IJE Advance Access originally published online on November 26, 2008
International Journal of Epidemiology 2009 38(1):72-82; doi:10.1093/ije/dyn221
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Pathways to obesity in a developing population: The Guangzhou Biobank Cohort Study
1Department of Community Medicine and School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
2Guangzhou Occupational Diseases Prevention and Treatment Centre, Guangzhou Number 12 Hospital, Guangzhou, China.
3Department of Public Health and Epidemiology, University of Birmingham, UK.
*Corresponding author. Department of Community Medicine and School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Pokfulam, Hong Kong SAR, China; E-mail: cms1{at}hkucc.hku.hk
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Abstract |
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Background ‘Environmental mismatch’ may contribute to obesity in rapidly developing societies, because poor early life conditions could increase the risk of obesity in a subsequently more socio-economically developed environment. In a recently developing population (from southern China) we examined the association of life-course socio-economic position (SEP) with obesity.
Methods In a cross-sectional study of 9998 adults from the Guangzhou Biobank Cohort Study (phase 2) examined in 2005–06, we used multivariable linear regression to assess the association of SEP at three life stages (proxied by parental possessions, education and longest held occupation) with obesity [body mass index (BMI) and waist–hip ratio (WHR)] in men and women.
Results There was no evidence that socio-economic position trajectory had supra-additive effects on BMI or WHR. Instead in women, higher SEP at any life stage usually contributed to lower BMI and WHR; e.g. women with higher early adult SEP had lower BMI [–0.45; 95% confidence interval (CI) –0.71 to –0.19) and WHR (–0.02; 95% CI –0.02 to –0.012]. In contrast, in men, higher childhood SEP was associated with higher BMI (0.53; 95% CI 0.18 to 0.88) and WHR (0.01; 95% CI 0.003 to 0.02) as was high late adulthood SEP with BMI (0.36; 95% CI 0.07 to 0.64).
Conclusions This study provides little support for environmental mismatch over the life course increasing obesity in this rapidly transitioning southern Chinese population. However, our findings highlight different effects of the epidemiologic transition in men and women, perhaps with pre-adult exposures as a critical window for sex-specific effects.
Keywords Obesity, life course, socio-economic position, mismatch, developing population
Accepted 24 September 2008
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Introduction |
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Obesity is associated with type 2 diabetes, cardiovascular disease and some cancers, as well as reduced quality of life and impaired mental health.1 The number of obese people has doubled over the last decade to 400 million.2 Changes in diet and physical activity play a role, however increasingly obesity is viewed as driven by mismatch between biology and the environment over the life course or across generations.3 The physiological processes governing energy requirements may be affected by environmental or epigenetic exposures, driven by maternal constraints or metabolic adjustments to match the predicted environment.3 Mismatch may occur in several ways, particularly during periods of rapid economic transition. Foetal constraint may occur because of poor conditions during pregnancy or poor conditions during the mother's own growth which constrains her ability to supply nutrients. Subsequently socio-economic development may enable more plentiful nutrition during childhood or facilitate a move from a constrained environment to a nutritionally rich sedentary lifestyle.3 This mismatch between energy intake and expenditure resulting from behaviour and physiology, is often patterned by life-course socio-economic position (SEP).4 A sudden increase in the degree of mismatch, as in societies undergoing rapid economic transition, with constrained early life conditions followed by subsequent improvements, may increase the risk of obesity,3 because sub-optimal growth and development, resulting from low SEP in early life might render a person more vulnerable to obesity when faced in later life with a more plentiful environment usually associated with higher SEP in developing countries.
In industrialized countries a high life-course SEP is usually protective for obesity,5–7 including for central obesity in old age.8 In developing countries, the associations are less consistent, with low adult SEP conferring protection against obesity in low-income economies, for men and women, but this is less consistent in middle-income economies, where higher SEP tends to be protective against obesity in women but not men.9,10 The impact of life-course SEP trajectories, on obesity is seldom studied in developing populations.11 The mechanisms which drive social inequalities in obesity are complex and not fully understood, nor is the relative importance of cumulative damage to biological systems12 compared with exposures during potentially critical developmental windows.
Due to recent and rapid economic development in the coastal cities of China, these populations have transitioned through very different economic and social environments during their lives.13 In a large sample of older (
50 years) adults from Guangzhou, the capital of Guangdong province in southern China, we examined the sex-specific associations of life-course SEP with later life adiposity, proxied by body mass index (BMI) and waist–hip ratio (WHR), to test the hypothesis that environmental mismatch within a single life course (represented here by discordant life-course SEP trajectory) impacts adiposity.
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Sources of data
The Guangzhou Biobank Cohort Study, a collaboration between the Guangzhou No. 12 Hospital and the universities of Hong Kong and Birmingham has been described in detail.13 Participants were drawn from The Guangzhou Health and Happiness Association for the Respectable Elders (GHHARE), a community social and welfare association, open to anyone aged 50 years or older. About 7% of permanent Guangzhou residents aged
50 years are members of GHHARE, of whom 11% were selected for this study, and included if capable of consenting, ambulatory, and not receiving treatment modalities which if omitted may result in immediate life threatening risk, such as chemotherapy or radiotherapy for cancer, or dialysis for renal failure. Of those eligible, 90% of the men and 99% of the women participated. Participants underwent a half-day detailed medical interview, including a physical examination. The Guangzhou Medical Ethics Committee of the Chinese Medical Association approved the study and all subjects gave written, informed consent before participation.
Anthropometric measurements
Waist circumference was measured horizontally around the smallest circumference between the ribs and iliac crest, or at the level of the naval for obese participants. Hip circumference was measured around the maximal girth of the hips. Weight and standing height were measured with light indoor clothes without shoes. WHR was computed as waist divided by hip circumference, BMI was computed as weight in kilograms divided by height in metres squared.
SEP across the life course
As recommended for life course studies we used childhood household conditions, education and longest held occupation as proxies for childhood, young adult and later adult SEP respectively.14 Pre-industrial societies lack the technology to record and preserve detailed information about their citizens, so we are restricted to retrospective information about childhood conditions. To proxy participants’ childhood environment we specifically selected possession of simple, notable items appropriate to mid 20th century China, based on contemporary sociological accounts.15,16 The items selected were parental possession of a watch, a sewing machine and a bicycle. Parental possessions were categorized as none, one or two and all three. Education was categorized as highest level of primary school or less (low), junior middle school (medium) and senior middle school or above (high) to obtain approximately evenly distributed tertiles in each sex. Occupation was categorized as manual (agricultural worker, factory work or sales and service) and non-manual (administrator/manager, professional/technical, military/police).
Finally, eight life-course SEP trajectories were created by dividing SEP at each of the three time points into as near as possible into halves representing ‘upper’ and ‘lower’ for each sex to give eight permutations. In the eight life-course SEP trajectories, parental possessions during childhood were dichotomized as none and at least one item because most participants reported none. Because of the different educational experiences of older Chinese men and women, primary school or less was categorized as low education for women whilst junior middle or less was categorized as low for men so as to get approximately equal halves.
Statistical analysis
Multivariable linear regression was used to assess the association of SEP with BMI and WHR. Model 1 adjusted for age in 5-year age groups. Model 2 additionally adjusted for lifestyle (smoking status, alcohol use and physical activity) using IPAQ17 (as categorized in Table 1) and number of offspring, because it may be socially patterned and associated with subsequent adiposity.18 Model 3 was additionally adjusted for SEP at the other two life stages.
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We present sex-specific mean differences with 95% confidence intervals (CI). The heterogeneity of association by sex and age group (50 to <60 and
60 years) was assessed from the significance of interaction terms and the heterogeneity of effect across strata. We assessed if the effects of life-course SEP trajectory were more than a simple sum of effects at each life stage (supra-additive effects19 in model 3) from the significance of the difference in the likelihood ratio test on the relevant chi-square distribution. Proxies of SEP were unavailable or unclassifiable for 23% of the participants, mainly because longest held occupation was missing for some of the women, who may have had a varied job history rather than a single definable longest held occupation. For these participants we used multiple imputation.20 SEP at any stage was predicted based on a flexible additive regression model with predictive mean matching incorporating age, sex, leg length, seated height and SEP at the other two stages. We imputed missing values 10 times and analysed each complete dataset separately. We summarized the results into single estimated β-coefficients with confidence intervals and P-values adjusted for the missing data uncertainty.20 As a sensitivity test, complete case analysis without imputation was performed. In addition, we repeated the analyses using personal income as an indicator of adulthood SEP because it was more complete, and arguable that women's own occupation is not a good SEP indicator.21
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Of the 9998 participants examined, 3.7% (379) had missing data for BMI, WHR, confounders or data needed for imputing SEP. Analysis was based on the remaining 9619 participants. Education was imputed for 10, parental possessions for 221 and occupation for 2324. There were more women (6917) than men (2702) (Table 1), the women were younger [mean age 59.8 years (SD ± 6.6)] than the men [mean age 63.1 (SD ± 6.4)]. Age ranged from 50 to 94 years and 1111 were aged
70 years.
Higher childhood SEP was associated with greater height (Table 1); and this association remained after adjustment for age (data not shown). Men and women with low SEP at any life stage were older, more likely to be smokers and had more offspring (Table 1). Women with high SEP at any life stage were more active and more likely to be ever-users of alcohol (Table 1). There was no evidence that the associations between SEP at any stage and BMI or WHR in men and women differed by age group (all P-values 0.09, data not shown). However, the associations between SEP at any stage, and BMI and WHR consistently differed by sex (Table 2).
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In men, childhood SEP was positively associated with higher BMI and WHR, as was late adult SEP with BMI (Table 2). In women SEP was usually negatively associated with BMI and WHR, although this association was least evident for childhood SEP. A sensitivity analysis using personal income instead of occupation produced similar results, and additionally a positive association between later adult SEP and WHR (Appendix 1). A complete case analysis also produced broadly similar results.
Life-course SEP trajectories did not have an effect over and above (supra-additive effect) that of SEP at each life stage in men or women (all P-values 0.38, data not shown), as illustrated in Figure 1.
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Consistent with studies from developed settings22,23 older Chinese women (
50 years) with low SEP had more general and central obesity than other women. Higher early adulthood SEP mainly contributed to lower BMI and WHR in women. In contrast, older Chinese men showed little consistent association between life-course SEP and adiposity, although higher childhood SEP contributed to higher BMI and WHR and late adulthood SEP to higher BMI. These differences between men and women were significant. There was no evidence that any trajectory of life-course SEP had effects beyond the effect of SEP at each life stage, suggesting that environmental mismatch within one life time, as represented here by discordant life-course SEP, does not affect adiposity. Our findings in women are consistent with observations in long-term industrialized countries where low SEP across the life course is associated with obesity,6,24 although in developing countries, higher SEP may be associated with obesity.25,26 However, the burden of obesity usually shifts towards groups with lower SEP with increases in gross national product (GNP)27,28 and our findings may be a reflection of the rapid pace of growth and currently relatively high GNP in Guangdong province.13,29 Guangzhou, with a per capita GNP of US$4596 in 2004,29 typical of a middle-income economy is most likely transitioning from under-nutrition to a nutritionally affluent society.30,31 The shift of obesity towards lower SEP groups typically occurs at a later stage of economic development in men than in women,10 consistent with our findings of the different effects of SEP at three life stages on obesity in men and women, with little relation between life-course SEP and obesity in men.
This study does not provide clear support for environmental mismatch over the life course increasing obesity in the rapidly transitioning population of Guangzhou. To date, studies in mainly western populations, have similarly found that mismatched social position over the life course does not contribute to a related outcome, i.e. cardiovascular risk, over and above the contribution of social position at each stage.32–34 Few studies have examined environmental mismatch and obesity in humans, because most studies have concentrated on the effect of birth weight and growth during infancy and/or childhood on later life obesity,35–37 so these previous studies are not directly comparable with ours. Nevertheless, there are several reasons why our study may have been unable to find evidence of mismatch. First, very few of our participants knew their birth weight, so we have no specific measure of possibly all-important prenatal conditions, nor do we have information on infant exposures. However we would have expected some continuity between a person's childhood exposures proxied by parental possessions here and their slightly earlier infant and pre-natal exposures. Second, our participants grew up in China largely around the time of the great leap forward probably resulting in a relatively lower difference between low and high childhood SEP, thus making the magnitude of mismatch between SEP groups too small to capture. However, higher childhood SEP was associated with greater height suggestive of some differences by childhood SEP in early life exposures. Third, given the general level of food availability and the isolation of China until the 1980s, it is unlikely that our participants were exposed to over-feeding or to westernized diets until relatively late in life, by which time the exposures may not be relevant to priming life long physiological responses. Fourth, the exact timing and nature of the mismatch may be crucial. Our study considered environmental mismatch within a single generation whilst environmental mismatch over generations mediated by epigenetic mechanisms may be a more appropriate conceptualization. Fifth, most of the evidence for environmental mismatch leading to obesity comes from rodent models.38 Growth patterns in humans are different from rodents; humans achieve maximal growth velocity during gestation with postnatal growth rates declining during infancy and a growth spurt again during puberty.39,40 Pubertal changes in endocrine function and the adolescent growth spurt may play a more important role in development in humans than in many other mammals.39
In women, our findings are consistent with the ‘association hypothesis’ by which longer duration of exposure to risk factors such as low SEP increases the risk of adiposity.41 A high SEP at any life stage could reverse or halt this accumulation and would also shorten the duration of exposure to the behavioural risk factors associated with low SEP. However, that we did not see the same association in men requires an explanation, particularly as similar findings have been seen, but not explained in other developing countries.42,43 Typically, this difference between men and women in the social patterning of obesity in response to economic development is explained in terms of differential social pressures on men and women,44 which more quickly shift women's preferences towards slimmer bodies unlike the fatter body shapes culturally preferred in developing countries.28 For men larger size translating into physical dominance could militate against education and awareness, although the processes of the nutrition transition often worsens the inequalities in diet between the rich and the poor, with the low status groups (which generally includes women) more likely to bear the brunt of economic and cultural convergence towards high density poor-nutritious diets.45 Given the recent transition in China and the age of our cohort it is surprising that these differential social forces were evident at the start of the transition, i.e. during the cohort's childhood and early adulthood. Alternatively, considering the importance of puberty in humans, we have previously suggested, based on physiological evidence, that puberty may be a key developmental window when sexual dimorphism in central obesity arises. Pubertal sex-steroids are nutritionally driven. Pubertal sex-steroids generate a more android fat pattern in boys, with correspondingly opposite effects in girls.46 The metabolic profile at the end of puberty tracks into adult life.46 In a population undergoing economic and epidemiological transition, higher SEP and hence more plentiful nutrition during adolescence, could then counter the generally protective effect of social advantage, in boys.47 To date, there is limited evidence for this theory.46–48 Nevertheless, if we speculate correctly, the predictive adaptive response theory may need to be conceptualized within a framework that encompasses all phases of development, including puberty.
There are several limitations to our study. First, the cross-sectional design makes it difficult to infer causation, especially for the association of adult SEP with adiposity, but this design should not affect the association between childhood or early adult SEP and adiposity. Second, we used potentially unreliable retrospective information for childhood conditions. Third, there could be gender based allocation of resources within families, most likely favouring boys and men or some other unmeasured sex-specific confounders. Fourth, our participants experienced the socio-political upheaval of the Great Leap Forward and the Cultural Revolution at different ages, most likely with highly heterogeneous effects, by class, location, age and sex. However there was little evidence of different effects by age group. Fifth, our participants were not a randomly selected, population representative sample; however that should not affect internal relationships, unless we are preferentially missing groups with particular associations between SEP and adiposity. Finally, we lack complete information on SEP, where we used multiple imputation, as a computationally convenient way of using all available data, while preserving the uncertainty from the missing data,49 minimizing inclusion bias and increasing statistical power.20 Moreover, the findings were generally robust when personal income replaced longest held occupation as proxy of late adulthood SEP.
Our study is one of the first, to our knowledge, to assess the association of life-course SEP with obesity in a developing society. It highlights the importance of understanding life-course SEP in the context of the epidemiological transition and stage of economic development. Our study provides little support for the notion of mismatched conditions over a single life course contributing to the current epidemic of obesity in developing countries, either because of the crude SEP proxies and the masking effect of strong economic growth or because the developmental origins of health paradigm needs to be extended to consider influences throughout growth. However, our study highlights the different effects of socio-economic development on men and women potentially with a critical period in pre-adult life, which needs to be elucidated so that the impact of the epidemiologic transition and environmental mismatch can be assessed and appropriate interventions to prevent obesity in transitioning populations developed.
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The University of Hong Kong Foundation for Development and Research, Hong Kong; the University of Hong Kong University Research Committee Strategic Research Theme Public Health, Hong Kong; Guangzhou Public Health Bureau; Guangzhou Science and Technology Bureau, Guangzhou, China; the University of Birmingham, UK.
Appendix 1 Adjusted mean differences in BMI and WHR with 95% CIs for SEP at each life stage using personal income as proxy for late adulthood SEP stratified by sex for 9619 older Chinese adults in the Guangzhou Biobank Cohort Study, Phase 2 (2005–06)
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Ref = reference group.
Model 1 adjusts for age (5-year age groups).
Model 2 adjusts for age (5-year age groups), smoking status, alcohol use status, physical activity and number of offspring.
Model 3 adjusts for age (5-year age groups), smoking status, alcohol use status, physical activity, number of offspring and other two SEP variables.
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The Guangzhou Biobank Cohort Study investigators include: Guangzhou No. 12 Hospital: XQ Lao, WS Zhang, M Cao, T Zhu, B Liu, CQ Jiang (Co-PI); the University of Hong Kong: CM Schooling, SM McGhee, RF Fielding, GM Leung, TH Lam (Co-PI); the University of Birmingham: GN Thomas, P Adab, Y Peng, KK Cheng (Co-PI). We would also like to thank Prof. Sir R Peto and Dr ZM Chen of the Clinical Trial Service Unit, the University of Oxford for their support.
Conflict of interest: None declared.
KEY MESSAGES
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