Association Between Socioeconomic Status and Prevalence of Cardio-Metabolic Risk Factors: A Cross-Sectional Study on Residents in North China

Studies have found associations between cardio-metabolic disorders and socioeconomic status (SES) in developed areas. However, little epidemiological data are available on residents of less developed areas in North China. A cross-sectional study that consisted of 2,650 adults randomly selected from local residents was conducted on a developing province, Hebei. SES was assessed in terms of education, personal income per year, and occupation. The association between SES and metabolic syndrome (MetS) was determined by multivariate logistic regression. The weighted prevalence of MetS was 26.8% among residents of Hebei province. The lower prevalence of MetS and abdominal obesity was associated with increase in SES groups. After adjustments regarding age, sex, body mass index, living area, smoking, salt intake, and family history of diabetes, odds ratio (OR) for elevated blood pressure (BP) of individuals with higher SES level was 0.71 [95% confidence interval (CI): 0.542–0.921] compared with those with lower SES level. Cardio-metabolic risk factors were commonly identified among residents of Hebei province in north China and were associated with SES conditions. This study indicated that from a public health perspective, more attention should be paid to screening of cardio-metabolic disorders in less developed areas.


INTRODUCTION
Cardiovascular and metabolic diseases are leading causes of death and pose a great threat to public health, especially in developing countries (1)(2)(3). Metabolic syndrome (MetS) is a set of physiological and biochemical disorders that are characterized by pathological components such as abdominal obesity, impaired glucose metabolism, and increased blood pressure. It has been known that the occurrence of MetS is associated with increased risks of developing cardio-metabolic diseases such as diabetes, hypertension, coronary heart disease, and stroke (4). The prevalence of cardiometabolic disorders is on the rise among Chinese populations and has already become the primary cause of death among Chinese residents (5).
Metabolic syndrome and its components are closely associated with increased risks of cardio-metabolic disorders (6,7). Other cardio-metabolic risk factors include gender, lifestyle, family history of disease, and socioeconomic status (SES) (8). SES reflects a person's position in society and mainly includes education, income, and occupation. Previous studies have demonstrated that lower SES was associated with higher risk of cardio-metabolic disorders in developed countries (9,10). China has experienced great social and economic transitions in the last decades. These transitions accompany lifestyle changes such as abundance in high-calorie foods and decrease in physical work, and have led to sharp increase in cardio-metabolic diseases (11). Several studies have investigated the association between SES and prevalence of cardio-metabolic risk factors in China. However, most of these studies were carried out on developed areas (12,13), and only few have been reported on populations in less developed areas. Hebei is a developing province located in the North China Plain and surrounded by the capital Beijing. This is the first time the association between SES and prevalence of cardio-metabolic risk factors among residents of Hebei province has been investigated.

Study Population
This epidemiological study was implemented in September 2016 and conducted in Hebei province. Sample selection was conducted based on a multistage, stratified sampling method. First, cities of Shijiazhuang and Renqiu were selected as representative urban and rural areas of Hebei province based on gross domestic product per capita. Second, one district was randomly selected from each city. Next, several residential communities were randomly selected from each district, and eligible individuals who met the inclusion criteria were included. The composition of age and sex of each community and urbanrural ratio are designed based on latest national census data (14) and are presented in Supplementary Table 1.
The inclusion criteria were as follows: age 18 years or older, has lived in the selected community for at least 5 years, and not pregnant. A total of 2,650 adults were randomly selected from local residents. Our study eventually included 2,638 participants after excluding 12 people with missing information on sex, age, plasma glucose, or SES questionnaire. This study was approved by the Medical Ethics Committee of The Second Hospital of Hebei Medical University, and all methods were performed in accordance with relevant guidelines and regulations. All participants provided written informed consent following a thorough explanation of research procedures. A flow diagram of the analytical sample is presented in Supplementary Figure 1.

Clinical and Laboratory Measurements
A standardized questionnaire was administered by trained professionals to collect in regional locations. Body weight, height, waist circumference, and BP were measured by trained nurses according to standard protocols. Body mass index (BMI) was calculated as weight (kg)/height (m 2 ) and was classified into three categories: normal (<24 kg/m 2 ), overweight (≥24 and <28 kg/m 2 ), and obese (≥28 kg/m 2 ) according to the criteria (15). Waist circumference (WC) was measured midway between the lower border of the rib margin and the iliac crest at the end of normal expiration. Salt intake was classified into three categories: mild (<5 g/day), moderate (5-10 g/day), and severe (>10 g/day). Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were measured with an electronic blood pressure monitor (Omron HEM-7430; Omron Corporation, Kyoto, Japan) on the non-dominant arm twice according to standard protocols.
After 12 h of overnight fasting, a blood sample was drawn from each participant, and fasting blood glucose (FBG), total cholesterol (TC), triglycerides (TGs), high-density lipoprotein cholesterol (HDL-C), and low-density lipoprotein cholesterol (LDL-C) were measured using an automatic biochemical analyzer (Mindray BS-180 Analyzer) according to standard protocols.

Cardio-Metabolic Risk Factors
The participants were diagnosed with MetS if they had at least three of the following criteria according to Chinese
The composite score was calculated for every participant in SES dimension. The lowest composite score is 3 points and the highest is 15 points. The distribution of SES scores was spilt into tertiles where T1 was the reference group and T3 was the best.

Statistical Analysis
To account for the complex sampling design of this study, we used the SUDAAN software (Research Triangle Institute, North Carolina, United States) to obtain estimates of prevalence and standard errors according to the Taylor linearization method. Estimates were weighted to reflect age, sex, and urban-rural distribution of adults living in Hebei province. Weighting coefficients were derived from the 2010 Chinese population census data, and the sampling scheme of our survey was designed to obtain a representative estimate. Categorical  Compared with those with no MetS, participants with MetS reported significantly higher levels of age, BMI, and WC, and higher values of SBP, DBP, FBG, TG, TC, and LDL-C, and lower values of HDL-C (all p < 0.01). Meanwhile, we found no significant differences in terms of location and family history of diabetes in the MetS and non-MetS groups (p > 0.05).

Weighted Prevalence of MetS and Its Components Across Groups of SES
The most common cardio-metabolic risk factors were elevated BP (46.2%), abdominal obesity (42.9%), elevated TG (31.2%), elevated BG (23.4%), and low HDL-C (14.9%). As shown in Table 2, the weighted prevalence of MetS (26.8%) and its components were different under three SES conditions. In general, a negative linear association was found between prevalence of MetS and abdominal obesity with increase in SES groups.

Adjusted ORs for MetS and Its Components Among Different Risk Factors
Multivariate logistic regression analysis suggested that the associations between SES levels and MetS were not statistically significant. Participants with higher SES condition (T3) had a significantly lower risk of having elevated BP (OR:0.71, 95% CI:0.54-0.92) than those with lower SES (T1). The analysis also suggested that age was an important risk factor for MetS and its components, with ORs appearing an increasing trend with increase in age, except for elevated TG and low HDL-   increased significantly in participants from overweight to obesity. Participants living in rural areas had a lower risk of developing elevated BG and elevated TG but have an increased risk of abdominal obesity, elevated BP, and low HDL-C compared with people living in urban areas. Our data also suggested that heavy salt intake, smoking, and diabetes history were associated with the prevalence of cardio-metabolic parameters. Adjusted ORs for MetS and its components between SES in males and females are presented in Table 4. It is observed that females with higher SES had significantly lower ORs in  developing elevated BP (OR:0.65, 95% CI:0.43-0.97). Adjusted ORs for MetS and its components between SES in urban or rural areas are presented in Table 5. The data showed that people with higher SES had a high risk of developing elevated BG (OR: 1.67, 95% CI: 1.08-2.59) in urban areas and low risk of having an elevated BP (OR:0.56, 95% CI:0.38-0.84) in rural areas. Unadjusted and age-sex-adjusted odds ratios for MetS and its components among risk factors by sensitivity analysis are presented in Supplementary Tables 2, 3.

DISCUSSION
Metabolic syndrome (MetS) has become a major threat to public health worldwide (16). If left untreated, patients with MetS are disposed to a series of chronic diseases such as diabetes, cardiovascular disease, and cognitive dysfunction, and have increased all-cause and cardiovascular death (17,18 (20), and Chinese Diabetes Society (CDS-2004) (21) are three frequently used guidelines in clinical practice and published articles. However, the diagnostic results are largely affected by which one of these three guidelines are applied in the analysis (22). Given that the Chinese have experienced rapid socioeconomic transitions during these years, adopting the latest CDS criteria (CDS-2017) might increase the accuracy of describing the prevalence of MetS in Chinese adults (15).
The prevalence of MetS has been increasing in recent years (16), especially in China, which faced great social and economic transitions in the last decade. Identifying populations at risk would contribute to more effective screening and prevention. Generally, the prevalence of MetS varies in different regions in China. It was reported that the adjusted prevalence of MetS across China was 11% in 2010 by 2004 CDS criteria (23). The prevalence of MetS was 16.7% in adult Hong Kong Chinese in 2005 by NCEP ATP III (24). In highly urbanized Beijing, MetS prevalence was 14.05% for males and 28.55% for females according to NCEP ATP III in 2007 (25). In our study, the weighted prevalence of MetS was 26.8% in Hebei, and 18.4% for females and 35.4% for males. Possible origins may be attributed to inequality in education, income, and occupation, and their associations with health between developed and developing areas in China, which has been discussed in many bodies of literature (26,27).
A composite SES score was then calculated to better understand the overall condition of SES (28). Patients with lower SES condition had increased prevalence of developing cardio-metabolic disorders, such as MetS and abdominal obesity ( Table 2). Our results were consistent with earlier studies, which demonstrated that better SES is associated with lower rates of specific diseases such as coronary disease, diabetes, cognitive impairment, stroke, cancer, and arthritis (29,30). Higher SES is generally associated with better education, income, medical services and other social benefits that provide positive effects on health (31). However, economic stress and social vulnerability are risk factors for various chronic disorders, particularly cardiovascular diseases (17). People with lower SES are generally more stressed, which often leads to restricted opportunities for good health services (32).
Differences in prevalence of MetS between males (35.4%) and females (18.4%) were significant (p < 0.01). Consistent with a previous study, our data suggested that females were less likely to develop MetS and other related cardio-metabolic risk parameters ( Table 3) (33). After multivariate adjustments, the ORs for MetS increased with higher SES levels in males. As for females, inverse associations were shown between SES and MetS. Lower SES was associated with higher risk of MetS among females ( Table 4). However, the associations between them were not statistically significant, which might be attributed to lack of sufficient sample size. This was consistent with other findings in Korea (34) and China (25). Another possible explanation may contribute to the gender differences. Males with better SES may spend more time sitting in the office, have little time to exercise, frequently consume high-fat foods, and suffer from work-related mental health problems (35).
The analysis was then stratified by living area ( Table 5). The ORs for elevated BG increased with higher SES levels in urban areas and for elevated BP decreased with higher SES levels in rural areas. The possible mechanism for different regional impacts of SES on MetS in urbanization may through unhealthy behaviors, such as decreased physical activity, excessive intake of animal fats and salts, and low intake of fruits and vegetables in urban areas (36).
Moreover, a relationship was observed between prevalence of MetS and age in both males and females, which is similar to other studies (37,38). The increased prevalence of MetS with age can be attributed to similar age-related trends in all components of MetS (39,40). The most common cardio-metabolic risk factors in Hebei province we identified in this study were elevated BP (45.6%) and abdominal obesity (42.9%). These data raised a red flag to public health that urgent measures need to be taken to prevent elevated BP-related and obesity-related cardiometabolic disorders in high-risk populations of Hebei province. Additionally, smoking and family history of diabetes were also independent risk factors for MetS and its components, as seen in previous studies (41).
Previous studies have shown that the link between SES and MetS was significant and positive (28). However, our results found that the association between them was not statistically significant ( Table 3), which was consistent with other studies (42, 43). Several explanations are possible. First, despite several diagnostic criteria of MetS such as ATP III criteria, IDF criteria, and CDS criteria, worldwide-accepted criteria do not exist. The CDS-2017 criteria were used in our study for better applicability in Chinese populations. Second, there is no unique definition for SES. It can be social, economic, or psychosocial. An analysis per type of status could show different links with MetS in terms of significance, sign, and magnitude. Third, our study focused mainly on age, sex, and living area. Other behavioral risk factors such as alcohol use, dietary quality, and physical activity were not discussed. Fourth, the null association between SES and MetS may be due to sample size issues. Our study only included data from a region in north China. The conclusion of this study should be further examined in prospective studies in the future.
In summary, the prevalence of MetS and cardio-metabolic risk factors is partially conditioned by individual SES status, which should be taken into account by healthcare professionals when making preventive strategies to reduce health inequality in society. Overall, our results supported the idea that there was a definite association between SES and prevalence of cardiometabolic risk factors in a developing area in China.

CONCLUSION
This was the first cross-sectional study to examine the associations between SES and MetS, as well as its cardiometabolic components, in north China, Hebei province. Our data suggested that better SES conditions were associated with lower prevalence of MetS and abdominal obesity. Lower SES condition, male gender, older age, obesity, smoking, and family history of diabetes were associated with higher risk of developing cardio-metabolic disorders. This should be the target group for possible early lifestyle intervention to reduce the occurrence of cardio-metabolic disorders in less developed areas in China.

DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

ETHICS STATEMENT
The studies involving human participants were reviewed and approved by Medical Ethics Committee of The Second Hospital of Hebei Medical University. The patients/participants provided their written informed consent to participate in this study.