    Elks CE, Perry JR, Sulem P, Chasman DI, Franceschini N, He C et al. Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 2010; 42: 1077–1085.

    CAS  Article  Google Scholar 

  23. 23

    Fernandez-Rhodes L, Demerath EW, Cousminer DL, Tao R, Dreyfus JG, Esko T et al. Association of adiposity genetic variants with menarche timing in 92,105 women of European descent. Am J Epidemiol 2013; 178: 451–460.

    Article  Google Scholar 

  24. 24

    Casey VA, Dwyer JT, Coleman KA, Krall EA, Gardner J, Valadian I . Accuracy of recall by middle-aged participants in a longitudinal study of their body size and indices of maturation earlier in life. Ann Hum Biol 1991; 18: 155–166.

    CAS  Article  Google Scholar 

  25. 25

    Koprowski C, Coates RJ, Bernstein L . Ability of young women to recall past body size and age at menarche. Obes Res 2001; 9: 478–485.

    CAS  Article  Google Scholar 

  26. 26

    Must A, Phillips SM, Naumova EN, Blum M, Harris S, Dawson-Hughes B et al. Recall of early menstrual history and menarcheal body size: after 30 years, how well do women remember? Am J Epidemiol 2002; 155: 672–679.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This research has been conducted using the UK Biobank Resource. Ethics and permission: UK Biobank has obtained Research Tissue Bank approval from its governing Research Ethics Committee, as recommended by the National Research Ethics Service. No separate ethics approval was required. Permission to use the UK Biobank Resource was approved by the Access Sub-Committee of the UK Biobank Board.

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Correspondence to S A E Peters.

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Peters, S., Huxley, R. & Woodward, M. Women’s reproductive health factors and body adiposity: findings from the UK Biobank. Int J Obes 40, 803–808 (2016). https://doi.org/10.1038/ijo.2015.254

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