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American Journal of Epidemiology Advance Access originally published online on December 4, 2007
American Journal of Epidemiology 2008 167(4):419-428; doi:10.1093/aje/kwm329
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Life-Course Origins of Social Inequalities in Metabolic Risk in the Population of a Developing Country

C. M. Schooling1, C. Q. Jiang2, T. H. Lam1, W. S. Zhang2, K. K. Cheng3 and G. M. Leung1

1 Department of Community Medicine and School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, China
2 Guangzhou Occupational Diseases Prevention and Treatment Centre, Guangzhou No. 12 Hospital, Guangzhou, China
3 Department of Public Health and Epidemiology, University of Birmingham, Birmingham, United Kingdom

Correspondence to Professor T. H. Lam, 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: commed{at}hkucc.hku.hk).

Received for publication July 9, 2007. Accepted for publication October 8, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In countries that have been industrialized for a long time, but not always elsewhere, low socioeconomic position (SEP) is associated with ischemic heart disease in men. The authors hypothesized that socioeconomic development could, via pubertal sex steroids, promote an atherogenic lipid profile and body shape in men but not in women. Therefore, they examined the associations of SEP with ischemic heart disease risk in a developing-country population. The authors used multivariable regression to examine the associations of SEP with the metabolic syndrome and its components in 9,746 Chinese adults aged ≥50 years from the Guangzhou Biobank Cohort Study, phase 2, recruited in 2005–2006. After adjustment for age, smoking, alcohol use, and physical activity, high SEP at each of three life stages, proxied by parental possessions in childhood, education, and longest held-occupation, was inversely associated with the metabolic syndrome in women but not in men. Higher SEP in men was associated with lower pulse pressure and fasting plasma glucose level but also with greater waist circumference and a lower high density lipoprotein cholesterol level. With socioeconomic development, diet-related hormonal changes at puberty may outweigh the usual protective effect of social advantage in men, with corresponding implications for boys currently undergoing the nutrition transition in the developing world.

China; developing countries; gonadal steroid hormones; metabolism; myocardial ischemia; risk factors; social class

Abbreviations: CI, confidence interval; HDL, high density lipoprotein; OR, odds ratio; SEP, socioeconomic position


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In Western countries that have been industrialized for a long period of time, ischemic heart disease is currently associated with poor childhood conditions (1) and with low socioeconomic position (SEP) across the life course (2, 3). In these same countries, the social patterning of ischemic heart disease in men reversed over the 20th century, from an association with high SEP to one with low SEP (4), although this finding has been controversial (5). Nevertheless, mounting evidence from settings outside Western Europe and North America makes it increasingly clear that the social patterning of ischemic heart disease or its risk factors is not universal but epidemiologic stage-specific (6–12), as Marmot originally hypothesized (13). Whether such epidemiologic stage specificity also affects the sexes differentially is not clear (14–16). In long-term industrialized countries, the impact of low SEP on ischemic heart disease sometimes appears to be greater in women (3, 17, 18), for reasons which are not clearly understood, but investigators have tended to interpret this finding mainly in terms of contemporaneous risk factors that differ by sex (18).

In industrialized countries, a more atherogenic lipid profile and body shape emerge in boys at puberty while the reverse happens in girls, because of the action of sex steroids, which lower levels of high density lipoprotein (HDL) cholesterol in boys and increase sexual dimorphism in body shape in both sexes (19–23). These sex-specific pubertal changes have previously been suggested as contributing to the earlier development of ischemic heart disease in men (20). Moreover, sex differences in HDL cholesterol level appear to be context-specific (24), which suggests that they are environmentally driven. Increases in the amount, tempo, and intensity of pubertal development with macroeconomic improvement due to better nutrition provide a potential explanation. This would counter the generally protective effect of social advantage among men in the early stages of economic development, when the socially advantaged might experience improved nutrition first.

In a large sample of older residents of Guangzhou in southern China, we assessed the relation of SEP at three stages in the life course with ischemic heart disease risk (proxied by the metabolic syndrome and its components (25, 26)). China is a society at an early stage of the epidemiologic transition (27). We tested three related hypotheses in this developing-country setting. First, was higher SEP less protective against the metabolic syndrome in men than in women? Second, was higher SEP less protective against central obesity and low HDL cholesterol in men than in women? Third, as a counterfactual example, was higher SEP similarly associated with precursors of diabetes in men and women? Diabetes risk appears to be more strongly related to another hypothalamic-pituitary-endocrine axis, namely growth hormone (28), and thus should not be affected by pubertal sex steroids (29–33).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Sources of data
The Guangzhou Biobank Cohort Study is a collaboration between the Guangzhou No. 12 Hospital (Guangzhou, China) and the universities of Hong Kong (Hong Kong, China) and Birmingham (Birmingham, United Kingdom). The study has been described previously in detail (26). Subjects were drawn from the Guangzhou Health and Happiness Association for the Respectable Elders, a community social and welfare association unofficially aligned with the municipal government, where membership is open to anyone aged 50 years or older for a nominal monthly fee of 4 yuan (US $0.50). Approximately 7 percent of permanent Guangzhou residents aged 50 years or more are members of the Guangzhou Health and Happiness Association for the Respectable Elders. Eleven percent of the members were selected for this study and were included if they were capable of consenting, were ambulatory, and were not receiving treatments which, if discontinued, might have resulted in immediate life-threatening risk, such as chemotherapy or dialysis. Of those eligible, 90 percent of the men and 99 percent of the women participated. Subjects included in this analysis underwent a detailed half-day medical interview that included information on disease history, as well as a physical examination conducted in the morning, with fasting blood sugar being measured (26). In view of the unique lifetime experiences of this cohort, spanning a period of rapid epidemiologic transition from largely preindustrial conditions to a quickly developing economy, additional questions about the participants' early lives were introduced in phase 2 of recruitment. The Guangzhou Medical Ethics Committee of the Chinese Medical Association approved the study, and all subjects gave written, informed consent prior to participation.

Details on the measurement methods have been reported elsewhere (26). In brief, seated blood pressure was recorded as the average of the last two of three measurements taken using the Omron 705CP sphygmomanometer (Omron Corporation, Kyoto, Japan). Waist circumference was measured horizontally at the smallest circumference between the ribs and the iliac crest, or at the level of the naval for obese participants. Fasting HDL cholesterol, triglyceride, and glucose levels were determined by means of the Shimadzu CL-8000 Clinical Chemical Analyzer (Shimadzu Corporation, Kyoto, Japan).

SEP across the life course
As in other, similar studies, we used education and longest-held occupation as proxies for adult SEP (18). Educational level was categorized into three groups (low, medium, and high): primary school or less (≤6 years of education), junior middle school (7–9 years of education), and senior middle school or above (≥10 years of education). Occupation was categorized as manual (agricultural work, factory work, or sales and service) or nonmanual (administrative/managerial, professional/technical, or military/police). By definition, preindustrial societies lack the technology to record and preserve detailed information about their citizens, so we were restricted to retrospective information about childhood conditions. As proxy measures of participants' childhood environments, we specifically selected the parental possession of three simple, notable items that were appropriate to China in the mid-20th century, based on sociologic accounts of life in southern China at that time (34–36). The items selected were parental possession of a watch, a sewing machine, and a bicycle. These items were also categorized on a three-point scale as 0, 1 or 2, and 3.

Outcome specification of ischemic heart disease risk
The metabolic syndrome was defined according to the criteria of the International Diabetes Federation (37)—that is, waist circumference ≥80 cm in women or ≥90 cm in men, plus any two of the following four factors: 1) triglyceride level ≥1.7 mmol/liter; 2) HDL cholesterol level <1.03 mmol/liter in men or <1.29 mmol/liter in women or treatment for this specific abnormality; 3) systolic blood pressure ≥130 mmHg or diastolic blood pressure ≥85 mmHg or treatment for hypertension; and 4) fasting plasma glucose level ≥5.6 mmol/liter or previously diagnosed type 2 diabetes. Five outcomes corresponding to the components of the metabolic syndrome—that is, waist circumference, blood pressure, fasting plasma glucose, triglycerides, and HDL cholesterol—were also considered. Three measures of blood pressure—systolic, diastolic, and pulse pressure—were included, because in younger people systolic and diastolic blood pressure track together, while in older people systolic blood pressure continues to rise, diastolic blood pressure falls, and the difference between them (pulse pressure) may be predictive of ischemic heart disease risk (38).

Statistical analysis
Multivariable logistic regression was used to assess the association of each measure of SEP with the metabolic syndrome. In model 1, we adjusted only for age in 5-year groups. In model 2, we also adjusted for lifestyle (smoking status, alcohol use, and physical activity as categorized in table 1) and height to control for possible famine exposure, as well as to control more generally for net nutrition in childhood. In model 3, we additionally adjusted for the other two measures of SEP. Multivariable linear regression was used to assess the association of each measure of SEP with waist circumference, blood pressure, fasting plasma glucose, triglycerides, and HDL cholesterol, with additional adjustment for the use of relevant medication where appropriate. The results of sex-specific analyses are presented. The heterogeneity of association by sex was assessed from the significance of interaction terms. We similarly assessed whether the associations were consistent in men and women at younger (50–<60 years) and older (≥60 years) ages from the significance of interaction terms.


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  		TABLE 1. Characteristics (mean value or percentage) of 9,746 Chinese adults aged ≥50 years according to socioeconomic position at three stages of the life course (proxy measures) and sex, Guangzhou Biobank Cohort Study, phase 2, 2005–2006

 
Proxy measures of SEP were not available or not classifiable for 23 percent of the participants, primarily because information on longest-held occupation was missing, mainly 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 (39, 40) (10 imputations). SEP at any stage was predicted on the basis of a flexible additive regression model with predictive mean matching (39) incorporating data on age, sex, leg length, seated height, and SEP at the other two stages. We imputed missing values and analyzed the 10 complete data sets separately. We summarized the results into single estimated beta coefficients with confidence intervals and p values adjusted for the missing data uncertainty (40). As a sensitivity check, we also performed the analyses without imputation while omitting the subjects with missing data.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Of the 9,998 participants examined, 2.5 percent (n = 252) had missing data related to the metabolic syndrome, potential confounders, or data needed for imputing SEP. Analysis was based on the remaining 9,746 participants. Education was imputed for 10 participants, parental possessions for 195, and occupation for 2,344. There were more women (n = 7,011) than men (n = 2,735) enrolled, and the women were younger (mean age = 59.8 years (standard deviation, 6.6)) than the men (mean age = 63.1 years (standard deviation, 6.4)). Ages ranged from 50 years to 94 years, but only 78 participants were aged 75 years or older.

Higher SEP was consistently associated with greater height (table 1), and this association remained after adjustment for age (data not shown). Parental possession of all three specified objects (watch, sewing machine, and bicycle) was associated with ever use of alcohol and physical activity in both sexes and with never smoking in women (table 1). Higher education was associated with never smoking in both sexes and also with use of alcohol and physical activity in women. Working in a nonmanual occupation was associated with never smoking in both sexes.

With adjustment only for age, each measure of SEP was clearly associated with lower risk of the metabolic syndrome in women but not in men (model 1 in table 2). Further adjustment for height and lifestyle (smoking, alcohol use, and physical activity) in model 2 had little effect.


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  		TABLE 2. Odds ratio for the presence of the metabolic syndrome among 9,746 Chinese adults aged ≥50 years according to socioeconomic position at three stages of the life course (proxy measures) and sex, Guangzhou Biobank Cohort Study, phase 2, 2005–2006

 
In women, both higher childhood SEP and higher education were independently associated with lower risk of the metabolic syndrome, although longest-held occupation was not (model 3). In contrast, in men, SEP was unrelated to the metabolic syndrome by any of the three measures. Associations between SEP at all three stages in the life course and the metabolic syndrome differed in men and women (p values for sex interactions were uniformly less than 0.05). In both sexes, there was no evidence that the associations of childhood SEP or occupation with the metabolic syndrome varied with age. The negative association of education with the metabolic syndrome was slightly stronger in younger (50–<60 years) women (odds ratio (OR) = 0.74 (95 percent confidence interval (CI): 0.60, 0.91) and OR = 0.54 (95 percent CI: 0.42, 0.69) for medium and high education, respectively, as compared with low education in model 3) than in older (≥60 years) women (OR = 0.85 (95 percent CI: 0.67, 1.08) and OR = 0.65 (95 percent CI: 0.48, 0.87) for the same comparison); however, there was a clear negative association in both age groups.

Table 3 shows the association of each dimension of the metabolic syndrome with SEP in models 2 and 3 only for compactness. In women, higher childhood SEP was independently associated with lower pulse pressure, and higher education was independently associated with lower waist circumference, lower blood pressure, a lower fasting plasma glucose level, and a lower triglyceride level (model 3 in table 3). In contrast, in men, higher childhood SEP was independently associated with greater waist circumference and lower HDL cholesterol. Higher education was independently associated with lower systolic and pulse pressure and a lower fasting glucose level. Nonmanual occupation was also associated with greater waist circumference and a lower HDL cholesterol level in men.


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  		TABLE 3. Adjusted absolute difference ({Delta}) in levels of ischemic heart disease risk factors among 9,746 Chinese adults aged ≥50 years according to socioeconomic position at three stages of the life course (proxy measures) and sex, Guangzhou Biobank Cohort Study, phase 2, 2005–2006

 
The associations between SEP and the central adiposity and lipid dimensions of the metabolic syndrome (waist circumference, triglycerides, and HDL cholesterol) were different in men and women. However, there was no evidence that the associations between SEP and fasting blood glucose level varied between men and women.

In both sexes, there was no evidence that the associations of childhood SEP with any dimension of the metabolic syndrome varied with age. In the men, there was no evidence that the associations of education or occupation with any dimension of the metabolic syndrome varied with age. In women, there were some possible differences in the associations of education and occupation with blood pressure, but these were not evident in the fully adjusted model (model 3). However, nonmanual occupation was associated with lower triglyceride levels only in the younger women (0.15 mmol/liter lower, 95 percent CI: 0.30, 0.01), not in the older women (0.07 mmol/liter higher, 95 percent CI: –0.08, 0.21). The results did not change appreciably when we did not impute information for missing items but instead analyzed the data by restricting the sample to persons with complete information (data not shown).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
As is currently the case in Western settings, in this Chinese study higher SEP was protective against the metabolic syndrome and corresponding manifestations of metabolic derangement in women. In men, on the other hand, SEP was unrelated to the metabolic syndrome, because SEP had inconsistent associations with components of the metabolic syndrome. Higher education in men was associated with lower pulse pressure and a lower fasting blood glucose level, with similar effect sizes as in women. However, in men, higher childhood SEP was also associated with greater waist circumference and a lower HDL cholesterol level, which was not evident in women.

These findings are consistent with our three hypotheses that, at this stage of economic development in China, social advantage would be less protective against metabolic risk in men, because of differences in lipid levels and central obesity, but not precursors of diabetes. Nevertheless, there are several caveats. First, we used potentially unreliable self-reports of parental possessions as a proxy for childhood conditions, albeit with items suitable to our population. However, parental possessions were consistently associated with greater height. Second, in the childhoods of these subjects, there could have been gender-based allocation of resources within families, most likely favoring boys, or there could have been differential residual confounding or different behavioral responses to SEP in men and women. However, these factors would have been unlikely to generate the differences in associations specific to certain components of the metabolic syndrome that we found. It is difficult to envisage how socially patterned dietary habits or lifestyle in men could have resulted in lower pulse pressure and fasting plasma glucose without any impact on the other dimensions of cardiovascular risk, and as such, this pattern of observations is not really compatible with a strong confounding effect of adult diet and/or lifestyle. Third, our participants experienced the sociopolitical upheaval of the Great Leap Forward and the Cultural Revolution at different ages. It would be inappropriate for us to speculate about the direction, let alone the magnitude, of the potential impact of these events on the observed outcomes without a detailed understanding of the (probably nuanced and highly heterogeneous) effects, by class, location, age, and sex, imposed by exposure to the Cultural Revolution and the Great Leap Forward. However, there was little evidence of different effects in different age groups. Fourth, our participants were not a randomly selected, representative sample of the population; however, that should not have affected internal relations. Fifth, we carried out many tests of interaction between age and SEP, so it is possible that the few apparent differences we found are a chance result of multiple comparisons. Finally, we lacked complete information on SEP, where we used multiple imputation. This technique provides a computationally convenient way of using all available data, as well as preserving the uncertainty from the missing data (41), minimizing inclusion bias and increasing statistical power (40).

To our knowledge, this was the first study to examine SEP at three different stages of the life course in relation to ischemic heart disease risk factors in an Asian setting, or more pertinently a developing-country setting. Nevertheless, our findings in women are consistent with observations in long-term industrialized countries on the detrimental effect of low SEP across the life course on ischemic heart disease risk (2, 17). Although our findings in men are not consistent with the association between low SEP and ischemic heart disease that is usually found in long-term industrialized countries (17), they are consistent with the (usually overlooked) discrepant associations between SEP and ischemic heart disease risk in men and women observed in Southern Europe (17) and Israel (3), which have a different history of socioeconomic development and thus a different epidemiologic history from Western Europe. Moreover, our specific observation that childhood SEP, independently of later-life SEP, has different associations with HDL cholesterol and waist circumference in men and women but not with a precursor of diabetes (higher glycated hemoglobin) has previously been demonstrated (but not explained) in the United Kingdom (18).

Our finding of no association between SEP and the metabolic syndrome only among men in a society at an early stage of the epidemiologic transition also provides support for the contention that a reversal in the social patterning of ischemic heart disease with economic development does happen but is specific to men (16). Our findings on the different dimensions of ischemic heart disease risk provide preliminary evidence for our biologically based hypothesis that nutritionally driven increases in sex steroid levels at puberty (42–47), facilitated by the epidemiologic transition, generate a less favorable HDL cholesterol profile in boys while having the opposite effect in girls (19–23), without causing sex differences in precursors of diabetes (28–33). Lipids and central obesity track across the life course from adolescence (48). Moreover, our hypothesis implies that the ischemic heart disease epidemic that emerged in men only with economic development (14, 15) could have arisen as a result of corresponding population-wide improvements in nutrition during childhood and puberty, with an associated detrimental impact on male central obesity and HDL cholesterol. Furthermore, more plentiful nutrition in boys in the developing world could potentially be currently fueling a future ischemic heart disease epidemic, albeit with potential benefits in girls.

Our study highlights the importance of interpreting life-course pathways in the historical context of economic development. Further investigation of the role of pubertal nutrition in the life-course development of ischemic heart disease is urgently needed, so that the long-term consequences of the nutrition transition in early life can be assessed and any potential risks averted before irrevocable changes in eating habits have taken place throughout the developing world.


   ACKNOWLEDGMENTS
 
This study was funded by the University of Hong Kong Foundation for Educational Development and Research, the Guangzhou Public Health Bureau, the Guangzhou Science and Technology Committee, and the University of Birmingham.

The authors thank the Clinical Trial Service Unit of the University of Oxford for their support and the Guangzhou Health and Happiness Association for the Respectable Elders for convoking the subjects.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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