Sex Differences in The Association Between Socioeconomic Status and Metabolic Syndrome in Rural China: An Updated Cross-Sectional Study

Background: The aim of this study was to evaluate the prevalence of metabolic syndrome (MS) and MS components as well as their association with socioeconomic status among rural Chinese adults. Methods: A cross-sectional study of 26836 participants aged 20 years and older was conducted from June to December 2012 in Yuhuan City, Zhejiang Province, China, which is located on Yuhuan Island. A multivariable logistic regression model was used to identify risk factors for MS and their possible interactions. Results: Among 26836 subjects with an average age of 53.4±14.0 years, 59% were female. The overall prevalence of MS was 20.5%, and there was a signicant sex difference in the prevalence (15.1% for males vs. 24.2% for females, p<0.001). Compared with males, females also showed a signicantly higher proportion of most MS components. A signicantly higher prevalence of MS was found among subjects who were elderly, had a lower income level, had a lower level of education, or were unemployed. Multiple signicant interactions were observed between the prevalence of MS and sex, age or socioeconomic status (p<0.001). The risk of MS increased signicantly with age in females but not in males. Additionally, a lower income level and a lower level of education were signicantly related to an increased risk only in females, and unemployed males had a higher risk of MS than unemployed females. Conclusions: The prevalence of MS and its components was relatively high in a rural island Chinese population with rapid urbanization, and sex-specic associations between socioeconomic factors and MS were found. Targeted preventive interventions should be developed and implemented to prevent and control MS among those with a low socioeconomic status, especially females.

Recent studies have shown that socioeconomic status (SES) is a strong predictor of morbidity and premature mortality both in developing and developed countries [19,20]. Prior studies reported that lower SES was associated with a higher risk for NCDs such as type 2 diabetes and coronary heart disease, and the severity varied by sex [21,22]. With the changing socioeconomic environment, few studies have examined the association between SES and MS in rural East China. This study aimed to estimate the prevalence of and risk factors for MS and the association between SES and MS in different sexes in a rural area with rapid urbanization in East China.

Study site and population
A cross-sectional study was conducted in 3 communities in Yuhuan City, Zhejiang Province, from June to December 2012 using cluster sampling. A total of 26836 participants were included in this research, and the inclusion criteria were as follows: 1) 20 years and older; 2) local permanent resident without migration or travel plans (1 year or longer); 3) provided informed consent; and 4) able to complete the questionnaire and physical examination.

Data collection and quality control
Face-to-face questionnaire interviews were conducted and anthropometric data were collected by trained local health professionals. The following demographic data were collected: age; sex; lifestyle information, including smoking history (non-smoker/former smoker/current smoker), alcohol consumption (Yes/No), and regular physical exercise (Yes/No); socioeconomic status, including years of education (<9 years/≥9 years), monthly household income (<2000 RMB/≥2000 RMB), and occupation status (Manual worker/Mental worker/Unemployed/Other); and health conditions, including disease history of hypertension, diabetes mellitus, stroke, cardiovascular disease or other [23]. Anthropometry data included height, weight, waist and hip circumference, and blood pressure.

De nition of metabolic syndrome
The diagnosis of metabolic syndrome was based on IDF criteria as follows: Central obesity (de ned as waist circumference ≥90 cm for males or ≥80 cm for females, or BMI >30 kg/m 2 ) plus any two or more of four additional factors: (1) triglyceride levels ≥1.7 mmol/L (150 mg/dL); (2) high blood pressure: systolic blood pressure ≥130 mmHg or diastolic blood pressure ≥85 mmHg or treatment of previously diagnosed hypertension; (3) high-density lipoprotein cholesterol levels <1.03 mmol/L (40 mg/dL) in males and 1.29 mmol/L (50 mg/dL) in females or speci c treatment for lipid abnormalities; (4) fasting plasma glucose levels ≥5.6 mmol/L (100 mg/dL) or previously diagnosed type 2 diabetes[24].

Statistical analysis
All data were entered into Epidata 3.1 twice. Pearson's chi-square test or Fisher's exact test was applied for categorical variables. Student's t-test or the Wilcoxon test was used for two-group comparisons of normally distributed and nonnormally distributed continuous variables, respectively. Logistic regression analysis was used to calculate crude odds ratios (cORs), adjusted ORs (aORs) and 95% con dential intervals (CIs) to estimate the potential risk factors as well as to explore the possible interactions between sex and socioeconomic factors. All analyses were conducted using SPSS 22.0, and a two-sided p-value of 0.05 or less was de ned as signi cant, missing data were deleted.

Results
Basic characteristics of subjects (Table 1) Data from 26836 individuals were analysed, including 59% females with an average age of 53.4±14.0 years. Compared with male subjects, females were more likely to have lower levels of education, lower monthly household income levels, and unemployment. Males showed signi cantly higher proportions of smoking and alcohol consumption. Additionally, MS components, including hypertension, high FPG levels and high TG levels, were more common in males than in females, except for low level of HDL-C. In addition, BMI and waist circumference were signi cantly higher in males than in females.

Prevalence of MS and its in uencing factors (Tables 2&3)
The overall prevalence of MS was 20.1%, and there was a signi cant sex difference in the prevalence between males and females (15.0% vs. 24.2%, p<0.001). Additionally, participants who were elderly, were unemployed, had a lower monthly household income or had a lower level of education had a signi cantly higher prevalence of MS; after adjusting for covariates, there were signi cant interactions between sex and SES (p<0.001). Males who were mental workers and unemployed participants had a higher risk of MS, and females with a lower monthly household income, lower education level and unemployment had a higher risk of MS.
Sex-speci c prevalence of MS components (Table 4 & Figure 1) The prevalence of MS components (except HDL-C) among females increased with age, but only the prevalence of hypertension among males increased with age. It was revealed that females had higher prevalences of most MS components, especially HDL-C, than males in all age groups, whereas there were higher proportions of triglyceride levels, high blood pressure and FPG levels among males under the age of 70, as shown in Figure 1. As presented in Table 4, females had a higher risk of HDL-C and central obesity components, while males had higher triglyceride levels, higher blood pressure, and higher FPG levels after adjusting for demographic and other MS components.

Discussion
In this study, we found a high prevalence of MS of 20.1% among 26836 participants in Yuhuan County, a coastal area located in developed East China, which was similar to previous studies ranging from 22.0-25.3%, and a higher prevalence for females was observed, which was consistent with previous studies [14,25,26]. Compared with the Northwest or other developing areas in China, MS was more prevalent in East China [27,28]. The prevalence of MS increased with age in females, while in males, it rst increased and then decreased, which was similar to the ndings of other studies [29]. Furthermore, the prevalence in females was higher than that in males among individuals over the age of 50 years old and among those over the age of 60 years old, which may be associated with menopausal oestrogen de ciency [30,31]. Another explanation was that the sex hormones affecting skeletal muscle mass were decreased in elderly and female subjects, which resulted in lower muscle mass and a higher risk of NCDs [32,33]. Such an increase for women may also result from similar age-related trends in all MS components in Fig. 1 except Another nding from this study was that signi cant interactions between sex and SES were observed among individuals with MS. In this study, females with a lower SES (especially lower income and lower education level) showed a higher risk for MS, which was consistent with prior studies [36][37][38][39]. This nding could be explained by the following potential reasons. First, participants with a lower SES were more likely to be exposed to unhealthy behaviours, psychological distress, lower life expectancy, lower access to health care, lower awareness of disease prevention and control, and a series of NCDs, such as obesity, hypertension, and diabetes mellites, which are commonly associated with MS [20,[36][37][38].
Compared with females, lower income was shown to be a protective factor for MS among males; this discrepancy may be due to males being more likely to have a manual occupation, which reduced their risk for MS [39,40]. Nam's study reported that o ce workers had a higher risk of MS than manual workers, which was consistent with the present study [41].

Limitations And Strengths
This study was carried out in the rural Chinese community population with rapid urbanization, and the ndings should be helpful to understand the status of MS in other similar areas of China or other countries. Of course, some limitations should be discussed. First, this study population was from the developed area in China, where the socioeconomic and lifestyle factors may be different than those in other rural areas in China. Second, anthropometric and demographic information were collected at a single point, which may lead to data inaccuracy, and it was less feasible for the present study to only use IDF criteria as a de nition without using other new de nitions. Third, as a cross-sectional study, it is not possible to draw causal conclusions. More well-designed studies should be conducted to con rm our ndings, especially regarding sex differences.

Conclusion
Our study indicated the different distribution of MS prevalence and MS components in males and females as well as sex differences in the association between in SES and MS. This study also updated the prevalence data in the Yuhuan rural area in Zhejiang Province in China. Risk factors for MS were identi ed to provide a reference for the prevention and management of this disease. More interventions and policies regarding the risk factors for MS need to be applied for people with lower SES, especially in females, to increase access to health care and to reduce health inequalities.

Availability of data and materials
The datasets generated and/or analysed during the current study are not publicly available owing to local legislation and the written consent forms of participants but are available from the corresponding author on reasonable request.

Competing interests
The authors have no conflicts of interest to declare.

Funding
This work was supported by the National Natural Science Foundation of China (grant number 81473038) and Taizhou City Science Program (grant number 1401KY49). The sponsors had no role in the study design, survey process, data analysis or manuscript preparation.

Authors' Contributions
XHY and SYY analysed the data, interpreted the analysis results and drafted the manuscript. YC, QJ and CF designed the study and revised the manuscript. XHY, STL, MFS and NW analysed the data and collected the data. MFS, STL and XHY collected data and supervised the study. All authors read and approved the nal manuscript.