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Increasing Prevalence of Metabolic Syndrome in Korea

OBJECTIVE The number of people with metabolic syndrome is increasing worldwide, and changes in socioenvironmental factors contribute to this increase. Therefore, investigation of changes in metabolic syndrome and its components in South Korea, where rapid socioenvironmental changes have occurred in recent years, would be foundational in setting up an effective strategy for reducing this increasing trend. RESEARCH DESIGN AND METHODS We compared the prevalence and pattern of metabolic syndrome among participants in the Korean National Health and Nutrition Examination Surveys for 1998, 2001, 2005, and 2007. In each survey, stratified, multistage, probability–sampling designs and weighting adjustments were conducted to represent the entire Korean population. The revised National Cholesterol Education Program criteria were used as the definition of metabolic syndrome. All biochemical parameters were measured in a central laboratory. RESULTS A total of 6,907 (mean ± SE age 45.0 ± 0.2 years), 4,536 (45.5 ± 0.2), 5,373 (47.1 ± 0.2), and 2,890 (49.9 ± 0.3) Koreans over 20 years of age have participated in the studies in 1998, 2001, 2005, and 2007, respectively. The age-adjusted prevalence of metabolic syndrome increased significantly from 24.9% in 1998, 29.2% in 2001, and 30.4% in 2005 to 31.3% in 2007. Among the five components, the level of low HDL cholesterol increased the most, by 13.8% over the 10 years. Abdominal obesity and hypertriglyceridemia followed, with 8.7 and 4.9% increases, respectively. CONCLUSIONS Because dyslipidemia and abdominal obesity were major factors in increasing the prevalence of metabolic syndrome in Koreans for the past 10 years, lifestyle interventions should be conducted at the national level to reduce the burden and consequences of metabolic syndrome.

M etabolic syndrome increases cardiovascular morbidity and mortality and all-cause mortality (1). Metabolic syndrome also increases the risk of developing diabetes because its components represent major risk factors for impaired glucose metabolism (2).
The prevalence of metabolic syndrome is increasing worldwide. According to data from the National Health and Nutrition Examination Survey (NHANES) III and NHANESs 1999-2006, the age-adjusted prevalence of metabolic syndrome increased from 29.2 to 34.2% in the U.S. (3). This increasing trend also has been observed in Asian countries (4), presenting a major challenge for public health professionals as well as becoming a social and economic problem in the near future.
The characteristics of metabolic syndrome can differ according to ethnicity and socioeconomic differences and changes. As a consequence, Asians have a higher prevalence of metabolic syndrome than whites after adjusting for body size (5). Hence, understanding the socioeconomic context of Asian populations is critical in establishing appropriate strategies for addressing this wide prevalence. South Korea is distinct for experiencing a major economic crisis in 1998, followed by a rapid recovery through adopting Western policies and cultures. This sudden change of the socioenvironment resulted in a dramatic lifestyle change for people living in South Korea. Today, South Koreans are eating more "Western" food and are less physically active than a decade ago. South Korea is one of the countries where the socioeconomic environment has changed rapidly to reflect more Westernization as well as its negative health consequences. Thus, documenting the changes in metabolic syndrome characteristics in South Korea during this period of socioeconomic changes is intriguing and important. In this study, we investigated the changes in the prevalence of metabolic syndrome in four nationwide surveys (the Korean NHANESs [KNHANESs] in 1998[KNHANESs] in , 2001[KNHANESs] in , 2005[KNHANESs] in , and 2007) by applying the revised National Cholesterol Education Program (NCEP) definition (6). We also investigated the changes in the factors constituting metabolic syndrome. To give an equal probability of being sampled, weights were assigned to each respondent, enabling the results to represent the entire Korean population. This weighting method guarantees unbiased point estimates of population parameters for the entire population and its subsets (9). All subjects in the studies participated voluntarily, and informed consent was obtained from them. The study protocol was approved by the Ministry of Health and Welfare in Korea.

Anthropometry
Anthropometric measurements were conducted by well-trained examiners in the same manner in the four studies. Height was measured to the nearest 0.1 cm using a portable stadiometer (Seriter, Bismarck, ND). Weight was measured to the nearest 0.1 kg using a calibrated balance-beam scale (Giant-150N; Hana, Seoul, Korea). Waist circumference measurements were taken at the end of normal expiration to the nearest 0.1 cm, measuring from the narrowest point between the lower borders of the rib cage and the iliac crest.

Measurement of metabolic risk factors
For each study, subjects were asked to refrain from smoking or consuming caffeine before the measurement. Blood pressure was measured twice, using a mercury sphygmomanometer (Baumanometer; Baum, Copiague, NY), in the sitting position after at least a 10-min rest. If the first two measurements differed by .5 mmHg, additional checks were obtained.
After a 12-h overnight fast, venous blood samples were drawn. Samples were immediately sent to a central, certified laboratory, and plasma was separated immediately by centrifugation. To confirm and compare accuracy and consistency in each survey, commutable frozen serum samples (n = 38) were taken from normal subjects and patients with dyslipidemia, according to the Clinical and Laboratory Standards Institute guidelines (www.clsi.org/). The commutable frozen serum samples were sent to the Centers for Disease Control and Prevention (Atlanta, GA) and were measured using the standard method. With data from the Centers for Disease Control and Prevention, the conversion rate for the KNHANES 2007 was obtained by a Passing and Bablok regression method ( Supplementary Fig. A). The revised HDL cholesterol extrapolations were based on a regression line, and it may theoretically cause excess residual error for prediction. However, the fitted regression line had an R 2 = 0.977. Therefore, the revised HDL cholesterol values were statistically well substantiated. Conversion rates for other surveys were obtained by a similar method as follows: Definition of metabolic syndrome According to the revised NCEP criteria (6), an individual may be diagnosed as having metabolic syndrome if he or she has three or more of the following criteria: 1) waist circumference .90 cm in men and .80 cm in women using the International Obesity Task Force criteria for the Asian-Pacific population to determine waist circumference (10); 2) triglycerides $150 mg/dL or medication use; 3) HDL cholesterol ,40 mg/dL in men and ,50 mg/dL in women or medication use; 4) blood pressure $130/85 mmHg or antihypertensive medication use; and 5) fasting glucose $100 mg/dL or medication use (insulin or oral agents).

Statistical analysis
All data are presented as means 6 SE or as prevalence (% and SE). Sampling weights were used to take the complex sampling into account, and statistical analyses were conducted using SAS version 8.   9 years older than those in the 1998 survey. Obesity indices, such as BMI and waist circumference, and lipid profiles, such as triglycerides and LDL cholesterol, increased significantly over 10 years (P , 0.05). In contrast, systolic and diastolic blood pressure decreased significantly over the same period (P , 0.05). Table 2 shows the prevalence of metabolic syndrome and its individual components among the U.S. NHANESs and the four KNHANESs. The prevalence of abdominal obesity, hypertriglyceridemia, and glucose criteria increased significantly in both countries. Compared with the U.S. NHANESs, the prevalence of high blood pressure has been decreasing in Korea. The prevalence of low HDL cholesterolemia decreased in the U.S. NHANES reports, but the opposite trend was observed in Korea. Of five individual metabolic syndrome components, the incidence of low HDL cholesterol criteria increased the most over 10 years (13.8%). Abdominal obesity and hypertriglyceridemia followed, showing 8.7 and 4.9% increases, respectively. In contrast, subjects meeting the blood pressure criteria decreased gradually. Even after stratifying subjects by antihypertensive medication status, a decreasing trend in blood pressured remained (Supplementary Fig. B).
There was a 5.5% difference in metabolic syndrome prevalence between men and women (22.4% in men and 27.9% in women) in 1998. In the 2007 KNHANES, there was a 3.9% difference between men and women; women had a significantly higher prevalence (32.9%) than men (29.0%; P , 0.05). However, the overall increase in metabolic syndrome prevalence over the 10 years was significantly higher in men (6.6%) than in women (5.0%; P , 0.05).
The prevalence of metabolic syndrome among Korean adults by sex in the four KNHANESs is shown according to age-groups (Fig. 1). In all studies, the prevalence of metabolic syndrome in men was higher than in women aged 20-49 years, but the prevalence of metabolic syndrome in women increased significantly at age 50 years and surpassed men thereafter.
In comparing the components of metabolic syndrome using the revised NCEP criteria (Fig. 2), men had a higher prevalence of fasting glucose, abnormal blood pressure, and hypertriglyceridemia criteria than women (all P , 0.05). In contrast, women showed a higher prevalence of abdominal obesity and low HDL cholesterolemia (both P , 0.05). The agespecific prevalence rates of the metabolic syndrome component using the revised NCEP definition for 1998, 2001, 2005, and 2007 are shown in Supplementary  Fig. C. It is noteworthy that, in all four studies, there was a tendency for men to have a relatively higher prevalence of increased fasting glucose, blood pressure, and hypertriglyceridemia at younger ages (20-49 years) than women.
CONCLUSIONS-When the revised NCEP definition using the Asia-Pacific abdominal obesity criteria was applied, the age-adjusted prevalence of metabolic syndrome was 24.9% in the KNHANES 1998 and 31.3% in the KNHANES 2007. The estimated annual increase was~0.6% over 10 years. Low HDL cholesterol, abdominal obesity, and hypertriglyceridemia played major roles in this increase.
The prevalence of metabolic syndrome in the KNHANES 2007 was 31.3%, which was similar to the result of the U.S. NHANESs for 1999-2006 at 34.2%, using the revised NCEP definition (3). However, it should be noted that lower criteria of abdominal obesity were used in the four KNHANESs than in the U.S. NHANESs. Indeed, the best BMI for Americans is 25 kg/m 2 for life expectancy, whereas the best BMI for Koreans is 23 kg/m 2 , based on hundreds of thousands of people for the extended .20-year longitudinal follow-up (11,12). Our distinctive data reserve plenty of reasons to use the standard criteria for metabolic syndrome in Koreans.
When comparing the percentage changes in the five components of metabolic syndrome, the prevalence of low HDL cholesterol increased the most (from 36.4 to 50.2%, a 13.8% increase). Thus, almost one-half of the Korean population has a low HDL cholesterol level. Besides HDL cholesterol, abdominal obesity and hypertriglyceridemia also have increased substantially. Both lipid levels and obesity are affected by lifestyle factors (13). Changing to a high-fat diet and low physical activity in Korean seems to have contributed to this high prevalence of abdominal obesity and dyslipidemia (14). In fact, Koreans' total energy intake increased from 1,985 and 1,976 kcal in 1998 and 2001, respectively, to 2,016 kcal in 2005 (15). Total fat intake also  Recently, several reports were published from the KNHANES with alternative analyses (19)(20)(21). Kim et al. (19) found that nutritional intakes were unequal by educational level and contributed this inequality to the economic crisis in Korea in 1998. This inequality of nutritional intake may be associated with a rapid increase of low HDL cholesterolemia. The other group reported that the treatment rate for hypertension was 59-90% (20). This high treatment rate may be associated with a decreasing tendency of hypertension over the period.
Another study (21) provided increasing trends in obesity measures among men and older-aged women but not in young women. This result is in accordance with the current analysis.
When comparing the prevalence of metabolic syndrome between men and women stratified by age-groups, men had a higher prevalence than women for ages ,50 years in every study (Fig. 1). In contrast, the prevalence of metabolic syndrome in women increased significantly from the age of 50 years and surpassed men thereafter. Considering that this remarkable increase in metabolic syndrome was observed for women starting at the age of~50 years, it seems likely that menopause could be a reason for this dramatic change. A similar increasing pattern of abdominal obesity in women supports this hypothesis.
As shown in Table 1, obesity indices and metabolic impairments have been rising over the past 10 years. In contrast, blood pressures have been significantly decreasing over the same period. Interestingly, these Korean data show conflicting trends of HDL cholesterolemia and blood pressure when compared with the U.S. data. The prevalence of low HDL cholesterolemia increased, whereas the prevalence of high blood pressure decreased in Korea, and the inverse is true for the U.S. NHANES III to NHANESs 1999NHANESs -2006. Thus, the characteristics of metabolic syndrome may change differently according to ethnicity and socioeconomic status.
In this analysis, blood pressure decreased, whereas antihypertensive medication rate increased from 6.1% in 1998 to 18.5% in 2007. There is no clear explanation to the decreasing pattern of prevalence of blood pressure criteria over the past 10 years in Korea. Several possibilities can be suggested. Koreans were traditionally used to eating a high-salt diet; however, for the recent 10 years, daily salt consumption decreased significantly as a result of the national campaign encouraging the "Dietary Approach to Stop Hypertension Diet" (22). Thus, changes in the dietary pattern to a lowsalt diet could be one reason for decreasing blood pressure, which was proven in Japan (23). A decrease in the smoking rate in men from 69.9% in 2001 to 42.0% in 2007 is believed to contribute to the decreasing pattern of high blood pressure (24). A dramatic increase in cardiovascular mortality in 1999, when South Korea experienced an economic crisis, could be another possible explanation for the decreasing trend in high blood pressure (25). The high cardiovascular mortality in 1999 leveled off and returned to an average level in the following years. In addition, there may be a possibility that the measurement of blood pressure had become more stabilized over time. South Korea is a good example demonstrating the impact of rapid lifestyle changes over a relatively short period on prevalence of metabolic abnormalities. South Korea experienced a major economic crisis in 1998, followed by a rapid and impressive economic recovery that is compatible to other developed countries. Thus, documenting such changes in metabolic syndrome characteristics in South Korea during this economic boom is critical in understanding the socioeconomic influence on public health.
In conclusion, the prevalence of metabolic syndrome increased rapidly from the KNHANES 1998 to the KNHANES 2007. Judging from this dramatic increase during these 10 years, a national strategy to prevent this increasing trend of metabolic syndrome should be developed. The first priority should be to reduce the burden of dyslipidemia and abdominal obesity. Lifestyle changes, such as regular exercise and a healthy diet with low sodium, carbohydrates, and fat, should be emphasized (6).