C. H. Chang* 1, W. Y. Shau 1, Y. D. Jiang* 1, H. Y. Li*, T. J. Chang*, W. H.-H. Sheu, C. F. Kwok**, L. T. Ho and L. M. Chuang* Abstract.

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1 DIABETICMedicine Original Article: Epidemiology Type 2 diabetes prevalence and incidence among adults in Taiwan during : a national health insurance data set study C. H. Chang* 1, W. Y. Shau 1, Y. D. Jiang* 1, H. Y. Li*, T. J. Chang*, W. H.-H. Sheu, C. F. Kwok**, L. T. Ho and L. M. Chuang* *Department of Internal Medicine, National Taiwan University Hospital, Institute of Preventive Medicine, College of Public Health, National Taiwan University, Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei, Division of Health Technology Assessment, Center for Drug Evaluation, Taipei, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, **Department of Medicine, Taipei Veterans General Hospital, and Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan Accepted 31 March 2010 DOI: /j x Abstract Aim To evaluate annual prevalence and incidence of Type 2 diabetes and to examine possible trends among adults in Taiwan. Methods A retrospective nationwide longitudinal study using the Taiwan National Health Insurance Research Database collected during Adult patients aged 20 years old with prevalent and incident Type 2 diabetes were identified using ICD-9-CM diagnostic codes. Age-specific and age-direct-standardized annual incidence and prevalence were calculated to describe their trends in different gender and age group and compared using Poisson regression. Results During the study years, the age-standardized prevalence of Type 2 diabetes increased from 4.7 to 6.5% for men and from 5.3 to 6.6% for women. The increasing trends in prevalence were significant and higher among people aged < 40 and 80 years. The age-standardized incidence rates of Type 2 diabetes per 1000 person-years were approximately 7.6 and remain stable for men, but decreasing from 7.7 to 6.9 for women. However, the incidence increased significantly in younger adults aged < 40 years whose relative incidence (RI with 95% confidence interval) was 1.31 ( ) for men and 1.04 ( ) for women. The incidence trends for people aged 40 years were decreased for men and women. The differences in incidence trends between age groups and between genders were all statistically significant (all P < 0.001). Conclusions This study demonstrated a substantial increasing trend in Type 2 diabetes prevalence during among adults in Taiwan. Despite the incidence decreased in older people, young men aged years were most susceptible to higher incidence of Type 2 diabetes. Diabet. Med. 27, (2010) Keywords epidemiology, incidence and prevalence, population-based, Taiwan, Type 2 diabetes Abbreviations CI, confidence interval; ICD-9-CM, International Classification of Diseases, 9th Revision, Clinical Modification; RI, relative incidence; RR, relative risk Introduction Type 2 diabetes is becoming a pandemic disorder and its alarming increase in prevalence raises significant concerns. The prevalence of diabetes for all age groups worldwide was estimated to be 2.8% in 2000 and is predicted to be 4.4% in Correspondence to: Dr. Lee-Ming Chuang, Department of Internal Medicine, National Taiwan University Hospital, 7 Chung-Shan South Road, Taipei, Taiwan leeming@ntu.edu.tw 1 These authors contribute equally to this work [1]. Consistently, several population-based studies conducted in the USA and Canada observed a significant increase in incidence, not only among the elderly, but also in the young population [2 6]. Together with the increased incidence, population ageing, changes in diagnostic criteria, increased interest in diagnosing and treating diabetic patients and declining mortality during the past decade also play important roles in this rise [7]. As a result of increased public awareness, intensive monitoring and aggressive management of diabetes has become more widespread. However, the overall decrease in rates of macrovascular and microvascular complications 636 Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

2 Original article DIABETICMedicine among diagnosed diabetic patients has not been consistently demonstrated in the recent literature [8 10]. Type 2 diabetes has become an important public health challenge in the Chinese population living in mainland China, Hong Kong, Taiwan and Singapore, which accounts for at least one-fifth of the global population [11 13]. Because of genetic susceptibility as well as rapid westernization of diet and lifestyle, a dramatic increase of Type 2 diabetes disease prevalence and incidence is expected [14,15]. In fact, it is estimated that, between 1995 and 2025, the prevalence and the number of people with diabetes will increase by 48 and 170%, respectively, in developing countries as compared with 27 and 42% in developed countries [16]. In contrast to developed countries, where the largest increase in the numbers of diabetic patients are the elderly population aged > 64 years, the majority of increases in developing countries will occur among members of the population aged years [1]. Furthermore, several studies also reported the emergence of a Type 2 diabetes epidemic in schoolchildren and adolescents [17,18]. However, these estimates were based on relatively small population studies with no or limited nationwide representativeness. This paucity of data limited the allocation of medical resources and policymaking. We therefore used the Taiwan National Health Insurance database to provide an estimate of nationwide prevalence and incidence of Type 2 diabetes and examine possible trends among adults in Taiwan. Patients and methods Data source A universal compulsory national health insurance programme was launched by the Taiwanese government in March 1995 [19]. By the end of 2005, it provided coverage for approximately 98% of the total population of 23 million in Taiwan. Although non- Chinese residents are also eligible for this programme, they only account for 1% of total beneficiaries. Large computerized administrative and claims data sets derived from this programme have been maintained on an ongoing basis by the National Health Research Institute of Taiwan and made available to investigators for research purposes after individual health information was de-identified. In this study, we used inpatient and outpatient claims data sets collected during The protocol of this study was approved by the National Taiwan University Hospital Research Ethics Committee, Taipei, Taiwan. Selection of cases Figure 1 shows the procedure for identification of adult patients 20 years with Type 2 diabetes. First, we searched the Taiwan National Health Insurance Database for the source population during to identify any hospitalized event with diabetes as one of the discharge diagnoses (The International Classification of Diseases, 9th Revision, Clinical Modification, ICD-9-CM code 250) and used outpatient claims to find any visit for diabetes (ICD-9-CM code 250 and A code A181). Patients were classified as having Type 2 diabetes and included in the analysis if they had at least one hospital admission with a diagnostic code of diabetes or three or more outpatient visits with a diabetes diagnostic code within 365 calendar days. This definition of diabetes was evaluated by a study sampling 9000 patients with a diagnosis of diabetes in National Health Insurance claims data in 2000 [20]. The accuracy of the diabetes diagnosis was assessed based on the patient s response to a questionnaire asking whether they were told by doctors that Adult subjects in the database fulfilling the criteria: (i) Having 3 outpatient visits with diabetes diagnosis within n = year but no hospital admission (ii) Having 1 hospital admission with diabetes diagnosis but no n = outpatient visit (iii)having 3 outpatient visits in 1 year and 1 hospital n = admission with diabetes diagnosis Total n = Excluded Potential type 1 diabetes n = Possible gestational diabetes only n = 4237 Gender or age information error n = 3348 Study subjects analysed Total Number of total prevalent patients Number of incident patients in Mean age at type 2 diabetes diagnosis (years) Mean follow-up duration (years) FIGURE 1 Study flow for identifying adult patients age 20 years with Type 2 diabetes from the Taiwan Health Insurance Database during Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

3 DIABETICMedicine Type 2 diabetes among adults in Taiwan C. H. Chang et al. they had diabetes or if they ever used oral hypoglycaemic agents or insulin injections. Subjects with negative or uncertain answers, but who had hypoglycaemic agents in the pharmacy claims database were also classified as having diabetes. Validation of this algorithm demonstrated a high level of sensitivity and positive predictive value (96.9 and 93.9%, respectively). We excluded patients whose ages upon first diagnosis of diabetes were < 0 or > 100 years old, which was probably attributable to incorrect data entry (n = 3348; 0.22%). To avoid including women who had gestational diabetes but returned to normoglycaemia after child delivery, we also excluded those who had diabetes visit claims within 270 days before parturition (n = 4237; 0.28%). However, women who had three or more subsequent outpatient visits with diabetes diagnostic codes within 365 days after childbirth were still included in the analysis. Patients with potential Type 1 diabetes were further identified if they (i) had ever been hospitalized because of diabetic ketoacidosis (ICD-9-CM code 250.1x); (ii) had ever had hospital admission with the discharge diagnosis of insulindependent diabetes mellitus (ICD-9-CM code 250.x1, 250.x3); or (iii) received a catastrophic illness certificate issued by the Department of Health Taiwan for several debilitating diseases, including Type 1 diabetes. A total of (2.7%) patients met at least two of the above criteria for potential Type 1 diabetes and were not included in the analysis. Finally, patients with prevalent Type 2 diabetes were included in the analysis. distribution was assumed for calculating 95% confidence intervals (CIs). The age was classified into 5-year intervals for the above calculation and for direct age standardization of annual prevalence and incidence. Results were presented gender specifically and grouped into four age groups: < 40, 40 59, and 80 years old. Graphs stratified by gender and age < 40 or 40 years were presented to illustrate the incidence and prevalence year trend. Because of the enormous sample size in this data set, in the present study most of the confidence intervals were very narrow and thus only point estimates were reported for the majority of the results. Poisson regression was used to analyse prevalence and incidence trend of Type 2 diabetes with age adjusted in a 5- year category and with the Taiwanese population used as an offset term. The calendar year as a continuous variable was used in the model to test for linear period trend. The interaction term with the gender cross-product year was used to test the difference in trends between male and female, as well as the interaction for year and age below or above 40 years to test the difference in trends between younger and older people. Estimated Poisson regression coefficients were used to calculate the 5-year interval (1999 to 2004), cumulative relative risk (RR for prevalence) and relative incidence (RI) and their 95% CI by multiplying the coefficients to 5 then taking the exponential. Two-sided P-values smaller than 0.05 were considered statistically significant. Incident and prevalent cases ascertainment An incident case was ascertained after confirming that the patient did not meet the criteria of diabetes in the claims database, with a minimum period of 3 years prior to their first diabetes diagnosis. As a result, we could only identify incident cases after 31 December 1998 as a 3-year diabetes-free observation period was not available during Of note, incident cases were ascertained up to 31 December 2004 because data required to fulfill the criteria of 3 outpatient visits within 365 calendar days was not sufficient after that date for every candidate. The hospital admission date or the first date of outpatient visit that met the definition for diabetes, whichever came first, was used as the date of incident event. Patients remained as prevalent cases regardless of whether or not they had claims with diabetes diagnoses in subsequent follow-up as long as they remained in the data set. Because of lack of death records in the database, if there was no claim for any health service in the database for more than 1 year, we assumed that Type 2 diabetes patients had unknown vital status and they were removed from the study after the date of the last record. Statistical analysis Age- and gender-specific annual incidence and prevalence of Type 2 diabetes from 1999 to 2004 were calculated by dividing the number of Type 2 diabetes patients by the mid-year Taiwanese population of the respective stratum. Poisson Results There were subjects fulfilling the study criteria of Type 2 diabetes and who were included in the final analysis. Of those, (50.8%) were men and (47.6%) were incident patients. The mean follow-up duration was 5.3 years for women and 4.9 years for men (Fig. 1). Age-gender-specific and age-standardized prevalence and incidence, and number of Type 2 diabetes patients of each study year are summarized in Table 1. The numbers of the adult population of age 20 years increased steadily and the gender ratios were fairly constant in Taiwan from 1999 to For Type 2 diabetes-prevalent patients, the numbers were higher in women than men, but the numbers of incident patients were higher in men than women for each year during the study period. The numbers of prevalent patients were narrowing, but the numbers of incident patients each year were widening in men and women following the study years. The age-standardized prevalence of Type 2 diabetes increased from 4.7 to 6.5% for men and from 5.3 to 6.6% for women. The incidence per 1000 person-years was approximately 7.6 and remained stable for men, but decreased from 7.7 to 6.9 for women. The annual incidence rates were the highest in 1999 during the study period. This may have been as a result of the change of diabetes diagnostic criteria for fasting plasma glucose from 140 to 126 mg dl in Figure 2(a) shows the prevalence trends for men and women. Both trends significantly increased with the RR of 1.38 (95% 638 Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

4 Original article DIABETICMedicine Table 1 Age- and gender-specific annual prevalence and incidence of adults aged 20 years with Type 2 diabetes in Taiwan during Gender Age (years) Population Prevalence (%) n (total) > Age standardized n (total) > Age standardized Incidence (per 1000 person-year) n (total) > Age standardized n (total) > Age standardized (a) 1.0% 0.8% Age 20 and < 40 years 20% 16% Age 40 years T2DM Prevalence 0.6% 0.4% 0.2% T2DM Prevalence 12% 8% 4% 0.0% Year 0% Year (b) T2DM Incidence per 1000 person-years Age 20 and < 40 years T2DM Incidence per 1000 person-years Age 40 years Year Year FIGURE 2 Gender-specific age-standardized trends of Type 2 diabetes (T2DM): (a) prevalence and (b) incidence for the adult population of age 20 and < 40 years, and age 40 years during in Taiwan. Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

5 DIABETICMedicine Type 2 diabetes among adults in Taiwan C. H. Chang et al. CI = 1.37, 1.39) for men and 1.24 (95% CI = 1.24, 1.25) for women in 5 years. The increasing trend for men was stronger than for that of women, with significant interaction of gender by year (P < 0.001) in the Poisson model. As illustrated in Figure 2(b), in contrast to the increasing trends of prevalence, a modest decrease in Type 2 diabetes incidence was observed for people aged 40 years. The age standardized incidence of this age group was 13.6 per 1000 for both genders in 1999 and decreased slightly to 13.1 and 12.0 per 1000 for men and women, respectively, in The RI was 0.96 (95% CI = 0.81, 1.14) for men and 0.87 (95% CI = 0.81, 0.94) for women. The declining incidence trend was not significant for men but was significant for women. However, there were significant increasing incidence trends among both men and women aged < 40 years. The RI was 1.31 (95% CI = 1.20, 1.42) and (95% CI = 1.006, 1.082) for men and women, respectively. The difference in the increasing trend for men and women was significant by gender and year interaction (P < 0.001) in the Poisson model. The interaction between year trend and age group was also significant for each gender (both P < 0.001). Figure 3 shows the age- and gender-specific prevalence and incidence of Type 2 diabetes in 1999 and The prevalence rapidly increased after the ages of years and peaked at age 70 79, then decreased for both genders in both study periods. Although the overall prevalent patient number was higher for women than men, the prevalence of men was higher than women in the younger age group. Incidence rate had similar age distributions to those of prevalence, although they peaked at an earlier age of years for both men and women. Incidence declined most obviously for women aged years, leading to a closer incidence distribution for men and women in this age group in However, higher incidence for men was shown in comparison with women in the younger age group. Discussion Using National Health Insurance claims data, we found a universal increase in the prevalence of Type 2 diabetes for both men and women, with the highest growth among those aged < 40 and > 80 years from 1999 to There was a 31% increase (5-year RI = 1.31) in the incidence of Type 2 diabetes for men and a 4.3% increase (5-year RI = 1.043) for women in the < 40-year-old age group, despite the modest decrease in incidence for men and women of age 40 years. The health insurance administrative and claims database is a valuable resource for estimating chronic disease burdens, monitoring epidemic trends and evaluating the impact of care in terms of disease prevention and outcome improvement [21,22]. Sloan and colleagues used a validated method to identify individuals with diabetes from Medicare administrative data and observed a substantial increase in diabetes incidence by 23% and a dramatic growth in prevalence by 62% in the US population aged 65 years or above [8]. Lipscombe and Hux undertook a longitudinal analysis of the Ontario diabetes database, a validated registry generated by administrative data from the government-funded Canadian health plan available to all residents [6]. They found that, for adults aged 20 years, the age- and gender-adjusted diabetes prevalence increased from 5.2% in 1995 to 8.8% in 2005 and incidence increased from 6.6 per 1000 in 1997 to 8.2 per 1000 in Their study also showed that, despite the fact that most cases of diabetes were in older individuals, rates of diabetes grew most rapidly in the population aged < 50 years. We found the age-standardized incidence per 1000 to be approximately 7.5 for adult men and 7.0 for adult women during Tseng and colleagues conducted a telephone interview among a random sample of Type 2 diabetes patients and suggested the incidence per 1000 of the population during was 1.9 for men and 2.2 for women, figures which were likely underestimated as a result of incomplete case ascertainment shortly after the launch of the Taiwan National Health Insurance Program in 1995 [23]. In addition, they found incidence increased for all age groups, while the highest increase was observed for men and women aged < 35 years. Our study, using the updated nationwide claim data, also indicated a universal increase in the prevalence of Type 2 diabetes between 1999 and 2004, with the highest growth among those aged < 40 and > 80 years; however, a significant increasing trend in incidence was found among those aged < 40 years. The incidence trend in the older age group had not increased and was even shown to be declining. This finding suggested that different factors contribute to the increase in Type 2 diabetes disease burden in these two age groups. For the elderly, an ageing population and decreased death rate might explain the rise in the total number and prevalence of Type 2 diabetes. For the younger population, increasing numbers of patients with newly diagnosed Type 2 diabetes may be attributable to increased accessibility to the healthcare facilities after the change in the insurance system. Meanwhile, several studies have suggested that rising rates of obesity resulting from increasing total energy and fat intake and physical inactivity may influence the younger aged group in particular [24,25]. In a comprehensive review examining the trends in obesity in China based on nationally representative data, Wang and colleagues found that, during the 10-year period between 1992 and 2002, younger adults aged experienced the largest relative increase in the prevalence of obesity; furthermore, men had experienced a greater rise in the prevalence of overweight and obesity than women [24]. In a recently published article, Chan and colleagues indicate that Type 2 diabetes is an increasing epidemic in Asia, characterized by onset at a relatively young age and low body mass index. They suggest the increasing trends of childhood obesity in Asia may place many young individuals at high risk for Type 2 diabetes in early adulthood [25]. Our study finding was consistent with these reports and highlighted the alarming increase in Type 2 diabetes among the younger population, especially in men. As diabetic patients with young age of onset and long disease duration were associated with higher risk of long-term micro- and 640 Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

6 Original article DIABETICMedicine (a) T2DM Prevalence (b) T2DM Incidence per 1000 person-years Age (years) Age (years) FIGURE 3 Age- and gender-specific (a) prevalence and (b) incidence of Type 2 diabetes (T2DM) among adults in 1999 and 2004 in Taiwan. macrovascular complications, our study results indicate a need for appropriate screening for high-risk subjects as well as increased efforts aimed at diabetes prevention [6]. Our study had the strengths of nationwide data with a large sample size, emphasizing incidence trends in the recent years and using a validated algorithm specific to Taiwan National Health Insurance Program to identify patients with diagnosed diabetes. Because the American Diabetes Association and World Health Organization recommended a decrease in the diagnostic fasting plasma glucose in 1997 and 1998, we used a 3-year diabetes-free observation period as part of the definition of incidence case, calculated annual estimates of incidence and prevalence starting from 1999 and compared trends thereafter when uniform diagnostic criteria for diabetes could be applied. To reduce the potential of prevalence underestimation, because many diabetic patients with no symptoms did not receive a healthcare service regularly, or even stop to attend the hospital, we assumed that patients remained prevalent cases once they fulfilled our criteria for diabetes, regardless of whether or not they had claims with diabetes diagnoses in subsequent years. Journal compilation ª 2010 Diabetes UK. Diabetic Medicine, 27,

7 DIABETICMedicine Type 2 diabetes among adults in Taiwan C. H. Chang et al. Several limitations need to be considered in this study. First, to determine Type 2 diabetes, we excluded patients who had been admitted because of diabetic ketoacidosis, with the discharge diagnosis of insulin-dependent diabetes mellitus, and those who received a catastrophic certificate for potential Type 1 diabetes. We cannot overlook the possibility that some Type 2 diabetes patients were also excluded by this algorithm. However, this would only have a small impact as patients excluded because of potential Type 1 diabetes accounted for only 3% of the total number of identified cases. It is also possible that some Type 1 diabetic patients could be included in the current analysis. Second, this study only included diagnosed Type 2 diabetes patients, which may underestimate the true extent of the epidemic. The 2002 Survey on the Prevalence of Hypertension, Hyperglycaemia and Hyperlipidaemia in Taiwan showed that the proportion of awareness of diabetes was approximately 59% for men and 69% for women [26]. Third, we could not analyse trends in mortality because information on cause of death was not available in the database. When calculating the prevalence, patients who had no claim for any health service in the database for more than 1 year were not counted as prevalent cases after the date of the last record. This was a reasonable assumption as Type 2 diabetes is a chronic disease that requires frequent access to healthcare services and Taiwan s National Health Insurance provides continuing universal coverage for the whole population. Finally, in this study we described a national diabetes surveillance system similar to that implemented in other countries, taking advantage of available administrative data. Information on the population such as body mass index or waist circumference, blood pressure, lipids, smoking and diabetes family history were not available in the claims database and thus were beyond the scope of this study. These data will be important in the future for finding the possible causes of the change we observed in the trends of Type 2 diabetes incidences and prevalence in our present study. Conclusion Using National Health Insurance claims data, we have demonstrated that there has been a substantial increasing trend in the Type 2 diabetes disease burden during the period and, in particular, a remarkable increase in incidence for young male individuals. We highly recommend appropriate screening for high-risk subjects and increased efforts aimed at diabetes prevention for the Chinese population. Competing interests Nothing to declare. Acknowledgements This work was supported by a grant from the Taipei Veterans General Hospital (grant no. V96S10-001). 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