Intergenerational ‘mismatch’ and adiposity in a developing population: The Guangzhou biobank cohort study

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Abstract

Intergenerational ‘mismatch’ between maternal and adult environments, common in developing economies, has been hypothesized as contributing to obesity. In a rapidly developing population, we examined whether maternal conditions, proxied by maternal literacy, were associated with adult adiposity, proxied by body mass index (BMI) and waist–hip ratio (WHR) and whether these associations were modified by later life conditions, proxied by socio-economic position (SEP) at three life stages. We also examined if maternal conditions had sex-specific associations with adult adiposity. In a cross-sectional study of 19,957 adults (≥50 years) from the Guangzhou Biobank Cohort Study (phases 2 and 3 in 2005–2008), we used multivariable linear regression to assess the association of maternal literacy with BMI and WHR, and whether the associations varied with sex, age or SEP. The adjusted association of maternal literacy with WHR varied with sex. In women, but not men, maternal illiteracy was associated with higher WHR and BMI, adjusted for age; these associations remained, although attenuated, after adjusting for lifestyle, life course SEP and paternal literacy. There was little evidence that associations varied with SEP at any stage, although continuity of poor conditions into early life may have exacerbated the association of maternal illiteracy with higher WHR in women. Poor maternal conditions in developing populations may increase vulnerability to adiposity in women. Whether such sex-specific intergenerational effects are driven by epigenetics, maternal sex hormones or other mechanisms, remains to be determined. However, mismatched maternal and later life conditions do not appear to be associated with adiposity. Our findings, although preliminary, imply that a transient epidemic of obesity may occur in the first generation of women who experience economic development.

Introduction

Obesity is a major contributor to the global burden of chronic diseases such as type 2 diabetes, cardiovascular disease and some cancers along with disability (World Health Organization, 1997). The number of obese people has grown over the last decade to 400 million (World Health Organization, 2005); sometimes with faster increases in developing than developed countries. Typically environmental, lifestyle and nutritional changes enabled by socio-economic development and rural to urban migration are seen as driving this epidemic. However, recently there has been increasing consideration of obesity (and other metabolic conditions) in the context of human developmental and evolutionary biology, with intergenerational environmental cues potentially driving the adipogenic response to nutritional excess (Varela-Silva, Azcorra, Dickinson, Bogin, & Frisancho, 2009).

Intergenerational effects on adiposity have largely been investigated from two main perspectives; the transmission of social disadvantage as a ‘fundamental cause’ of obesity (Link & Phelan, 1995) and the long-term effects of foetal and early life environment. Focusing on social causes could be taken as obviating the need to consider intervening mechanisms, however, particularly in developing countries, knowledge of underlying mechanisms may facilitate more rapid improvements in population health or more explicitly acknowledged trade-offs (Wagstaff, 2002). Few studies have been able to consider social disadvantage over generations (Modin & Fritzell, 2009). Measures of high parental socio-economic position (SEP) are usually associated with low adult adiposity, particularly in women perhaps because of sex-specific social pressures (Senese, Almeida, Fath, Smith, & Loucks, 2009). Notwithstanding the pervasive detrimental effects of social disadvantage, we have previously hypothesized that in some populations the generally detrimental effects of social disadvantage may be countered in men for adiposity by a more plentiful growth environment acting via pubertal sex hormones to generate a life long more android fat pattern, with correspondingly opposite effects in women where pubertal sex hormones generate a more gynoid fat pattern (Schooling, Jiang, et al., 2008). We have previously postulated that the underlying mechanism for this association is nutritionally-driven levels of sex-steroids set during growth having persistent effects throughout life (Schooling et al., 2008, Schooling et al., 2008, Schooling et al., 2007) with potentially effects across generations via hormone levels in pregnancy (Chung et al., in press, Schooling and Leung, in press, Wong et al., 2009). Maternal experiences affect the development and functioning of the offspring's gonads in both sexes (Leonhardt et al., 2003, Satoh, 1991), with well-known life long consequences for breast cancer (Trichopoulos, 1990). Similarly intergenerational experiences i.e. maternal environment could also have sexually dimorphic effects on offspring adiposity, particularly for central obesity.

Foetal environment, mainly proxied by birth weight, has also been examined as a determinant of cardiovascular diseases, diabetes and adiposity (Barker, 1998, Huxley et al., 2007, Whincup et al., 2008). However, birth weight is not clearly, linearly associated with adiposity (Wells, Chomtho, & Fewtrell, 2007). Nevertheless, intergenerational effects on adiposity may be driven by ‘mismatch’ between biology and environment driving the adipogenic response to nutritional excess (Gluckman & Hanson, 2006). Intergenerational ‘mismatch’ may occur when there is a maternally constrained environment followed by a nutritionally rich post-natal environment (Gluckman, Hanson, & Pinal, 2005), because environmental cues during the critical period of maternal/foetal growth, possibly via epigenetic mechanisms, may biologically prime the pathways regulating energy homeostasis (Gluckman & Hanson, 2006). A sudden increase in the degree of ‘mismatch’ as often seen in rapidly transitioning populations could increase the risk of obesity (Gluckman & Hanson, 2006). In older people from a rapidly transitioning population we have previously shown that mismatched conditions within a single life course were not associated with adiposity (Kavikondala et al., 2009), perhaps because the ‘mismatch paradigm’ is better considered in an intergenerational framework.

Currently, most of the evidence for intergenerational mismatch comes from experiments in small mammals where maternal/foetal stress followed by nutritional excess leads to later life adiposity (Ikenasio-Thorpe et al., 2007, Ozanne et al., 2004) in both sexes. In usually well-fed western populations a transient experience of extreme food scarcity during pregnancy, such as during the Dutch famine, may be associated with offspring adiposity (Ravelli, van der Meulen, Osmond, Barker, & Bleker, 1999), although there was no such association for the offspring of mothers' pregnant during the Leningrad siege (Stanner et al., 1997). However whether the experience of a relatively short exposure to famine, most likely followed by catch-up growth, in otherwise well-fed western populations can be extrapolated to developing populations, where many generations have experienced very limited living conditions throughout life, is unclear. Moreover, how the mismatch hypothesis should be interpreted and tested in such socio-ecological settings of rapidly transitioning populations, to which it is perhaps most relevant, is rarely investigated. One study from China compared people born during famine to people born later and found those born during famine to be more adipose (Yang, Zhao, et al., 2008). However the study did not consider the potentially confounding influence of age and varying later life course conditions on adiposity in adulthood.

In this study we took advantage of a large sample of older (≥50 years) people from southern China, who due to recent and rapid economic development have experienced transitions through very different economic and social environments during their lives, to examine these two different hypotheses concerning the pathogenesis of adult adiposity, shown schematically in Fig. 1. First, we examined a general intergenerational hypothesis (Fig. 1A), i.e. whether maternal conditions, proxied by maternal literacy, had effects on later life adiposity, proxied by body mass index (BMI) and waist–hip ratio (WHR), either directly or indirectly, and whether these were sex-specific. Second, we examined an intergenerational ‘mismatch’ hypothesis (Fig. 1B), i.e. whether the association between maternal conditions and later life adiposity was modified by later life living conditions, proxied by SEP at three stages in the life course (childhood, early adulthood and late adulthood).

Section snippets

Sources of data

The Guangzhou Biobank Cohort Study is a collaboration between the Guangzhou No. 12 Hospital and the University of Hong Kong and University of Birmingham, UK which has been described in detail (Jiang et al., 2006). Participants were drawn from “The Guangzhou Health and Happiness Association for the Respectable Elders” (GHHARE), a community social welfare association unofficially aligned with the municipal government where membership is open to anyone aged 50 years or older for a monthly, nominal

Results

Of the 20,086 participants examined, 0.64% (129) had missing data for BMI, WHR or data needed for imputing maternal and paternal literacy and SEP. Analysis was based on the remaining 19,957 participants. There were more women (14,623) than men (5334), the women were younger (mean age 59.5 (standard deviation (SD) ± 7.1)) than the men (mean age 63.1 (SD ± 7.04)). Age ranged from 50 to 96 years and 2641 were aged 70 years or older.

Table 1 shows the distribution of life course SEP, age and

Discussion

In an ethnically homogeneous older (≥50) population, where everyone experienced improved living conditions during their lifetime, we found some evidence for intergenerational effects but little evidence for intergenerational ‘mismatch’. Maternal literacy was negatively associated with adiposity in women, but there was no evidence that the association was greater when there was a mismatch between maternal conditions and later conditions proxied by SEP in childhood, early adulthood or late

Conclusion

This study provides evidence from a rapidly developing population that poor maternal conditions are associated with adiposity in women. There was little evidence that specifically mismatched intergenerational conditions were associated with adult adiposity in men or women. Whether the association between poor maternal conditions and adiposity in women is driven by exposure of a growing foetus to maternal sex hormones or through other mechanisms is not clear. However, regardless of the

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    The study was funded by The University of Hong Kong Foundation for Development and Research and The University of Hong Kong University Research Committee Strategic Research Theme Public Health; Guangzhou Public Health Bureau, and Guangzhou Science and Technology Bureau, China; and The University of Birmingham, UK. 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.

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