a National Center for Preventive Medicine, Public Health Ministry of Russia, Moscow, Russia.
b Department of Biostatistics, School of Public Health, University of North Carolina, Chapel Hill, NC, USA.
c Cardiovascular Institute and Fu Wai Hospital, Chinese Academy of Medical Sciences, Beijing, PRC.
d Institute of Public Health, Collegium Medicum Jagiellonian University, Krakow, Poland.
e Hadassah University Hospital, Jerusalem, Israel.
f Department of CVD Epidemiology and Prevention, Stefan Cardinal Wyszynski, National Institute of Cardiology, Warsaw, Poland.
g Department of Cardiovascular Epidemiology, Guangdong Provincial Cardiovascular Institute, Guangzhou, PRC.
h Department of Epidemiology, School of Public Health, University of North Carolina, Chapel Hill, NC, USA.
Correspondence: Sandra H Irving, Department of Biostatistics, School of Public Health CB#8030, University of North Carolina, Chapel Hill, NC 27514, USA.
Abstract
Background The association between coronary heart disease (CHD) and social status has differed among societies in strength and direction. As years of schooling is a major determinant of socioeconomic status and dyslipidaemia a major CHD determinant, the purpose of this investigation is to estimate the association of years of schooling with plasma lipids and lipoproteins among samples from five countries representing different cultures, socio-political systems and stages of economic development.
Methods Men and women from Chinese, Polish, Russian, Israeli and US samples were studied. Years of schooling were analysed both as a multi-category ordinal variable and divided into two strata: less than the equivalent of high school and greater than or equal to high school equivalence. Fasting plasma cholesterol, low density lipoprotein (LDL) cholesterol, high density lipoprotein (HDL) cholesterol and triglycerides were compared across years of schooling strata within each country. Lipid levels were computed unadjusted and then adjusted for age and lipid risk factor variables.
Results Total cholesterol, LDL cholesterol, and triglycerides varied directly with years of schooling in Chinese, Polish and Russian men, and in contrast varied inversely with years of schooling among US white men. The HDL cholesterol varied inversely with years of schooling for Chinese, Polish, and Russian men, but varied directly with years of schooling among US white men. The lipid differences between men of high versus low years of schooling were not explained by age, body mass index, smoking, alcohol consumption or blood pressure medication use. Findings were less consistent for women and for Israelis and US blacks of both genders.
Conclusions Lipid and lipoprotein levels consistent with atherogenicity varied directly with years of schooling in Chinese, Polish, and Russian samples. Opposite trends were present in US whites. These findings are consistent with a hypothesized influence of social status on CHD risk differing among populations in relation to stages in societal economic development.
Keywords Lipids, years of schooling, China, US, Israel, Poland, Russia
Accepted 15 November 2000
The association of socioeconomic status (SES) with coronary heart disease (CHD) has varied over time among populations in different phases of the epidemic of the disease. Coronary heart disease mortality was positively associated with SES during the rise of the epidemic in the UK and the US and subsequently has become inversely associated with SES during the decline.1 Marmot advanced the explanatory hypothesis that the direction of association of CHD with SES is related to the stages in the economic development of societies.2 A postulated mechanism is that during the ascending limb of the CHD epidemic in industrialized societies in the earlier stages of modernization and economic development, the risk factors of an atherogenic diet, sedentariness, and smoking are aggregated in the more socially advantaged affluent and influential members of society; with established economic development and knowledge regarding the aetiology and prevention of CHD, health promotive behaviours are preferentially adopted by those socially advantaged resulting in a aggregation of risk factors and the disease itself in the more socially disadvantaged members of society. Davey Smith, in a review and critique of CHD certification for mortality data of England and Wales, concluded that: this notion of a generational social class cross-over in coronary heart disease risk is not supported by these data.3 Further, in a systematic overview of studies of CHD incidence and prevalence of CHD in the UK and US until 1960, he concluded there is not evidence of a positive association between social position and CHD, except for the Evans Co. Study,4 which analysed CHD social patterns in a rural, bi-racial US community. Given this conceptual framework and the conflicting evidence, the present study was addressed to the direction and magnitude of the association of serum lipids with SES, indexed by years of schooling, among individuals sampled from five industrialized or industrializing nations, but of different cultures, socio-political systems and at different stages of economic development.
The specific goals of this study were to identify, quantify and compare the association, if any, of the levels of the major atherogenic plasma lipids and lipoproteins with years of schooling in men and women age 4554 years in population-based samples from China, Poland, Russia, Israel, and the US. The populations studied exhibit a wide range of CHD levels and plasma lipid and lipoprotein profiles, extending from very low atherogenicity in China to high atherogenicity in US whites. The social environments also varied markedly, extending from those of the Orient to the Middle East, Eastern Europe and North America. The politico-economic organization of the societies range from market economies to state socialism. The a priori hypothesis was that the association of SES with atherogenic plasma lipids and lipoproteins would be negative in contemporary US populations and positive in the other populations sampled.
Methods
The participants for this study were sampled between 1972 and 1989 from communities in China (four population samples), Poland (two populations), Russia (two populations), Israel (one population), and the US (13 populations). Analyses were restricted to men and women ages 4554 years fasting at least12 hours. Exclusions included pregnant women, participants known to be taking lipid lowering medication or those missing lipid and lipoprotein values. The dates of the studies and identification and sample sizes of subpopulations within countries are set out in Table 1. Study designs, populations studied, methods used, and standardization procedures have been described in detail elsewhere.517 Brief descriptions follow.
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Since different laboratories were used in the studies, comparison of lipid levels between strata based on years of schooling was performed within each sampled population. For descriptive purposes, age-adjusted differences between levels of years of schooling were computed using least squares means from mixed linear models for each country separately. Mixed linear models were used to estimate the association between years of schooling strata and the lipids and lipoproteins for all populations combined adjusted for age alone and subsequently adjusted for four potentially explanatory covariablesbody mass index (BMI), alcohol intake (g/day), smoking, and antihypertensive medication use. In these models, the sampled population (country) was considered a random effect and all other variables (e.g. age, BMI) were considered fixed effects. All covariables were used as continuous variables except smoking which was current smoker versus never or ex-smoker.
Data on age, smoking, and alcohol consumption were obtained using a standard questionnaire. Smoking was categorized into current smokers and non-smokers. Alcohol consumption was evaluated on a 7-day recall. Weight was measured on a beam balanced scale while the participant stood without shoes and heavy outer garments. Height was measured in the standing position and BMI was computed as weight (kg) divided by height (m) squared. Data collected for years of schooling were specific to each country ranging from five categories (in China and Poland) to seven (in US-LRC). High and low achievement in years of schooling was constructed for each country. Low attainment represented years of schooling judged to be less than or equivalent to high school graduation in the US and the high achievement stratum represented years of schooling greater than high school graduation in the US.
Lipid laboratories in each country were standardized according to the Centers for Disease Control programme. Plasma lipid determinations were made in all of the samples except those from China where serum was used. Serum samples were adjusted to be equivalent to plasma samples using a standard formula.18 In Poland and the LRC studies (US, Russia, and Israel), high density lipoprotein (HDL) cholesterol was evaluated in the supernatant after precipitation of other cholesterol fractions with heparin and manganese (Mn2+).19 In the ARIC Study and China, HDL cholesterol was measured using a mixture of dextran sulphate, an analogue of heparin, and magnesium (MG2+).20 Low density lipoprotein (LDL) cholesterol was estimated using the Friedewald21 formula.
Age-adjusted mean lipid levels by years of schooling strata were determined by gender for each country's sample. The relation of lipid and lipoprotein levels to polytomous schooling strata was determined by visual inspection and by regression analysis, after coding the ordinally ranked strata by years of schooling by ascending integers. After demonstrating differences in the relation of the ordinally ranked polytomous years of schooling strata to lipids and lipoproteins among country samples, mixed effects analysis of combined US-LRC and ARIC white samples, called Group 2 populations, and the aggregate of all other samples, called Group 1 populations, was performed. In these models, years of schooling strata were aggregated into one judged equivalent to US high school graduation or greater and one stratum of less that US high school graduation. In the modelling, a random country variable was included. Age-adjusted mean and standard error of the years of schooling strata differences in lipid levels were determined for men and women, for models with and without additional candidate explanatory covariables.
Results
The number of participants, ages 4554 years, ranged from a low of 253 men in the Israeli population to a high of 3975 white men in the Russian sample, with a total of 17 602 people, 9856 men and 7746 women (Table 1). The distribution of participants by years of schooling strata and gender within countries is displayed in Table 2
. Different classifications of years of schooling and landmarks of achievement were employed across studies precluding direct comparisons. However, the strata were ordinally arrayed within each study, and regression analyses were carried out for each. The sign and magnitude of the regression coefficient, indicating the direction and magnitude of association of lipid levels with years of schooling, and its CI is displayed for men and women in Table 3
. Given the differences in classification of years of schooling and possible differences in lipid determinants among country samples, comparisons of the magnitude of the coefficients across countries are not relevant: however, the signs indicate qualitative differences in direction of associations in US whites compared with all other samples studied. In US white sampled populations, both in the ARIC and LRC studies, for both men and women, total cholesterol decreased with increasing years of schooling (although not all the regression coefficients were statistically significant). In contrast, for populations sampled in China, Poland, Russia, Israel and US ARIC blacks, total cholesterol increased with increasing years of schooling (although not all the regression coefficients were significant). For the other lipids in the US white populations, LDL cholesterol and triglycerides decreased and HDL cholesterol increased with increasing years of schooling with opposite direction of associations for men and women (except HDL cholesterol) in the population samples from China, Poland and Russia. The unadjusted means and standard deviations of each lipid are displayed in Table 4
by sample and gender. For both genders, China has the lowest total and LDL cholesterol and Russia the highest. The age-adjusted differences in mean levels of plasma lipids and lipoproteins of men and women with schooling equal to or greater than the equivalence of high school compared with levels among individuals with less than high school (levels in higher years of schooling minus levels in lower years of schooling) and their 95% CI are presented in Figure 1
for each country separately and for the aggregate of whites in the LRC and ARIC samples (Group 2 populations), and for the aggregate of all other samples (Group 1 populations), derived from mixed model analyses including a random country term variable. Among men, each of the lipids differed significantly by years of schooling strata and the direction of the association of lipids with years of schooling was significantly different in the two population groups: Total plasma cholesterol, LDL cholesterol, and triglycerides were significantly higher, and HDL cholesterol significantly lower, in the men with more years of schooling in Group 1 populations. By contrast in Group 2 populations, total plasma cholesterol, LDL cholesterol and triglycerides were lower, and HDL cholesterol higher in the men with more years of schooling. The patterns were somewhat different for women than men. Women with more years of schooling in Group 1 populations had higher total cholesterol, LDL cholesterol and triglycerides than women with fewer years of schooling. However, in contrast to men, HDL cholesterol was also higher in women with more years of schooling. For women in Group 2 populations, triglycerides were significantly lower and HDL cholesterol significantly higher in those with greater years of schooling, however, neither total nor LDL differed significantly by educational level. Overall comparisons of population groups indicated that the difference between lipid levels of individuals with the equivalent of high school graduation compared to those with less years of schooling was significantly different between Group 1 and 2 populations for each lipid and for both men and women.
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The point estimates and 95% CI for the data graphed in Figure 1 are presented in Table 4
with the addition of the results of models adjusting for BMI, smoking status, alcohol consumption, blood pressure medication use and hormone use in women. There was little difference in the findings in the two analyses, and the random effect country variable was not significant in either model or gender for any lipids.
Discussion
This multi-country study of the association of plasma lipid levels with years of schooling compares the findings among an array of populations of differing cultures and ethnicity residing in communities with marked differences in social, political, and economic organization. Despite this diversity, there was an association of lipid levels with years of schooling within each of these populations. Years of schooling as a marker or indicator of social status taps access to power, prestige, and control of resources. It relates to knowledge and the ability to translate that knowledge to health behaviour relevant to lipid levels. The observed association of years of schooling with lipid levels was not unexpected and is consistent with reports from numerous countries including England,22 Scotland,23 Ireland,24 East and West Germany,25 Sweden,26 Finland,27 Australia,28 Norway,29 and many ethnic subgroups of US populations, including African Americans;30,31 in addition to the findings reported herein from populations in China, Israel, Poland, Russia, and the US.
The pervasiveness of the effect of SES on CHD risk factors including plasma lipid levels, while compelling, does not, however, indicate that the nature of the effect, its direction and its magnitude all are invariant over time or across divergent populations. In our study, total plasma cholesterol and LDL cholesterol, the major atherogenic components of the lipid profile, were consistently higher among those with greater years of schooling in populations sampled from China, Israel, Poland, Russia, and African Americans in the US; however, the converse was true, i.e. total plasma cholesterol and LDL cholesterol levels were lower among those with more years of schooling in surveys performed among whites in the ARIC and LRC surveys in the US. The differences in these atherogenic lipid profiles were not explained in this study by analysis of the potential effects of age, BMI, smoking, alcohol consumption, antihypertensive medication use nor hormone use. Other putative determinants such as dietary and physical activity differences between the social strata were not uniformly available for study across all participating country cohorts. Additionally, it is important to note the existence not only of patterns and levels of risk factors, per se, but also of possible differences in their risk functions for heart disease among different populations and social groups. For example, HDL cholesterol was not observed to be CHD protective and levels of total plasma cholesterol exhibited a J-shaped relation to the incidence of heart disease among Russian men with lower years of schooling in the LRC Prevalence follow-up study.8
Empirical evidence indicating that the association of SES with CHD has changed between the rise and the fall of the CHD epidemic and in industrialized countries has depended principally upon mortality data. However, the validity of the CHD mortality-SES association has been challenged and the findings of only one cohort morbidity study, and that in a rural community, have been consistent with the hypothesis.3 The studies reported herein indicate variation, not in the presence or absence of an association, but in the direction of the association of SES, as indexed by years of schooling, with the atherogenic profile of lipids and lipoproteins among populations sampled from countries differing in socio-political systems and stages of economic development. For men, more consistently than women, atherogenic lipid and lipoprotein profiles were inversely associated with SES in population samples from China, Poland and Russia. Determination of the possibly differential influence of social status on CHD among populations in relation to stages in their societal economic development requires morbidity and mortality studies. However, one major CHD risk factor, the atherogenicity of the lipid-lipoprotein profile, has been found in this study to vary in a manner consistent with the hypothesis.
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Supported by the National Heart, Lung, and Blood Institute, Bethesda, MD, through the Office of International Programs and under contract N0-1HV12243, N01-HV08112 and N0-1HV59224 with the University of North Carolina at Chapel Hill. For their important contributions the authors would like to thank the following staff from Beijing, China: Beifan Zhou, Ying Li, Yen Zhu, Xiuzhen Tian; from Cracow, Poland: Witold Rostworowski, Ewa Baczynska, Ewa Kawalec, Dorota Kurek, Witoslawa Misiowiec; from Warsaw, Poland: Stefan Rywik, Ewa Chodkowska, Maria Polakowski, Henryka Wagrowska, Aleksandra Pytlak, Pawel Kurjata; from US-ARIC: the staff and participants in the ARIC study; and from the Collaborative Studies Coordinating Center: Lilin She and Ratna Thomas for programming and Colleen O'Briant for graphics and editorial assistance.
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