Trends in the Diabetes Epidemic in Korea

Review Endocrinol Metab 2015;30:142-146 http://dx.doi.org/10.3803/EnM.2015.30.2.142 Article pISSN 2093-596X · eISSN 2093-5978

Kyoung Hwa Ha1,2, Dae Jung Kim1,2

1Department of Endocrinology and Metabolism, 2Cardiovascular and Metabolic Disease Etiology Research Center, Ajou University School of Medicine, Suwon, Korea

Diabetes mellitus is a leading cause of mortality and increased disability-adjusted life years worldwide. In Korea, the prevalence of diabetes increased from 8.6% to 11.0% in 2001 to 2013 and the prevalence of adult obesity, which is the most important risk factor of diabetes, increased from 29.2% to 31.8% during the same period. There has been a dramatic increase in the number of obese Koreans with diabetes in recent decades and the prevalence of diabetes in people aged 40 years and older also increased in 2001 to 2013. Nevertheless, the mean age at the first diagnosis of diabetes was very similar for men in 2005 and 2013, while the mean age for women decreased slightly. There is an inverse linear relationship between body mass index and age at the diagnosis of diabetes among those who are newly diagnosed. Accordingly, the prevalence of diabetes is increasingly shifting to younger individuals and those who are obese. Therefore, public efforts should focus on healthy lifestyle changes, primary prevention measures, screening for the early detection of diabetes, and long-term management.

Keywords: Age; Diabetes mellitus; Epidemiology; Korea; National survey; Obesity; Prevalence

INTRODUCTION increases in medical costs [4].

Diabetes mellitus is a leading cause of mortality and increased PREVALENCE OF DIABETES AND OBESITY disability-adjusted life years (DALYs) worldwide. In 2010, an estimated 1.3 million diabetes-related deaths occurred world- Recently, the prevalence of diabetes has increased in conjunc- wide, which was twice as many as occurred in 1990 [1]. Fur- tion with the incidence of obesity. According the Korea Na- thermore, the DALYs from diabetes increased by 30% during tional Health and Nutrition Examination Survey (KNHANES) this same period from 380 per 1,000 persons to 523 per 1,000 studies in 2001 to 2013, the age-standardized prevalence of di- persons [2]. Although the mortality rate of diabetes in Korea abetes among adults 30 years of age and older increased from decreased from 25.0 per 100,000 persons in 2003 to 21.5 per 8.6% to 11.0% and the age-standardized prevalence of adult 100,000 persons in 2013, diabetes was still ranked as the fifth obesity, defined as a body mass index (BMI) of 25 kg/m2 or most common cause of death in 2013 [3]. In addition to its as- higher, increased from 29.2% to 31.8% [5,6]. During the same sociation with mortality, diabetes, and diabetes-related chronic period, the rates of diabetes and obesity tended to increase complications such as retinopathy, neuropathy, nephropathy, among men, while among women the prevalence of diabetes cardiovascular, and cerebrovascular diseases, peripheral artery increased but the prevalence of obesity decreased (Fig. 1). occlusive diseases, and amputations are related to significant Studies have consistently reported an association between

Received: 17 March 2015, Revised: 20 March 2015, Copyright © 2015 Korean Endocrine Society Accepted: 25 March 2015 This is an Open Access article distributed under the terms of the Creative Com Corresponding author: Dae Jung Kim mons Attribution Non-Commercial License (http://creativecommons.org/ Department of Endocrinology and Metabolism, Ajou University School of licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribu Medicine, 164 World cup-ro, Yeongtong-gu, Suwon 443-380, Korea tion, and reproduction in any medium, provided the original work is properly Tel: +82-31-219-5128, Fax: +82-31-219-4497, E-mail: [email protected] cited.

142 www.e-enm.org Diabetes Epidemic in Korea Endocrinol Metab 2015;30:142-146 http://dx.doi.org/10.3803/EnM.2015.30.2.142 pISSN 2093-596X · eISSN 2093-5978 Obesity Diabetes mellitus 100 40 31.8 32.4 39.9 29.2 31.3 31.7 30.7 31.3 30.9 31.4 80 46.7 30 53.7 47.4 20 60 % Obesity 10 11.0 26.5 Overweight 9.1 9.6 9.7 9.6 9.7 9.8 9.0 Prevalence in total (%) in total Prevalence 8.6 40 27.6 24.2 0 19.4 Normal 2001 2005 2007 2008 2009 2010 2011 2012 2013 Year A 20 33.6 25.6 26.9 28.4

Obesity 0 2001 2005 2009 2013 60 Diabetes mellitus Year A 50 37.6 34.7 36.2 35.8 36.4 35.1 36.3 40 31.8 35.3 100 30 20 50.5 10 12.8 80 47.6 10.5 11.8 10.7 11.0 11.9 52.1 Prevalence in men (%) Prevalence 9.5 10.6 10.1 50.1 0 2001 2005 2007 2008 2009 2010 2011 2012 2013 60 B Obesity

Year % Overweight 40 27.0 22.1 23.6 25.1 Normal Obesity 40 Diabetes mellitus 20 30 25.1 25.4 24.8 25.8 27.4 27.3 26.3 25.2 26.0 24.8 27.1 28.0 25.9 20 0 10 2001 2005 2009 2013 9.1 7.9 7.7 7.3 8.5 8.4 8.3 7.6 8.0 Year B

Prevalence in women (%) Prevalence 0 2001 2005 2007 2008 2009 2010 2011 2012 2013 Year C Fig. 2. Distribution of obesity in diabetic (A) men and (B) women in the Korea National Health and Nutrition Examination Survey Fig. 1. (A-C) Prevalence of diabetes and obesity among Korean 2001 to 2013. We defined obesity using the following body mass < 2 adults aged ≥30 years in 2001 to 2013. index (BMI) categories: normal (BMI 23 kg/m ), overweight (23≤BMI<25 kg/m2), and obese (BMI≥25 kg/m2).

obesity and diabetes. In a large representative sample from the number of obese people with diabetes in Korea. The average United States, the highest prevalence of diabetes was observed BMI of diabetic Korean patients increased from 21.9 kg/m2 in in subjects with a BMI ≥40 kg/m2 [7], and Menke et al. [8] 1989 to 1990 to 24.8 kg/m2 in 2010 to 2012 [12,13]. In 2013, found that changes in BMI over time are the greatest contribu- 71.6% of men and 74.2% of women with diabetes were obese tor to the increased prevalence of diabetes in this population. or overweight (Fig. 2, unpublished data). Eckel et al. [9] demonstrated that obesity is linked to diabetes through the increased production of adipokines and cytokines, AGE-SPECIFIC TRENDS IN THE reductions in adiponectin levels, altered ectopic fat deposition, PREVALENCE OF DIABETES and mitochondrial dysfunction. However, because not all obese individuals develop diabetes, the relationship between National surveys conducted between 2001 and 2013 in Korea obesity and diabetes remains unclear. For example, the influ- revealed age-related increases in the prevalence of diabetes in ence of abdominal obesity on the risk of diabetes was found to all age groups, except for those between 30 and 39 years of be more important than that of general obesity [10]. Given the age [5]. Because Korea is a rapidly aging society, this increase striking parallel increases in the incidences of these two condi- was particularly evident in people aged 70 years and older; the tions, obesity is likely an important contributing factor to the rate of diabetes in this age group was 27.6% in 2013, approxi- manifestation of diabetes and the complications, mortality, and mately twice as high as in 2001 (Fig. 3). However, the mean morbidity related to this disease [11]. age at first diagnosis of diabetes was very similar among men In recent decades, there has been a dramatic increase in the in 2005 (49.3 years) and 2013 (50.6 years), while the mean Copyright © 2015 Korean Endocrine Society www.e-enm.org 143 Ha KH, et al.

60 30

25 56.4 55.3 55 20 53.5 Total

% 52.9 15 52.6 52.2 Women Men 50 50.9 50.6 10 49.3 5 45

0 (yr) diagnosis of diabetes Age at initial 2005 2009 2013 30–39 40–49 50–59 60–69 70+ Year Age group 2001 4.9 5.9 10.2 16.1 15.1 Fig. 4. Age at the initial diagnosis of diabetes in the Korea Na- 2007 4.2 5.7 13.4 19.7 17.5 tional Health and Nutrition Examination Survey 2005 to 2013. 2013 2.5 7.3 12.6 25.2 27.6

32 Fig. 3. Age-specific prevalence rates of diabetes among Koreans during 2001 to 2013. 30.4 30 Obese age among women decreased slightly from 56.4 to 55.3 years 28

) 27.2 (Fig. 4, unpublished data). Thus, there is roughly a 5-year dif- 2 26.0 26.5 ference between men and women in terms of age at the first 26 diagnosis of diabetes. BMI (kg/m 24.6 24.4 According to the Centers for Disease Control and Preven- 24 Overweight tion in the United States, the mean and median ages at the first 22 diagnosis of diabetes among American adults aged 18 years or Normal weight older were 53.7 and 53.8 years in 1997 and 53.8 and 54.2 20 years in 2011 [14]. The median ages at diagnosis of diabetes <30 31–40 41–50 51–60 61–70 ≥71 were 53.6 years for men and 55.2 years for women in 2011 Age at diagnosis of diabetes (yr) [14]. In Korea, the age at the diagnosis of diabetes is similar to Fig. 5. Association of body mass index (BMI) and age at diagno- that in the United States, but Korean men tend to develop dia- sis in newly diagnosed subjects with diabetes in the Korea Na- betes about 3 years earlier than American men (unpublished tional Health and Nutrition Examination Survey 2013. data). cardiovascular disease, and all-cause mortality. For example, OBESITY AND AGE AT THE DIAGNOSIS OF Banerjee et al. [17] suggested that the duration of diabetes is DIABETES an important determinant of ischemic stroke risk. Zoungas et al. [18] reported that diabetes duration is independently asso- The KNHANES 2013 revealed an inverse linear relationship ciated with the risk of macrovascular complications such as between BMI and age at diagnosis of diabetes among newly cardiovascular death, non-fatal myocardial infarctions or non- diagnosed subjects (Fig. 5, unpublished data). It has been re- fatal strokes, microvascular complications such as nephropa- ported that obesity is independently associated with early on- thy and retinopathy, and death from any cause. Additionally, a set diabetes [15] and the European Prospective Investigation longer duration of diabetes is associated with serious diabetes- into Cancer and Nutrition-Potsdam Study found that weight related long-term complications in midlife [19]. gain in early adulthood (25 to 40 years) is more strongly asso- Wannamethee et al. [20] demonstrated that people who de- ciated with the risk and earlier onset of diabetes than weight veloped diabetes prior to 60 years of age had a risk of coro- gain after the age of 40 years [16]. nary heart disease that was approximately twice that of per- A number of studies have reported that the age at onset and sons who were diagnosed with diabetes after age 60. Because duration of diabetes are associated with microvascular events, the chronic worsening of hyperglycemia is generally associat- 144 www.e-enm.org Copyright © 2015 Korean Endocrine Society Diabetes Epidemic in Korea

ed with an insulin insufficiency in individuals with a longer sis for the Global Burden of Disease Study 2010. Lancet duration of diabetes, it is difficult to determine the underlying 2012;380:2197-223. mechanisms. This finding may have important public health 3. National Statistical Office. Annual report on the vital sta- and economic implications because individuals with diabetes tistics in Korea. Seoul: National Statistical Office of Ko- tend to require sustained health services and often develop rea; 2014. early complications during the period of highest productivity. 4. Moon EJ, Jo YE, Park TC, Kim YK, Jung SH, Kim HJ, Kim DJC, Y S, Lee KW. Clinical characteristics and direct CONCLUSIONS medical costs of type 2 diabetic patients. Korean Diabetes J 2008;32:358-65. In conclusion, the prevalence of diabetes is increasingly shift- 5. Korean Ministry of Health and Welfare. Korea Health Sta- ing to younger individuals and obese people. As more people tistics 2012: Korea National Health and Nutrition Exami- develop diabetes earlier and live longer, public efforts should nation Survey. Seoul: Korean Ministry of Health and Wel- focus on healthy lifestyle changes, primary prevention mea- fare; 2014. sures, screening for the early detection of diabetes, and long- 6. Kim DJ. The epidemiology of diabetes in Korea. Diabetes term management. Following a diagnosis of diabetes, treat- Metab J 2011;35:303-8. ment measures should include intensive glycemic control to 7. Nguyen NT, Nguyen XM, Lane J, Wang P. Relationship minimize the risk of microvascular and macrovascular com- between obesity and diabetes in a US adult population: plications. Because the treatment of obesity is an important in- findings from the National Health and Nutrition Examina- tervention that can reduce the prevalence of diabetes, the man- tion Survey, 1999-2006. Obes Surg 2011;21:351-5. agement of obesity should be considered for obese people 8. Menke A, Rust KF, Fradkin J, Cheng YJ, Cowie CC. Associ- with diabetes. ations between trends in race/ethnicity, aging, and body mass index with diabetes prevalence in the United States: a series CONFLICTS OF INTEREST of cross-sectional studies. Ann Intern Med 2014;161:328-35. 9. Eckel RH, Kahn SE, Ferrannini E, Goldfine AB, Nathan No potential conflict of interest relevant to this article was re- DM, Schwartz MW, Smith RJ, Smith SR. Obesity and type ported. 2 diabetes: what can be unified and what needs to be indi- vidualized? J Clin Endocrinol Metab 2011;96:1654-63. ACKNOWLEDGMENTS 10. Lee YH, Bang H, Kim HC, Kim HM, Park SW, Kim DJ. A simple screening score for diabetes for the Korean popula- This study was supported by a grant from the Korea Health tion: development, validation, and comparison with other Technology R&D Project through the Korea Health Industry scores. Diabetes Care 2012;35:1723-30. Development Institute (KHIDI), Ministry of Health and Wel- 11. Scheen AJ, Paquot N. Obesity: a new paradigm for treating fare, Republic of Korea (grant no.: HI13C0715). obesity and diabetes mellitus. Nat Rev Endocrinol 2015;11: 196-8. REFERENCES 12. Jeon JY, Kim DJ, Ko SH, Kwon HS, Lim S, Choi SH, Kim CS, An JH, Kim NH, Won JC, Kim JH, Cha BY, Song KH; 1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Taskforce Team of Diabetes Fact Sheet of the Korean Diabetes Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY. Glob- Association. Current status of glycemic control of patients al and regional mortality from 235 causes of death for 20 age with diabetes in Korea: the fifth Korea National Health and groups in 1990 and 2010: a systematic analysis for the Glob- Nutrition Examination Survey. Diabetes Metab J 2014;38:197- al Burden of Disease Study 2010. Lancet 2012;380:2095- 203. 128. 13. Ko KS, Oh TG, Kim CH, Park KS, Lee MK, Kim SY, Cho 2. Murray CJ, Vos T, Lozano R, Naghavi M, Flaxman AD, BY, Lee HK, Koh CS, Min HK. A clinical study on the Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S. complications of non-insulin-dependent diabetes mellitus Disability-adjusted life years (DALYs) for 291 diseases in Korea. J Korean Diabetes Assoc 1991;15:257-62. and injuries in 21 regions, 1990-2010: a systematic analy- 14. Centers for Disease Control and Prevention (CDC); Na- Copyright © 2015 Korean Endocrine Society www.e-enm.org 145 Ha KH, et al.

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