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Rapidly increasing diabetes-related mortality with socio-environmental changes in South Korea during the last two decades
Diabetes Research and Clinical Practice 74 (2006) 295–300 www.elsevier.com/locate/diabres
Rapidly increasing diabetes-related mortality with socio-environmental changes in South Korea during the last two decades Young Ju Choi 1, Young Min Cho 1, Chul Ku Park, Hak Chul Jang, Kyong Soo Park, Seong Yeon Kim, Hong Kyu Lee * Department of Internal Medicine, Seoul National University College of Medicine, 28 Yongon-dong Chongno-gu, Seoul 110-744, Republic of Korea Received 3 August 2005; accepted 30 March 2006 Available online 16 May 2006
Abstract Diabetes mellitus is the result of complex interactions involving many genes and environmental factors, and rapid socioenvironmental changes have been strongly associated with the development of diabetes. In this study, we examined the trends in diabetes mortality and associated socio-environmental changes that have occurred in South Korea over the last 20 years. Data from a national database and government reports for the years from 1983 to 2001 were analyzed. The data included mortality, socioeconomic changes, physical activity and dietary pattern indicators. Deaths from diabetes per 100,000 people increased from 5.3 in 1983 to 18.4 in 2001. Along with increasing diabetes-related mortality, many socio-economic indices (gross domestic production, proportion of tertiary industry and urbanization rate), proxies for physical activity (numbers of cars and time spent watching television) and diet indices (animal protein intake and fat intake) showed remarkable changes. To counter increasing prevalence of diabetes and its related mortality in South Korea, multidirectional efforts including lifestyle modification should be mandatory features of future public health policy. # 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Diabetes mellitus; Mortality; Korea; Socio-environmental change
1. Introduction The worldwide prevalence of diabetes mellitus has risen dramatically over the past two decades. Globally, the number of people with diabetes is expected to rise
Abbreviations: GDP, gross domestic product; ICD-10, Internal Classification of Disease, Injuries and Causes of Death, 10th revision; KNSO, Korea National Statistical Office; OECD, Organization for Economic Cooperation and Development * Corresponding author. Tel.: +82 2 2072 2266; fax: +82 2 762 9662. E-mail address: [email protected] (H.K. Lee). 1 They equally contributed to this work.
from the current estimate of 150–220 million in 2010 and 300 million in 2025 [1]. Diabetes is the result of complex interactions involving many genes and environmental factors. Evidence that exposure to certain environmental factors influences the development of diabetes, especially type 2 diabetes, is provided by studies on migrant populations. For example, Japanese Americans living in Seattle had a higher prevalence of type 2 diabetes than the Japanese living in Japan, which could be explained by increased visceral adiposity and insulin resistance associated with a westernized lifestyle [2,3]. Thus, rapid socio-environmental changes appear to be strongly associated with
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the development of diabetes. Most striking examples of environmental influences on diabetes are provided by the population of the Pacific island Nauru, the urbanized people of Papua New Guinea and Pima Indians [4–6]. In these populations, diabetes was virtually unknown 50 years ago, but now it affects approximately 40% of the adult populations. The marked increases in the prevalence of diabetes in parallel with modernization in the populations mentioned above could be explained by ‘‘thrifty genotype hypothesis’’ [7]. During the past 20–30 years, remarkable socioeconomic changes have occurred in South Korean society with respect to the economy, work force structure, urbanization, dietary patterns, physical activity and demographic structure. The economy of South Korea has grown impressively during the decades following the Korean War (1950–1953). Furthermore, urbanization in South Korea has increased about five-fold, which outstrips those experienced by other developing countries [8]. This unique socio-economic environment offers a suitable background for the analysis of the influence of socio-economic development on community disease profiles, including diabetes. Unfortunately, no longitudinal data exist on the incidence or prevalence of diabetes in a representative South Korean population, although published data from several community surveys are available [9–12]. However, mortality data is readily available and this data has the advantage of being comprehensive and utilizing a standard nomenclature [13]. Therefore, diabetes-related mortality might reflect the prevalence of diabetes, although there are many limitations and bias [13]. In this study, using summarized data reported by Korea National Statistical Office (KNSO) and Korean government, we examined the trend of changes in diabetesrelated mortality rate and socio-environmental factors in South Korea during the last two decades.
2. Materials and methods 2.1. Mortality data We re-analyzed the annual reports on mortality in South Korea by KNSO for the period from 1983 to 2001. Mortality statistics are posted in the web site of the KNSO; http:// www.nso.go.kr/eng [14]. Mortality statistics of KNSO cover virtually all death occurred in Koreans living in South Korea, including children and adolescents. Mortality records with unknown age at death were excluded (0.00001% of the total deaths during the study period). We used the crude numbers of death and death rate per 100,000 persons of each year, which were classified by age and cause of death. Using direct method
[15], we adjusted crude diabetes-related mortality rate of each year by age. South Korean national population of the year 1992, which was the median of study period, was used as standard for the adjustment. In terms of cause-of-death statistics, the underlying causes of death, i.e., the disease or injury that initiated the sequence of events that led to death, were used to count and rank leading causes of death in the manner recommended by the World Health Organization [16]. Diseases were classified according to the Korean Standard Classification of Causes of Death [17], which is based on the World Health Organization’s International Statistical Classification of Diseases, Injuries and Causes of Death (ICD-10) [16]. Causes of death ascribed to diabetes were determined by instructions of U.S. National Center for Health Statistics (http://www.cdc.gov/nchs/about/ major/dvs/im.htm). The actual ICD-10 codes of diseases classified to diabetes-related death in Korea were: (i) certain infectious and parasitic diseases (ICD-10 codes: A400-9, A410-9, A46, A480, A499, B010-2, B018, B019, B020-3, B027-9, B99), (ii) diseases of the blood and of blood-forming organs, and certain disorders involving the immune mechanism (D500-9, D531-9, D65, D683-4, D688-9, D728-9, D751-2, D758, D892), (iii) endocrine, nutritional and metabolic diseases (E100-E149, E15, E161-2, E208-15, E222, E233, E261, E26872, E274-89, E300-9, E311, E318-9, E348-9, E511-2, E518-9, E52, E538-9, E550, E559, E750-6, E769-889), (iv) mental and behavioral disorders (F010-9, F050-9, F060-9, F078-9, F09, F430-9, F450-9, F480, F501-9), (v) disorders of the nervous system (G248-9, G250-9, G318-9, G441-8, G470-9, G570-9, G580, G587-9, G628-9, G64, G700, G708-9, G711, G908-9), (vi) disorders of the eye and adnexa (H264, H269, H300-2, H308-9, H350), (vii) disease of the circulatory system (I250-9, I260, I288, I300-I520, I670-9, I700-I790, I800-I879, I950-9), (viii) diseases of the respiratory system (J00-069, J120-189, J200-J22, J40, J80-1, J850-3, J90-J949), (ix) diseases of the digestive system (K112-3, K149, K250-K3190, K550-K639, K650, K658-9, K710-K769, K810-869), (x) diseases of the skin and subcutaneous tissue (L020-089, L123, L300, L304, L308-9, L88-9), (xi) diseases of the musculoskeletal system and connective tissue (M218, M611, M614-5, M619, M725, M808-9, M818-9), (xii) diseases of the genitourinary system (N000-069, N10-N159, N17-N19, N25-N289, N300-N399, N72-N768) and (xiii) certain conditions originating in the perinatal period (P282, P90-P969). For inter-country comparison of diabetes-related mortality, we used the Organization for Economic Cooperation and Development (OECD) mortality data at http://www.oecd.org [18], which were age-standardized using the total OECD population for 1980 as the reference population (detailed description for the method is available at http://www.irdes.fr/ecosante/OCDE/112000.html). 2.2. Socio-economic data In terms of quantifying economic trends, we used national income data from the Bank of Korea official estimates for gross domestic product (GDP) per capita [19]. For data on the work force structure, the proportions of individuals employed
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by industry type were obtained from the Annual Report on the Economically Active Population Survey [20]. The proportions of the population involved in agriculture-, forestry- and fishery-related work were used to represent energy-intensive primary rural industry, and the proportions involved in production, transportation and equipment operation represented secondary industry. On the other hand, sedentary tertiary industry included professional, technical, administrative and managerial workers, clerical and related workers, sales workers and service workers. Urbanization ratios (the proportion of the population living in urban areas) were obtained from the Statistical Yearbook of Transportation [21]. 2.3. Physical activity data In this study, instead of direct measurement of physical activity, we used indirect proxies of physical activity, such as motor vehicle utilization or leisure activities. The number of private cars per year was obtained from the Statistical Yearbook of Transportation [21]. In terms of leisure activity trends, we used the Social Statistics Survey report issued by the Korea National Statistical Office [22]. The number of personal computers was taken from the Statistical Yearbook of the Information and Communication Industry; data was available from 1992 and thereafter [23]. 2.4. Diet data Most of the dietary intake data were collected and analyzed by National Nutrition Survey, which was conducted annually by the Ministry of Health and Welfare from 1983 to 1995. Thereafter, the survey was conducted in 3-year intervals (in 1995, 1998 and 2001) [24]. For dietary intake data per capita per day, trained interviewers detailed all food consumed at home in surveyed homes for 2 consecutive days, and thus the figures present problems of inaccuracy concerning recall and underestimation due to eating out. For this reason, we also analyzed dietary supply per capita per day; these figures were calculated on a nationwide basis using food production, import, export figures, etc. Total energy, protein and fat supply values were taken from the food balance sheet issued by the Korea Rural Economics Institute. Nutrient values were calculated using a food-composition table issued by the Rural Development Administration and the Rural Nutrition Institute [25].
3. Results 3.1. Trends of diabetes-related mortality Fig. 1 shows age-adjusted diabetes- and infectionrelated mortality during 1983–2001. The deaths from infectious diseases per 100,000 people decreased from 29.0 in 1983 to 9.5 in 2001. In contrast, the deaths from diabetes per 100,000 people increased
Fig. 1. Age-adjusted death rate related to diabetes and infection in Korea (1983–2001).
from 5.3 in 1983 to 18.4 in 2001 (3.5-fold increase). The increase in diabetes-related mortality was strikingly higher in the elderly (>65 years of age) (data not shown). The percentages of elderly (>65 years of age) among total crude diabetes-related deaths per year were 31.7% in 1983, 67.2% in 1993 and 86.7% in 2001 (data not shown). Although it might be difficult to directly compare crude mortality rates from different countries, we thought it would be possible to examine the temporal trends of changes in mortality rates in a given country. As shown in Table 1, the magnitude of the increase in diabetes-related mortality in South Korea was much greater than that of other developed countries, such as Table 1 Age-adjusted diabetes-related mortality rates of South Korea, Japan, the United Kingdom and the United States (1985–2000) Year
South Korea
Japan
UK
1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000
10.8 11.1 11.2 10.8 13.7 16.6 17.8 21.2 27.3 28.9 28.8 28.3 29.7 32.8 33.4 33.7
7.9 7.5 7.3 7.4 6.8 6.7 6.6 6.5 6.5 6.7 8.4 7.3 6.8 6.7 6.6 6.1
10.3 10.8 10.3 10.3 10.3 10.1 10.1 10.0 8.0 7.6 7.8 7.5 7.3 7.3 7.5 7.5
(1.00) (1.02) (1.03) (1.00) (1.26) (1.53) (1.64) (1.96) (2.52) (2.67) (2.66) (2.62) (2.75) (3.03) (3.09) (3.12)
(1.00) (0.94) (0.92) (0.93) (0.86) (0.84) (0.83) (0.82) (0.82) (0.84) (1.06) (0.92) (0.86) (0.84) (0.83) (0.77)
USA (1.00) (1.04) (1.00) (1.00) (1.00) (0.98) (0.98) (0.97) (0.77) (0.73) (0.75) (0.72) (0.70) (0.70) (0.72) (0.72)
14.3 14.1 14.4 14.8 16.9 17.1 17.2 17.3 18.2 18.9 19.5 20.0 19.9 20.1 – –
(1.00) (0.98) (1.01) (1.03) (1.18) (1.19) (1.20) (1.21) (1.27) (1.32) (1.36) (1.39) (1.39) (1.40)
Data shown as death rate per 100,000 persons of each year (fold increase from 1985).
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Fig. 2. Trends of changes in socio-economic factors in South Korea. The urbanization ratios means the proportion of the population living in urban areas (the population living in urban areas/the total population 100).
Japan, the United States and the United Kingdom over the same period (1985–2000) (Table 1). 3.2. Socio-economic transition As shown in Fig. 2, the GDP of South Korea increased by more than five-fold from US$ 82.3 billion in 1983 to US$ 427.3 billion in 2001. This increase in GDP was associated with changes in the structure of the work force, the urbanization rate and the ageing index. Energy-intensive occupations in rural primary industries, such as agriculture, forestry and fisheries reduced (data not shown), and those employed in the service industry continuously increased. In 1983, nearly 30.0% of the economically active population worked in the rural primary sector, but in 2001 only 10.3% had similar work, while about 70% of them worked in tertiary industry. The urbanization ratio increased from 73.3% in 1983 to 88.1% in 2001 (Fig. 2).
Fig. 3. Trends of changes in proxies for physical activities among South Koreans.
The numbers of personal computers increased from 314,000 in 1993 to 1,346,000 in 2001 (Fig. 3). 3.4. Nutritional changes Fig. 4 shows food energy intake and supply changes over the past 20 years. Although overall total energy intake reduced slightly from 2012 kcal per capita per day in 1983 to 1976 kcal in 2001, consumption patterns have changed. The percentage of plant–food intake reduced from 75.0% in 1983 to 56.0% in 2001, but the percentage of animal protein intake increased from
3.3. Changes of indirect measures of physical activity In parallel with urbanization, marked increases occurred in private car ownership, which increased from 293,000 in 1983 to 8,588,000 in 2001 (Fig. 3), and the number of persons per private car reduced from 136.1 in 1983 to 5.5 in 2001. For the type of leisure activity, the proportion of people enjoying dynamic activity, such as sports was slightly decreased (data not shown), but the proportion of static leisure activity, such as watching TV marked increased (from 24.5% in 1990 to 62.7% in 2000). Time spent viewing television per week in 2001 was 72.0% higher than that of 1983 (from 13.8 to 23.7 h/ week) (Fig. 3), and this was particularly prominent among 15–19 year olds of both sexes (data not shown).
Fig. 4. Trends of changes in diet factors in South Korea: (A) energy intake and (B) energy supply.
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33.5% to 47.9%, and fat intake increased from 23.5 to 41.6 g per day over the same period (Fig. 4A). In terms of food energy supply, total supply increased gradually from 2622 kcal in 1983 to 2994 kcal in 2001, and total protein and the percentage animal protein consumed increased gradually. In particular, fat supply increased remarkably from 47.1 g in 1983 to 84.0 g in 2001 (Fig. 4B). 4. Discussion As previously described as ‘‘epidemiologic transition’’ [26,27], we found a similar phenomenon in South Korea in that the death rate associated with communicable diseases decreased while those associated with diabetes, one of the chronic non-communicable diseases, increased with the advent of westernization and industrialization. Indeed, diabetes-related mortalities were not included among major leading causes of death in 1983 in South Korea, but in 2001 they ranked as the fourth leading cause of death, following malignancy, cerebrovascular disease and cardiovascular disease [28]. The major socio-economic changes in South Korea during the last two decades are characterized by a marked increase in GDP and rapid urbanization. As this socio-economic transition progressed, South Koreans tended to reduce physical activity levels and increase animal food consumption and dietary fat intake. Physical inactivity is a well-established risk factor of diabetes [29,30]. The shift from energyintensive primary rural industry to occupations in services and manufacturing as shown in this study is known to be associated with a major reduction in the amount of energy expended at work [31–33]. Along with the work force structural changes, the remarkably rapid urbanization witnessed in South Korea has led to a dramatic increase in private car ownership, and an increase in subway and bus transportation, and these changes may have led to a remarkable reduction in physical activity. The nutrition transition in South Korea has been already reported elsewhere [34]. In this study, although the total energy intake and the total energy supply mismatched, the animal protein and fat intake increased continuously. In accordance with reduced physical activity, the nutrition transition in South Korea might contribute to increased prevalence of obesity. According to Korean National Nutrition Surveys and the National Health and Nutrition Interview Survey, the prevalence of overweight (defined as BMI 25–29.9 kg/ m2) among people older than 20 years increased from
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23.9% in 1998 to 27.4% in 2001, and obesity (BMI > 30 kg/m2) increased from 2.4% to 3.2% over the same period [35]. We can speculate that the thrifty genes [7] might contribute to the increase of the prevalence of diabetes and its related mortality through interactions with prior exposure to the rapid environmental changes. However, we could not provide evidence for the causal relationship between socio-environmental changes and a sharp increase in diabetesrelated mortality owing to the atemporal approach used in this study. The magnitude of increase in the diabetes-related mortality in Korea was much greater than that of other developed countries in the same period. This can be explained by ‘‘thrifty phenotype hypothesis’’, which proposes that the epidemiological associations between poor fetal and infant growth and the subsequent development of type 2 diabetes and the metabolic syndrome result from the effects of poor nutrition in early life [36]. Since Korean people experienced malnutrition during Japanese occupation (1909–1945) and the Korean War (1950–1953), babies born in that period might have acquired a thrifty phenotype and subsequently have become more susceptible to diabetes and its complication than the other ethnic groups. This study has limitations related to the general problems in using national mortality statistics; the reliability and validity of cause of death, inaccuracy of diagnoses, variation in interpreting causal sequences and conditions contributing to death, changing perceptions of the causal role of diseases and lack of training in death certificate completion [37]. The causes of death ascribed to diabetes-related mortality were numerous and some might be non-specific. Therefore, the diabetes-related mortality in Korea could be overestimated. However, it would be a good surrogate reflecting the prevalence of diabetes during the study period. Indeed, the prevalence of diabetes directly observed from independent cohorts in Korea increased with time: the prevalence of diabetes aged 30 was 8.5% in 2001 [24], which was higher than in previous studies, i.e., 7.2% in 1993 [9] and 7.7% in 1997 [10]. We hereby showed that the rapidly increasing diabetes-related mortality came along with rapidly changing socio-environmental factors. Although the cost-effectiveness and clinical outcome are not known, intensive lifestyle modification can prevent or delay the onset of diabetes [38,39]. Considering the huge burden of diabetes and its related complications, multidirec-
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tional efforts including lifestyle interventions should be exercised in the South Korean society. Acknowledgements This work was supported by a grant from the Korea Health 21 R&D Project, Ministry of Health & Welfare, Republic of Korea (02-PJ1-PG1-CH04-0001). We thank Bu-Youn Kim, for help in gathering information from National Statistical Office. Also, the authors deeply thank two anonymous reviewers for their helpful comments. References [1] P. Zimmet, K.G. Alberti, J. Shaw, Global and societal implication of the diabetes epidemic, Nature 414 (2001) 782–787. [2] W.Y. Fujimoto, R.W. Bergstrom, E.J. Boyko, J.L. Kinyoun, D.L. Leonetti, L.L. Newell-Morris, et al., Diabetes and diabetes risk factors in second- and third-generation Japanese Americans in Seattle, Washington, Diab. Res. Clin. Pract. 24 (1994) S43–S52. [3] W.Y. Fujimoto, R.W. Bergstrom, E.J. Boyko, K. Chen, S.E. Kahn, D.L. Leonetti, et al., Type 2 diabetes and the metabolic syndrome in Japanese Americans, Diab. Res. Clin. Pract. 24 (2000) S73–S76. [4] P. Zimmet, G. Dowse, C. Finch, S. Serjeantson, H. King, The epidemiology and natural history of NIDDM: lessons from the South Pacific, Diab. Metab. Rev. 6 (1990) 91–124. [5] D. Simmons, The epidemiology of diabetes and its complications in New Zealand, Diab. Med. 13 (1996) 371–375. [6] H. King, M. Rewers, Global estimates for prevalence of diabetes mellitus and impaired glucose tolerance in adults, WHO Ad. Hoc. Diabetes Reporting Group, Diab. Care 16 (1993) 157–177. [7] J.V. Neel, Diabetes mellitus: a ‘‘thrifty’’ genotype rendered detrimental by ‘‘progress’’? Am. J. Hum. Genet. 14 (1962) 353–362. [8] M.G. Kang, Understanding urban problems in Korea: continuity and change, Dev. Soc. 17 (1998) 99–120. [9] Y. Park, H. Lee, C.S. Koh, H. Min, K. Yoo, Y. Kim, et al., Prevalence of diabetes and IGT in Yonchon County, South Korea, Diab. Care 18 (1995) 545–548. [10] C.S. Shin, H.K. Lee, C.S. Koh, Y.I. Kim, Y.S. Shin, K.Y. Yoo, et al., Risk factors for the development of NIDDM in Yonchon County, Korea, Diab. Care 20 (1997) 1842–1846. [11] J.Y. Park, Y.I. Kim, C.S. Choi, Y.E. Chung, S.W. Kim, M.S. Lee, et al., Prevalence of diabetes, impaired glucose tolerance, and impaired fasting glucose in a rural population of Korea, according to 1997 American Diabetes Association and 1985 World Health Organization Criteria, Diab. Care 23 (2000) 707–708. [12] J.Y. Oh, Y.S. Hong, Y.A. Sung, E. Barrett-Connor, Prevalence and factor analysis of metabolic syndrome in an urban Korean population, Diab. Care 27 (2004) 2027–2032. [13] N.E. Stroup, Sources of Routinely Collected Data for Surveillance: In Principle and Practice of Public Health Surveillance, Oxford Univ. Press, 1994, pp. 53–68. [14] Korea National Statistical Office, Annual Report on the Vital Statistics in Korea, Seoul Government Printing, 1983–2001. [15] H.S. Shyyock, J.S. Siegal, The Method and Materials of Demography, Academic Press, NewYork, NY, 1976, pp. 1103–1126. [16] Internal Classification of Disease, 10th revision, Genova, Switzerland World Health Organization, 2003.
[17] Korea National Statistical Office, The Korean Standard Classification of Disease and Cause of Death, Seoul Government Printing, 2003. [18] OECD Health Data 2004 [article on line], Available from http:// www.oecd.org/document/44/ 0,2340,en_2649_201185_2085228_1_1_1_1,00, Accessed 24 September, 2004. [19] Korea National Statistical Office, Korean Statistical Yearbook, Seoul Government Printing, 1983–2001. [20] Korea National Statistical Office, Annual Report on the Economically Active Population Survey in Korea, Seoul Government Printing, 1983–2001. [21] Ministry of Construction and Transportation, Statistical Yearbook of Transportation, Seoul Government Printing, 1983–2001 . [22] Korea National Statistical Office, Report on the Social Statistics Survey in Korea, Seoul Government Printing, 2000. [23] Electronic Industries Association of Korea, Statistical Yearbook of Information & Communication Industry in Korea, Seoul Government Printing, 2002. [24] Ministry of Health and Social Affairs, Yearbook of Health and Social Statistics, Seoul Government Printing, 1983–2001. [25] Korean Rural Economics Institute, Food Balance Sheet, Seoul Government Printing, 1983–2001. [26] A.R. Omran, The epidemiologic transition: a theory of the epidemiology of population change, Millbank Mem. Fund. Q. 49 (1971) 509–538. [27] A.R. Omran, The epidemiologic transition theory: a preliminary update, J. Trop. Pediatr. 29 (1983) 305–316. [28] National Statistical Office, Yearbook of Cause of Death Statistics in Korea, Seoul Government Printing, 2001. [29] J.E. Manson, E.B. Rimm, M.J. Stampfer, G.A. Colditz, W.C. Willett, W.C. Krolewski, et al., Physical activity and incidence of non-insulin-dependent diabetes mellitus in women, Lancet 338 (1991) 774–778. [30] J.E. Manson, D.M. Nathan, A.S. Krolewski, M.J. Stampfer, W.C. Willett, C.H. Hennekens, A prospective study of exercise and incidence of diabetes among US male physicians, JAMA 268 (1992) 63–67. [31] B.M. Popkin, The nutrition transition and its health implications in lower-income countries, Public Health Nutr. 1 (1998) 5–21. [32] B.M. Popkin, C.M. Doak, The obesity epidemic is a worldwide phenomenon, Nutr. Rev. 56 (1998) 106–114. [33] B. Caballero, Introduction Symposium: obesity in developing countries: biological and ecological factors, J. Nutr. 131 (2001) 866S–870S. [34] S.W. Kim, S.J. Moon, B.M. Popkin, The nutrition transition in South Korea, Am. J. Clin. Nutr. 71 (2000) 44–53. [35] Ministry of Health and Welfare, 2001 National Health And Nutrition Survey, Health Examination, 2002. [36] C.N. Hales, D.J. Barker, The thrifty phenotype hypothesis, Br. Med. Bull. 60 (2001) 5–20. [37] K.A. Park, Recent trends and patterns of mortality in Korea, Dev. Soc. 27 (1998) 67–81. [38] J. Tuomilehto, J. Lindstrom, J.G. Eriksson, T.T. Valle, H. Hamalainen, P. Ilanne-Parikka, et al., The Finnish Diabetes Prevention Study Group, Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance, N. Engl. J. Med. 344 (2001) 1343–1350. [39] Diabetes Prevention Program Research Group, Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin, N. Engl. J. Med. 346 (2002) 393–403.
Rapidly increasing diabetes-related mortality with socio-environmental changes in South Korea during the last two decades Young Ju Choi 1, Young Min Cho 1, Chul Ku Park, Hak Chul Jang, Kyong Soo Park, Seong Yeon Kim, Hong Kyu Lee * Department of Internal Medicine, Seoul National University College of Medicine, 28 Yongon-dong Chongno-gu, Seoul 110-744, Republic of Korea Received 3 August 2005; accepted 30 March 2006 Available online 16 May 2006
Abstract Diabetes mellitus is the result of complex interactions involving many genes and environmental factors, and rapid socioenvironmental changes have been strongly associated with the development of diabetes. In this study, we examined the trends in diabetes mortality and associated socio-environmental changes that have occurred in South Korea over the last 20 years. Data from a national database and government reports for the years from 1983 to 2001 were analyzed. The data included mortality, socioeconomic changes, physical activity and dietary pattern indicators. Deaths from diabetes per 100,000 people increased from 5.3 in 1983 to 18.4 in 2001. Along with increasing diabetes-related mortality, many socio-economic indices (gross domestic production, proportion of tertiary industry and urbanization rate), proxies for physical activity (numbers of cars and time spent watching television) and diet indices (animal protein intake and fat intake) showed remarkable changes. To counter increasing prevalence of diabetes and its related mortality in South Korea, multidirectional efforts including lifestyle modification should be mandatory features of future public health policy. # 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Diabetes mellitus; Mortality; Korea; Socio-environmental change
1. Introduction The worldwide prevalence of diabetes mellitus has risen dramatically over the past two decades. Globally, the number of people with diabetes is expected to rise
Abbreviations: GDP, gross domestic product; ICD-10, Internal Classification of Disease, Injuries and Causes of Death, 10th revision; KNSO, Korea National Statistical Office; OECD, Organization for Economic Cooperation and Development * Corresponding author. Tel.: +82 2 2072 2266; fax: +82 2 762 9662. E-mail address: [email protected] (H.K. Lee). 1 They equally contributed to this work.
from the current estimate of 150–220 million in 2010 and 300 million in 2025 [1]. Diabetes is the result of complex interactions involving many genes and environmental factors. Evidence that exposure to certain environmental factors influences the development of diabetes, especially type 2 diabetes, is provided by studies on migrant populations. For example, Japanese Americans living in Seattle had a higher prevalence of type 2 diabetes than the Japanese living in Japan, which could be explained by increased visceral adiposity and insulin resistance associated with a westernized lifestyle [2,3]. Thus, rapid socio-environmental changes appear to be strongly associated with
0168-8227/$ – see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.diabres.2006.03.029
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the development of diabetes. Most striking examples of environmental influences on diabetes are provided by the population of the Pacific island Nauru, the urbanized people of Papua New Guinea and Pima Indians [4–6]. In these populations, diabetes was virtually unknown 50 years ago, but now it affects approximately 40% of the adult populations. The marked increases in the prevalence of diabetes in parallel with modernization in the populations mentioned above could be explained by ‘‘thrifty genotype hypothesis’’ [7]. During the past 20–30 years, remarkable socioeconomic changes have occurred in South Korean society with respect to the economy, work force structure, urbanization, dietary patterns, physical activity and demographic structure. The economy of South Korea has grown impressively during the decades following the Korean War (1950–1953). Furthermore, urbanization in South Korea has increased about five-fold, which outstrips those experienced by other developing countries [8]. This unique socio-economic environment offers a suitable background for the analysis of the influence of socio-economic development on community disease profiles, including diabetes. Unfortunately, no longitudinal data exist on the incidence or prevalence of diabetes in a representative South Korean population, although published data from several community surveys are available [9–12]. However, mortality data is readily available and this data has the advantage of being comprehensive and utilizing a standard nomenclature [13]. Therefore, diabetes-related mortality might reflect the prevalence of diabetes, although there are many limitations and bias [13]. In this study, using summarized data reported by Korea National Statistical Office (KNSO) and Korean government, we examined the trend of changes in diabetesrelated mortality rate and socio-environmental factors in South Korea during the last two decades.
2. Materials and methods 2.1. Mortality data We re-analyzed the annual reports on mortality in South Korea by KNSO for the period from 1983 to 2001. Mortality statistics are posted in the web site of the KNSO; http:// www.nso.go.kr/eng [14]. Mortality statistics of KNSO cover virtually all death occurred in Koreans living in South Korea, including children and adolescents. Mortality records with unknown age at death were excluded (0.00001% of the total deaths during the study period). We used the crude numbers of death and death rate per 100,000 persons of each year, which were classified by age and cause of death. Using direct method
[15], we adjusted crude diabetes-related mortality rate of each year by age. South Korean national population of the year 1992, which was the median of study period, was used as standard for the adjustment. In terms of cause-of-death statistics, the underlying causes of death, i.e., the disease or injury that initiated the sequence of events that led to death, were used to count and rank leading causes of death in the manner recommended by the World Health Organization [16]. Diseases were classified according to the Korean Standard Classification of Causes of Death [17], which is based on the World Health Organization’s International Statistical Classification of Diseases, Injuries and Causes of Death (ICD-10) [16]. Causes of death ascribed to diabetes were determined by instructions of U.S. National Center for Health Statistics (http://www.cdc.gov/nchs/about/ major/dvs/im.htm). The actual ICD-10 codes of diseases classified to diabetes-related death in Korea were: (i) certain infectious and parasitic diseases (ICD-10 codes: A400-9, A410-9, A46, A480, A499, B010-2, B018, B019, B020-3, B027-9, B99), (ii) diseases of the blood and of blood-forming organs, and certain disorders involving the immune mechanism (D500-9, D531-9, D65, D683-4, D688-9, D728-9, D751-2, D758, D892), (iii) endocrine, nutritional and metabolic diseases (E100-E149, E15, E161-2, E208-15, E222, E233, E261, E26872, E274-89, E300-9, E311, E318-9, E348-9, E511-2, E518-9, E52, E538-9, E550, E559, E750-6, E769-889), (iv) mental and behavioral disorders (F010-9, F050-9, F060-9, F078-9, F09, F430-9, F450-9, F480, F501-9), (v) disorders of the nervous system (G248-9, G250-9, G318-9, G441-8, G470-9, G570-9, G580, G587-9, G628-9, G64, G700, G708-9, G711, G908-9), (vi) disorders of the eye and adnexa (H264, H269, H300-2, H308-9, H350), (vii) disease of the circulatory system (I250-9, I260, I288, I300-I520, I670-9, I700-I790, I800-I879, I950-9), (viii) diseases of the respiratory system (J00-069, J120-189, J200-J22, J40, J80-1, J850-3, J90-J949), (ix) diseases of the digestive system (K112-3, K149, K250-K3190, K550-K639, K650, K658-9, K710-K769, K810-869), (x) diseases of the skin and subcutaneous tissue (L020-089, L123, L300, L304, L308-9, L88-9), (xi) diseases of the musculoskeletal system and connective tissue (M218, M611, M614-5, M619, M725, M808-9, M818-9), (xii) diseases of the genitourinary system (N000-069, N10-N159, N17-N19, N25-N289, N300-N399, N72-N768) and (xiii) certain conditions originating in the perinatal period (P282, P90-P969). For inter-country comparison of diabetes-related mortality, we used the Organization for Economic Cooperation and Development (OECD) mortality data at http://www.oecd.org [18], which were age-standardized using the total OECD population for 1980 as the reference population (detailed description for the method is available at http://www.irdes.fr/ecosante/OCDE/112000.html). 2.2. Socio-economic data In terms of quantifying economic trends, we used national income data from the Bank of Korea official estimates for gross domestic product (GDP) per capita [19]. For data on the work force structure, the proportions of individuals employed
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by industry type were obtained from the Annual Report on the Economically Active Population Survey [20]. The proportions of the population involved in agriculture-, forestry- and fishery-related work were used to represent energy-intensive primary rural industry, and the proportions involved in production, transportation and equipment operation represented secondary industry. On the other hand, sedentary tertiary industry included professional, technical, administrative and managerial workers, clerical and related workers, sales workers and service workers. Urbanization ratios (the proportion of the population living in urban areas) were obtained from the Statistical Yearbook of Transportation [21]. 2.3. Physical activity data In this study, instead of direct measurement of physical activity, we used indirect proxies of physical activity, such as motor vehicle utilization or leisure activities. The number of private cars per year was obtained from the Statistical Yearbook of Transportation [21]. In terms of leisure activity trends, we used the Social Statistics Survey report issued by the Korea National Statistical Office [22]. The number of personal computers was taken from the Statistical Yearbook of the Information and Communication Industry; data was available from 1992 and thereafter [23]. 2.4. Diet data Most of the dietary intake data were collected and analyzed by National Nutrition Survey, which was conducted annually by the Ministry of Health and Welfare from 1983 to 1995. Thereafter, the survey was conducted in 3-year intervals (in 1995, 1998 and 2001) [24]. For dietary intake data per capita per day, trained interviewers detailed all food consumed at home in surveyed homes for 2 consecutive days, and thus the figures present problems of inaccuracy concerning recall and underestimation due to eating out. For this reason, we also analyzed dietary supply per capita per day; these figures were calculated on a nationwide basis using food production, import, export figures, etc. Total energy, protein and fat supply values were taken from the food balance sheet issued by the Korea Rural Economics Institute. Nutrient values were calculated using a food-composition table issued by the Rural Development Administration and the Rural Nutrition Institute [25].
3. Results 3.1. Trends of diabetes-related mortality Fig. 1 shows age-adjusted diabetes- and infectionrelated mortality during 1983–2001. The deaths from infectious diseases per 100,000 people decreased from 29.0 in 1983 to 9.5 in 2001. In contrast, the deaths from diabetes per 100,000 people increased
Fig. 1. Age-adjusted death rate related to diabetes and infection in Korea (1983–2001).
from 5.3 in 1983 to 18.4 in 2001 (3.5-fold increase). The increase in diabetes-related mortality was strikingly higher in the elderly (>65 years of age) (data not shown). The percentages of elderly (>65 years of age) among total crude diabetes-related deaths per year were 31.7% in 1983, 67.2% in 1993 and 86.7% in 2001 (data not shown). Although it might be difficult to directly compare crude mortality rates from different countries, we thought it would be possible to examine the temporal trends of changes in mortality rates in a given country. As shown in Table 1, the magnitude of the increase in diabetes-related mortality in South Korea was much greater than that of other developed countries, such as Table 1 Age-adjusted diabetes-related mortality rates of South Korea, Japan, the United Kingdom and the United States (1985–2000) Year
South Korea
Japan
UK
1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000
10.8 11.1 11.2 10.8 13.7 16.6 17.8 21.2 27.3 28.9 28.8 28.3 29.7 32.8 33.4 33.7
7.9 7.5 7.3 7.4 6.8 6.7 6.6 6.5 6.5 6.7 8.4 7.3 6.8 6.7 6.6 6.1
10.3 10.8 10.3 10.3 10.3 10.1 10.1 10.0 8.0 7.6 7.8 7.5 7.3 7.3 7.5 7.5
(1.00) (1.02) (1.03) (1.00) (1.26) (1.53) (1.64) (1.96) (2.52) (2.67) (2.66) (2.62) (2.75) (3.03) (3.09) (3.12)
(1.00) (0.94) (0.92) (0.93) (0.86) (0.84) (0.83) (0.82) (0.82) (0.84) (1.06) (0.92) (0.86) (0.84) (0.83) (0.77)
USA (1.00) (1.04) (1.00) (1.00) (1.00) (0.98) (0.98) (0.97) (0.77) (0.73) (0.75) (0.72) (0.70) (0.70) (0.72) (0.72)
14.3 14.1 14.4 14.8 16.9 17.1 17.2 17.3 18.2 18.9 19.5 20.0 19.9 20.1 – –
(1.00) (0.98) (1.01) (1.03) (1.18) (1.19) (1.20) (1.21) (1.27) (1.32) (1.36) (1.39) (1.39) (1.40)
Data shown as death rate per 100,000 persons of each year (fold increase from 1985).
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Fig. 2. Trends of changes in socio-economic factors in South Korea. The urbanization ratios means the proportion of the population living in urban areas (the population living in urban areas/the total population 100).
Japan, the United States and the United Kingdom over the same period (1985–2000) (Table 1). 3.2. Socio-economic transition As shown in Fig. 2, the GDP of South Korea increased by more than five-fold from US$ 82.3 billion in 1983 to US$ 427.3 billion in 2001. This increase in GDP was associated with changes in the structure of the work force, the urbanization rate and the ageing index. Energy-intensive occupations in rural primary industries, such as agriculture, forestry and fisheries reduced (data not shown), and those employed in the service industry continuously increased. In 1983, nearly 30.0% of the economically active population worked in the rural primary sector, but in 2001 only 10.3% had similar work, while about 70% of them worked in tertiary industry. The urbanization ratio increased from 73.3% in 1983 to 88.1% in 2001 (Fig. 2).
Fig. 3. Trends of changes in proxies for physical activities among South Koreans.
The numbers of personal computers increased from 314,000 in 1993 to 1,346,000 in 2001 (Fig. 3). 3.4. Nutritional changes Fig. 4 shows food energy intake and supply changes over the past 20 years. Although overall total energy intake reduced slightly from 2012 kcal per capita per day in 1983 to 1976 kcal in 2001, consumption patterns have changed. The percentage of plant–food intake reduced from 75.0% in 1983 to 56.0% in 2001, but the percentage of animal protein intake increased from
3.3. Changes of indirect measures of physical activity In parallel with urbanization, marked increases occurred in private car ownership, which increased from 293,000 in 1983 to 8,588,000 in 2001 (Fig. 3), and the number of persons per private car reduced from 136.1 in 1983 to 5.5 in 2001. For the type of leisure activity, the proportion of people enjoying dynamic activity, such as sports was slightly decreased (data not shown), but the proportion of static leisure activity, such as watching TV marked increased (from 24.5% in 1990 to 62.7% in 2000). Time spent viewing television per week in 2001 was 72.0% higher than that of 1983 (from 13.8 to 23.7 h/ week) (Fig. 3), and this was particularly prominent among 15–19 year olds of both sexes (data not shown).
Fig. 4. Trends of changes in diet factors in South Korea: (A) energy intake and (B) energy supply.
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33.5% to 47.9%, and fat intake increased from 23.5 to 41.6 g per day over the same period (Fig. 4A). In terms of food energy supply, total supply increased gradually from 2622 kcal in 1983 to 2994 kcal in 2001, and total protein and the percentage animal protein consumed increased gradually. In particular, fat supply increased remarkably from 47.1 g in 1983 to 84.0 g in 2001 (Fig. 4B). 4. Discussion As previously described as ‘‘epidemiologic transition’’ [26,27], we found a similar phenomenon in South Korea in that the death rate associated with communicable diseases decreased while those associated with diabetes, one of the chronic non-communicable diseases, increased with the advent of westernization and industrialization. Indeed, diabetes-related mortalities were not included among major leading causes of death in 1983 in South Korea, but in 2001 they ranked as the fourth leading cause of death, following malignancy, cerebrovascular disease and cardiovascular disease [28]. The major socio-economic changes in South Korea during the last two decades are characterized by a marked increase in GDP and rapid urbanization. As this socio-economic transition progressed, South Koreans tended to reduce physical activity levels and increase animal food consumption and dietary fat intake. Physical inactivity is a well-established risk factor of diabetes [29,30]. The shift from energyintensive primary rural industry to occupations in services and manufacturing as shown in this study is known to be associated with a major reduction in the amount of energy expended at work [31–33]. Along with the work force structural changes, the remarkably rapid urbanization witnessed in South Korea has led to a dramatic increase in private car ownership, and an increase in subway and bus transportation, and these changes may have led to a remarkable reduction in physical activity. The nutrition transition in South Korea has been already reported elsewhere [34]. In this study, although the total energy intake and the total energy supply mismatched, the animal protein and fat intake increased continuously. In accordance with reduced physical activity, the nutrition transition in South Korea might contribute to increased prevalence of obesity. According to Korean National Nutrition Surveys and the National Health and Nutrition Interview Survey, the prevalence of overweight (defined as BMI 25–29.9 kg/ m2) among people older than 20 years increased from
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23.9% in 1998 to 27.4% in 2001, and obesity (BMI > 30 kg/m2) increased from 2.4% to 3.2% over the same period [35]. We can speculate that the thrifty genes [7] might contribute to the increase of the prevalence of diabetes and its related mortality through interactions with prior exposure to the rapid environmental changes. However, we could not provide evidence for the causal relationship between socio-environmental changes and a sharp increase in diabetesrelated mortality owing to the atemporal approach used in this study. The magnitude of increase in the diabetes-related mortality in Korea was much greater than that of other developed countries in the same period. This can be explained by ‘‘thrifty phenotype hypothesis’’, which proposes that the epidemiological associations between poor fetal and infant growth and the subsequent development of type 2 diabetes and the metabolic syndrome result from the effects of poor nutrition in early life [36]. Since Korean people experienced malnutrition during Japanese occupation (1909–1945) and the Korean War (1950–1953), babies born in that period might have acquired a thrifty phenotype and subsequently have become more susceptible to diabetes and its complication than the other ethnic groups. This study has limitations related to the general problems in using national mortality statistics; the reliability and validity of cause of death, inaccuracy of diagnoses, variation in interpreting causal sequences and conditions contributing to death, changing perceptions of the causal role of diseases and lack of training in death certificate completion [37]. The causes of death ascribed to diabetes-related mortality were numerous and some might be non-specific. Therefore, the diabetes-related mortality in Korea could be overestimated. However, it would be a good surrogate reflecting the prevalence of diabetes during the study period. Indeed, the prevalence of diabetes directly observed from independent cohorts in Korea increased with time: the prevalence of diabetes aged 30 was 8.5% in 2001 [24], which was higher than in previous studies, i.e., 7.2% in 1993 [9] and 7.7% in 1997 [10]. We hereby showed that the rapidly increasing diabetes-related mortality came along with rapidly changing socio-environmental factors. Although the cost-effectiveness and clinical outcome are not known, intensive lifestyle modification can prevent or delay the onset of diabetes [38,39]. Considering the huge burden of diabetes and its related complications, multidirec-
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tional efforts including lifestyle interventions should be exercised in the South Korean society. Acknowledgements This work was supported by a grant from the Korea Health 21 R&D Project, Ministry of Health & Welfare, Republic of Korea (02-PJ1-PG1-CH04-0001). We thank Bu-Youn Kim, for help in gathering information from National Statistical Office. Also, the authors deeply thank two anonymous reviewers for their helpful comments. References [1] P. Zimmet, K.G. Alberti, J. Shaw, Global and societal implication of the diabetes epidemic, Nature 414 (2001) 782–787. [2] W.Y. Fujimoto, R.W. Bergstrom, E.J. Boyko, J.L. Kinyoun, D.L. Leonetti, L.L. Newell-Morris, et al., Diabetes and diabetes risk factors in second- and third-generation Japanese Americans in Seattle, Washington, Diab. Res. Clin. Pract. 24 (1994) S43–S52. [3] W.Y. Fujimoto, R.W. Bergstrom, E.J. Boyko, K. Chen, S.E. Kahn, D.L. Leonetti, et al., Type 2 diabetes and the metabolic syndrome in Japanese Americans, Diab. Res. Clin. Pract. 24 (2000) S73–S76. [4] P. Zimmet, G. Dowse, C. Finch, S. Serjeantson, H. King, The epidemiology and natural history of NIDDM: lessons from the South Pacific, Diab. Metab. Rev. 6 (1990) 91–124. [5] D. Simmons, The epidemiology of diabetes and its complications in New Zealand, Diab. Med. 13 (1996) 371–375. [6] H. King, M. Rewers, Global estimates for prevalence of diabetes mellitus and impaired glucose tolerance in adults, WHO Ad. Hoc. Diabetes Reporting Group, Diab. Care 16 (1993) 157–177. [7] J.V. Neel, Diabetes mellitus: a ‘‘thrifty’’ genotype rendered detrimental by ‘‘progress’’? Am. J. Hum. Genet. 14 (1962) 353–362. [8] M.G. Kang, Understanding urban problems in Korea: continuity and change, Dev. Soc. 17 (1998) 99–120. [9] Y. Park, H. Lee, C.S. Koh, H. Min, K. Yoo, Y. Kim, et al., Prevalence of diabetes and IGT in Yonchon County, South Korea, Diab. Care 18 (1995) 545–548. [10] C.S. Shin, H.K. Lee, C.S. Koh, Y.I. Kim, Y.S. Shin, K.Y. Yoo, et al., Risk factors for the development of NIDDM in Yonchon County, Korea, Diab. Care 20 (1997) 1842–1846. [11] J.Y. Park, Y.I. Kim, C.S. Choi, Y.E. Chung, S.W. Kim, M.S. Lee, et al., Prevalence of diabetes, impaired glucose tolerance, and impaired fasting glucose in a rural population of Korea, according to 1997 American Diabetes Association and 1985 World Health Organization Criteria, Diab. Care 23 (2000) 707–708. [12] J.Y. Oh, Y.S. Hong, Y.A. Sung, E. Barrett-Connor, Prevalence and factor analysis of metabolic syndrome in an urban Korean population, Diab. Care 27 (2004) 2027–2032. [13] N.E. Stroup, Sources of Routinely Collected Data for Surveillance: In Principle and Practice of Public Health Surveillance, Oxford Univ. Press, 1994, pp. 53–68. [14] Korea National Statistical Office, Annual Report on the Vital Statistics in Korea, Seoul Government Printing, 1983–2001. [15] H.S. Shyyock, J.S. Siegal, The Method and Materials of Demography, Academic Press, NewYork, NY, 1976, pp. 1103–1126. [16] Internal Classification of Disease, 10th revision, Genova, Switzerland World Health Organization, 2003.
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