A rural-urban comparison of the characteristics of the metabolic syndrome by gender in Korea: The Korean Health and Genome Study (KHGS)

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1 J. Endocrinol. Invest. 29:??-??, 2006 A rural-urban comparison of the characteristics of the metabolic syndrome by gender in Korea: The Korean Health and Genome Study (KHGS) S. Lim 1, H.C. Jang 1, H.K. Lee 1, K.C. Kimm 2, C. Park 2, and N.H. Cho 3 1 Department of Internal Medicine, Seoul National University College of Medicine; 2 Korean National Genome Institute, Korean National Institute of Health, Seoul; 3 Department of Preventive Medicine, Ajou University School of Medicine, Suwon, Korea ABSTRACT. The number of cases of the metabolic syndrome is increasing dramatically in Western countries. However, the evaluation of the metabolic syndrome is limited in Asian countries. Thus, our objectives were: 1) to investigate parameters of the metabolic syndrome defined by the National Cholesterol Education Program (NCEP)-Adult Treatment Panel III (ATPIII) in the subjects representing Korean general population and 2) the modification of which factor is most effective in reducing the metabolic syndrome. A total of 10,044 (5024 rural and 5020 urban) Korean men and women in the age range yr voluntarily participated in this community-based cross-sectional study (a rural and an urban community was selected). Anthropometric parameters (weight, height, waist and hip circumference and blood pressure), social factors (smoking, alcohol, exercise and education status) as well as biochemical parameters (fasting glucose and insulin, lipids and body composition) were measured. Twenty-six point one per cent of the total subjects were classified as having the metabolic syndrome. Age- and sex-adjusted prevalences were 29.3 and 22.3% in the rural and urban community, respectively (p<0.01). Abdominal obesity (46.9%) and high blood pressure (45.2%) were major components in the rural community; hypertriglyceridemia (37.6%) and low HDL-cholesterolemia (37.0%) in the urban community. In conclusion, abdominal obesity in the rural community and dyslipidemia in the urban community should be a main subject of intervention, aimed at reducing the prevalence of the metabolic syndrome in Korea. Given the rapid progression of the Korean economy over the past 30 yr, the prevalence of the metabolic syndrome is expected to increase continuously. A strategy to prevent this expected extraordinary event should be conducted at a national level. (J. Endocrinol. Invest. 29:??-??, 2006) 2006, Editrice Kurtis INTRODUCTION The metabolic syndrome has also been called syndrome X or insulin resistance syndrome. Abdominal obesity, diabetes, glucose intolerance, dyslipidemia, high blood pressure and hyperuricemia are its main components (1). The metabolic syndrome has been shown to be associated with cardiovascular morbidity and mortality (2, 3). In a prospective study, the clustering of factors related to the metabolic syndrome was found Key-words: Metabolic syndrome, prevalence, urban, rural, Korean. Correspondence: N.H. Cho, MD, PHD, Preventive Medicine, Ajou University School of Medicine, San 5, Wonchon-dong, Paldal-gu, Suwon, South Korea, Post code: chnaha@ajou.ac.kr Accepted November 16, to be associated with an increased risk of coronary disease, which further worsens with weight gain (4). In addition, components of the metabolic syndrome are risk factors for impaired glucose metabolism (5). In the USA, 23.7% of adults were classified as having the metabolic syndrome by the National Cholesterol Education Program (NCEP) (6) definition when the 3 rd National Health and Nutrition Examination Survey was used (7). From this report, >40 million US adults seem to be affected by the metabolic syndrome. Furthermore, the number of cases of metabolic syndrome is increasing. This trend has also been observed in Asian countries (8, 9). Thus, the metabolic syndrome constitutes a major challenge for public health professionals and will be a social and economical problem in the near future. Compared with Caucasians, Asian-Americans had higher prevalence of the metabolic syndrome after 1 1 Bozza JEI 58/06 Soolim

2 S. Lim, H.C. Jang, H.K. Lee, et al. Ready for press adjusting for age, body size and composition, smoking, alcohol and exercise (10). These results imply that the prevalence of the metabolic syndrome differs according to genetic-environment interaction. Through the period , South Korea experienced an epidemiologic switchover from infectious diseases to chronic degenerative diseases (11). Westernization of diet and a decrease in activity due to modern conveniences have evoked metabolic imbalance, obesity, and explosive increase in cardiovascular disease and diabetes. Recently, a few studies on the metabolic syndrome have been undertaken in Korea, but these studies have tended to use their own criteria (12), or study subjects are usually confined to small numbers of restrictive groups (13). In this study, two communities representing a rural () and an industrial () area were selected for a prospective cohort study, named as the Korean Health and Genome Study (KHGS). There might be a significant difference in the obesity, lipid levels and blood pressures between rural and urban community, since lifestyle and diet patterns have been very different (14, 15). Thus, the characteristics of the metabolic syndrome in such communities are thought to differ. This cohort study will be continued prospectively for a period of 10 yr. As a baseline study, we estimated the prevalence of the metabolic syndrome according to the region and sex, by applying the NCEP definitions. The most effective way to reduce the prevalence of the metabolic syndrome in this population was also discussed. MATERIALS AND METHODS Study population Two South Korean communities were selected, one from cohort, representing a rural community, and the other from, representing an urban community. The first survey was performed in 2001 and follow-up surveys will be undertaken biennially up to The target number for study was 10,000 (5000 in each community). Eligibility criteria were based on age (40-69 yr), residence within the borders of the survey area for at least 6 months before testing, and mental and physical ability to participate. The farming community of is located about 60 km south of Seoul and had a population of 132,906 in 2000 (16). Cluster sampling was conducted, and 5024 subjects were surveyed among 7192 eligible subjects (response rate 70%). The industrial community of is located about 40 km southwest from Seoul and had a population of 554,998 in 2000 (16). Twenty-one clusters were selected by district, and cluster sampling was conducted according to age and sex, using a local telephone directory. The total number of the population who were yr old was 125,775, and 5020 subjects (4.0%) were enrolled in the present study. In total, 10,044 people were eligible: 5024 in the farming community, and 5020 in the industrial community,. Anthropometric information was assessed using a standard questionnaire and recorded during the baseline visit. The face-toface interview method was used. All subjects participated in the study voluntarily and informed consent was obtained in all cases. The study protocol was approved by the Ethic Committee of the Korean Health and Genome Study. Measurement of anthropometric and biochemical parameters Height (cm) and body weight (kg) were measured to the nearest 0.1 cm or 0.1 kg. Height and weight measurements were made barefoot in light clothing. Body mass index (BMI) was calculated as the weight divided by the height squared (kg/m 2 ). Waist circumference was measured at the narrowest point between the lower limit of the ribcage and the iliac crest to the nearest 0.1 cm. Hip circumference was measured at maximal extension of the buttocks to the nearest 0.1 cm. Body fat and lean body mass were measured by tetrapolar bioelectrical impedance analysis (Inbody 3.0, Biospace, Korea). Bioelectrical impedance analysis measures two parameters, fat and lean tissue, and the results of this method correlate well with underwater weighing, except in extremely obese subjects (17, 18). Subjects were also asked to refrain from food, beverages and exercise for 4 h before measurement. Blood pressure was recorded 3 times between 07:00 and 09:00 h, after subjects had been in a relaxed state for at least 10 min, and a 5 min resting period was given between each measurement. Subjects were asked to refrain from smoking for 24 h and from consuming alcohol for 7 days before blood sampling. After 14 h overnight fasting, venous blood samples were drawn from the antecubital vein at 07:00 to 09:00 h. Plasma was separated immediately by centrifugation (2000 rpm, 20 min, at 4 C), and biochemical measurements were conducted immediately. The fasting plasma concentrations of glucose, total cholesterol, triglyceride, and HDL-cholesterol were measured enzymatically using the Hitachi 747 chemistry analyzer (Hitachi, Tokyo, Japan). The level of LDL-cholesterol was calculated by using the following formula: [total cholesterol HDL-cholesterol triglyceride/5] (19) Fasting plasma insulin concentrations were determined by radioimmunoassay (LINCO kit, Missouri, USA). The homeostasis model assessment of the insulin resistance (HOMA-IR) index was calculated using the following formula: fasting plasma insulin (µiu/ml) fasting plasma glucose (mg/dl) /22.5 (20) Definition of the metabolic syndrome According to the NCEP-Adult Treatment Panel III (ATP III) criteria (6), an individual may be diagnosed as having the metabolic syndrome if he or she has three or more of the following criteria: 1) abdominal obesity: waist circumference 90 cm in men and 80 cm in women (International Obesity Task Force criteria for Asian-pacific population was used to determine waist circumference criteria) (21), 2) triglycerides: 150 mg/dl (1.7 mmol/l), 3) HDL cholesterol: <40 mg/dl (1.0 mmol/l) in men and <50mg/dl (1.3 mmol/l) in women, 4) blood pressure: 130/85 mmhg or antihypertensive medication, 5) fasting glucose: 110 mg/dl (6.1 mmol/l) or medication (insulin or oral agents). Statistical analysis All data is presented as means±sd. Mean variable value of the two groups was compared using the student s t-test (Table 1). Chi-square test was used to compare social factors (Table 1). Multiple regression 2

3 Baseline report of a 10 yr-prospective study analysis, including community and age as a categorical variable, was performed to compare continuous variables related with insulin resistance in two communities (Table 2). After age adjustment was done by direct method, comparison of the prevalence of components constituting the metabolic syndrome was analyzed using the chi-square test (Table 3). Chi-square test was also used to compare the prevalence of metabolic syndrome between a rural community () and an urban community () in male and female (Fig. 1). Statistical significance was defined as p<0.05. All analyses were performed using SPSS 10.0 software (SPSS, Inc., Chicago, Illinois). RESULTS In this study, 26.1% of the total subjects were classified as having the metabolic syndrome as defined by the NCEP using Asian-Pacific criteria for waist circumference. Age and sex adjusted prevalences were 29.3 and 22.3% in the rural and urban community, respectively (p<0.01). The anthropometric characteristics of male and female subjects by community are shown in Table 1. The mean age and the proportion of female to male subjects were higher than that of the subjects. The residence period of population was about three times longer than that of. The percentage of current smokers was >40% in males, but that was <5% in females in both communities, which is much lower than in the West. In terms of exercise, the proportion of regular exercise in the urban community was higher than that in the rural community, especially for female subjects. The urban community had higher education achievement levels than the rural community. The physical and biochemical parameters related to insulin resistance are shown in Table 2. Most factors were significantly higher in males of the urban community than in those of the rural community except waist-hip ratio, blood pressure and fasting plasma insulin. However, females of the rural community had higher BMI, waist circumference, waist-hip ratio, blood pressure, fasting insulin, triglyceride, and HOMA-index than that of urban community. Table 1 - Anthropometric characteristics of male and female subjects from the (rural) and (urban) communities. Males (no.=4763) Females (no.=5281) (no.=2240) (no.=2523) (no.=2784) (no.=2497) Mean±SD Mean±SD p Mean±SD Mean±SD p Age (yr) 55.5± ±7.5 < ± ±8.2 <0.01 Residence (yr) 45.0± ±9.5 < ± ±8.1 <0.01 Smoking status (%) <0.01 ns Non-smoker Ex-smoker Current smoker Alcohol status (%) ns <0.01 Non-drinker Ex-drinker Current drinker Exercise status (%) <0.01 <0.01 Non Once/week >2-3/week Education (%) <0.01 <0.01 Elementary High school Occupation (%) <0.01 <0.01 Farming Values are expressed as means±sd or percentages; Two-sided independent samples t-test was used; Chi-square test was used. 3

4 S. Lim, H.C. Jang, H.K. Lee, et al. Ready for press Table 2 - Age-adjusted comparison of insulin resistance factors in (rural) and (urban) communities by sex. Males (no.=4763) Females (no.=5281) (no.=2240) (no.=2523) (no.=2784) (no.=2497) Mean±SD Mean±SD Mean±SD Mean±SD Height (kg) 165.7± ± ± ±5.2 Weight (cm) 65.2± ± ± ±8.2 BMI (kg/m 2 ) 23.7± ± ± ±3.2 Waist circ. (cm) 83.8± ± ± ±8.7 Hip circ. (cm) 90.6± ± ± ±5.3 Waist-hip ratio 0.92± ± ± ±0.07 LBM (kg) 51.4± ± ± ±4.2 Fat mass (kg) 13.8± ± ± ±5.1 Body fat (%) 20.8± ± ± ±5.0 SBP (mmhg) 125.8± ± ± ±18.1 DBP (mmhg) 83.1± ± ± ±11.3 FPG (mg/dl) 92.4± ± ± ±23.9 FPI (µiu/ml) 7.3± ± ± ±4.1 Total C (mg/dl) 188.1± ± ± ±37.4 TG (mg/dl) 167.5± ± ± ±82.8 HDL-C (mg/dl) 49.2± ± ± ±11.8 LDL-C (mg/dl) 110.7± ± ± ±34.6 HOMA-index 1.7± ± ± ±1.1 Waist and hip circ.: waist and hip circumference; LBM: lean body mass; SBP and DBP: systolic and diastolic blood pressure; FPG and FPI: fasting plasma glucose and insulin; Total C: total cholesterol; HDL-C: HDL- cholesterol; and LDL-C: LDL- cholesterol; TG: triglyceride; BMI: body mass index. p<0.01, p<0.05, p-value for community in a multiple regression with community and age groups (40-49, 50-59, and yr) as predictors. LDL-cholesterol was calculated using the following formula: [total cholesterol (HDL-cholesterol + TG/5)]; homeostasis model assessment (HOMA) index = fasting plasma insulin (µiu/ml) x fasting plasma glucose (mg/dl) /22.5. Conversion factor to SI U: mg/dl x =mmol/l in glucose, µiu/ml x 6.945=pmol/l in insulin, mg/dl x =mmol/l in Total C, HDL and LDL-C, mg/dl x =mmol/l in TG. Figure 1 shows sex-specific prevalence comparison of the metabolic syndrome between the rural () and urban () community by NCEP working definition using Asian-Pacific criteria for waist circumference. The prevalence of the metabolic syndrome was significantly different between male and female subjects (20.0 and 31.7%, respectively; p<0.01). As age increases, so does the prevalence of the metabolic syndrome in females in both communities. The prevalence in males also increased with age but the degree of increase was not as remarkable as for females. The prevalence of males even decreased in their 60s. When comparing with in each sex, showed higher prevalence than in all ages of females, but there was a cross in males; that is, was higher in 40s and was higher in 60s. Age-adjusted prevalence of the components of the metabolic syndrome as used by the NCEP definition is shown in Table 3. In males, abdominal obesity and blood pressure were higher in, but fasting plasma glucose was higher in. In females, the prevalence of abdominal obesity, blood pressure and low HDL-cholesterolemia were higher in than in. DISCUSSION In this study, 26.1% of subjects had the metabolic syndrome according to the NCEP definitions using Asian-Pacific criteria for waist circumference. The agestandardized prevalence was 25.6% using the Korean standard population. This is comparable to the result of the US 3 rd National Health and Nutrition Examination 4

5 Baseline report of a 10 yr-prospective study Table 3 - Age-adjusted prevalence (%) of components of metabolic syndrome by the National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATP III) definition. Males (no.=4763) Females (no.=5281) Variables p p Waist circumference 90 for men and 80 cm for women <0.001 BP 130/85 mmhg or medication < <0.001 FPG 110 mg/dl (6.1 mmol/l) or medication < ns TG 150 mg/dl (1.7 mmol/l) ns ns HDL-cholesterol <40 mg/dl (1.0 mmol/l) for men and 50 <mg/dl (1.3 mmol/l) for women ns BP: blood pressure; FPG: fasting plasma glucose; TG: triglyceride. Chi-square test was used; abdominal obesity as defined by Asian-Pacific guideline. Survey showing 23.7% of metabolic syndrome (7). Comparing rural with urban community, rural was 32.1% and urban was 20.1% in the prevalence of the metabolic syndrome (age and sex adjusted prevalences were 29.3 and 22.3%, respectively; p <0.01). As age increases, the prevalence of the metabolic syndrome increased in females in both communities, but it was not so in males (Fig. 1). The degree of increase in males was not as high as that in females and even the prevalence decreased in males of the community. The main reason for the discrepancy was based on the abdominal obesity. In females, waist circumference correlated with age (r=0.350, p<0.01), but there was no correlation in males (r= 0.014, p>0.05). Interestingly, waist circumference was higher, but hip circumference was lower in the farming than in the industrial area after age adjustment (Table 2). Therefore, there was a large difference in mean waisthip ratios between the two communities. This is assumed to be due to the difference in environmental background in the two communities. In a recent study, 500 rural and 492 urban subjects aged were surveyed in a Middle East country (22). The results showed no differences in the prevalence of hypertension and diabetes, but found that elevated triglycerides, low HDL-cholesterol, and overall obesity were more prevalent in the urban population. Interestingly, these results were very different from the present study showing that abdominal obesity and high blood pressure were more prevalent in the rural population of present study (Table 3). Among five components of the metabolic syndrome, the waist circumference of females was the factor showing the biggest difference between the rural and urban community (69.1 vs 41.7%). This seems to be due to a lack of regular exercise; the proportion of females doing regular exercise was 25.2% lower in the rural (16.2%) than in the urban community (41.4%). Metabolic syndrome (%) Males (rural community) (urban community) Metabolic syndrome (%) Females (rural community) (urban community) Age group Age group Fig. 1 - Prevalence comparison of the metabolic syndrome between a rural community () and an urban community () in males and females. [The National Cholesterol Education Program-Adult Treatment Panel III criteria was used (p<0.01)]. 5

6 S. Lim, H.C. Jang, H.K. Lee, et al. Ready for press High blood pressure was also more prevalent in the rural population of the present study (Table 3). A high salt diet in the rural community in Korea can influence this difference (23). Considering the levels of HDLcholesterol are determined by the degree of obesity, alcohol consumption, diabetes, the status of nutrition and physical inactivity (24-26), the higher prevalence of low HDL-cholesterolemia in females living in the rural community might be due to their higher degree of obesity and their lower levels of physical activity (Tables 1 and 2). In terms of fasting plasma glucose criteria, the males living in the urban population showed a higher prevalence than those in the rural population. This is estimated to be affected by the preference of western diet in the urban male population. Until now, there has been no clear rationale for the application of different cutoff points for waist circumference in the Asian population. However, when the original NCEP-ATP III criteria were used for waist circumference, only 1.1% of male subjects had abdominal obesity in this study. A number of studies suggested that at obesity cutoff points, that are much lower than World Health Organization (WHO)-recommended values, the absolute risk of developing cardio vascular disease (CVD) is markedly elevated for the Asian population (27, 28). For this reason and the world-wide comparison, Asia- Pacific criteria of waist circumference were used for abdominal obesity in this study. Considering waist circumference was the most prevalent among the components of the metabolic syndrome in female subjects, intervention to waist circumference is estimated to be the most effective way to reduce the prevalence of the metabolic syndrome. In fact, if waist circumference is reduced by 1 inch (2.54 cm), the prevalence of the metabolic syndrome will be decreased by 18.4% (20.1% 16.4%) in females. Abdominal obesity is well proven to be associated with the leading causes of death, such as CVD, diabetes, cancer and so on (29-31). The role of physical activity in treating these obesity-related disorders is therefore of great interest. The metabolic syndrome as well as diabetes is known to easily develop in sedentary men (32). A randomized controlled study reported that physical activity substantially reduced abdominal obesity and improved the lipid profiles (33). Furthermore, many large-scale epidemiologic studies showed that physical activity could prevent the development of diabetes and hypertension, which are typical phenotypes of the metabolic syndrome (34, 35). In the present study, 2.4% of subjects had taken some kind of lipid lowering agents. These may alter the levels of triglycerides or HDL cholesterol, but the variety of agents involved prevented analysis. The inclusion of individuals taking such medications would have caused underestimations in the present study. The response rate of 70% in the rural community was not low, but we examined the demographic characteristics of the nonresponders to assess potential selection bias. Responders and non-responders were compared by age, sex and the prevalence of several diseases. No significant differences were found in the average ages, age distribution, or prevalence of diabetes in these two groups. In conclusion, abdominal obesity in the rural and dyslipidemia in the urban community were found to be the most prevalent components of the metabolic syndrome in this study. Women living in the rural community were found to be most vulnerable to the metabolic syndrome. The final goal of this study was to identify the most contributing factor to the metabolic syndrome in each community and to apply the result to the general population to prevent the development of diabetes or CDV. Judging from this point of view, it is necessary to encourage people to have healthy dietary habits and high physical activity. As a recent study proved, modest modification of lifestyle can be the most effective way of treating this clustering of metabolic abnormalities (36). Given the rapid progression of the Korean economy over the past 30 yr, the prevalence of the metabolic syndrome is expected to increase continuously. We therefore suggest that the national strategy for prevention of the metabolic syndrome should be concentrated on reducing abdominal obesity and dyslipidemia. Healthy dietary habits and regular exercise should be emphasized as part of the strategy. ACKNOWLEDGMENTS This study was supported by the National Genome Research Institute, Korea, National Institute of Health research contract (budgets , , , and ). REFERENCES 1. Meigs JB. Invited commentary: insulin resistance syndrome? Syndrome X? Multiple metabolic syndrome? A syndrome at all? Factor analysis reveals patterns in the fabric of correlated metabolic risk factors. Am J Epidemiol 2000, 152: Trevisan M, Liu J, Bahsas FB, Menotti A. 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