September 2011
Volume 52, Issue 10
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Clinical and Epidemiologic Research  |   September 2011
Racial Differences in the Prevalence of Diabetes but Not Diabetic Retinopathy in a Multi-ethnic Asian Population
Author Affiliations & Notes
  • Peggy P. C. Chiang
    From the Singapore Eye Research Institute, Singapore National Eye Centre, Singapore;
    the DUKE-NUS Graduate Medical School, Singapore, Singapore;
  • Ecosse L. Lamoureux
    From the Singapore Eye Research Institute, Singapore National Eye Centre, Singapore;
    the Centre for Eye Research Australia, University of Melbourne, Melbourne, Victoria, Australia;
  • Carol Y. Cheung
    From the Singapore Eye Research Institute, Singapore National Eye Centre, Singapore;
    the DUKE-NUS Graduate Medical School, Singapore, Singapore;
  • Charumathi Sabanayagam
    the Department of Community Medicine, West Virginia University School of Medicine, Morgantown, West Virginia;
  • Wanling Wong
    From the Singapore Eye Research Institute, Singapore National Eye Centre, Singapore;
  • E. Shyong Tai
    the University Medicine Cluster, National University Health System, Singapore, Singapore; and
  • Jeannette Lee
    the Department of Epidemiology and Public Health, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
  • Tien Y. Wong
    From the Singapore Eye Research Institute, Singapore National Eye Centre, Singapore;
    the Centre for Eye Research Australia, University of Melbourne, Melbourne, Victoria, Australia;
    the University Medicine Cluster, National University Health System, Singapore, Singapore; and
  • Corresponding author: Tien Y. Wong, Singapore Eye Research Institute, 11 Third Hospital Ave, 05-00, Singapore 168751; ophwty@nus.edu.sg
Investigative Ophthalmology & Visual Science September 2011, Vol.52, 7586-7592. doi:https://doi.org/10.1167/iovs.11-7698
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      Peggy P. C. Chiang, Ecosse L. Lamoureux, Carol Y. Cheung, Charumathi Sabanayagam, Wanling Wong, E. Shyong Tai, Jeannette Lee, Tien Y. Wong; Racial Differences in the Prevalence of Diabetes but Not Diabetic Retinopathy in a Multi-ethnic Asian Population. Invest. Ophthalmol. Vis. Sci. 2011;52(10):7586-7592. https://doi.org/10.1167/iovs.11-7698.

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Abstract

Purpose.: To compare the prevalence and risk factors of diabetes (DM) and diabetic retinopathy (DR) in a multi-ethnic Asian population of Chinese, Malays, and Indians in Singapore.

Methods.: A total of 2919 individuals participated in a population-based, cross-sectional study in Singapore of Chinese (n = 1633), Malays (n = 658), and Indians (n = 628) aged 40 to 95 years, with retinal photographs, graded using the Early Treatment Diabetic Retinopathy Study (ETDRS) severity scale. DM was defined as fasting plasma glucose ≥7 mmol/L, self-reported physician-diagnosed diabetes, and use of glucose-lowering medication.

Results.: The overall age-standardized prevalence of diabetes was 13.8% (Chinese, 11.5%; Malays, 17.1%; and Indians, 21.6%; P < 0.0001). Among persons with diabetes (n = 401), the overall age-standardized prevalence of DR was 25.4% (20.1%, 24.8%, and 28.9% in Chinese, Malays, and Indians, respectively; P = 0.290). In multivariate analysis, longer diabetes duration (odds ratio [OR], 1.05; 95% confidence interval [CI], 1.01–1.09, per year increase), higher glycated hemoglobin (OR 1.25; 95% CI, 1.01–1.54, per 1% increase), and serum creatinine levels (OR, 1.01; 95% CI, 1.00–1.03, per mg/dL increase) were the independent risk factors of DR in the whole population. Race was not found to be associated with DR (OR, 1.35; CI, 1.00–1.83). The associations of major risk factors with DR were similar among the three ethnic groups.

Conclusions.: There was a significant difference in the prevalence of diabetes between Chinese, Malays, and Indians. The main risk factors of DR, similar among the three ethnic groups, are longer diabetes duration, higher hbA1c, and higher creatinine levels. No significant racial differences were found in the prevalence of DR among persons with diabetes.

Diabetes mellitus (DM) affects over 246 million people worldwide. About a third have diabetic retinopathy (DR) 1 and of those, a third will have vision threatening retinopathy (defined as severe retinopathy or macular edema). 2 The World Health Organization (WHO) estimates that by 2025, an estimated 300 million people will have diabetes, with many expected to develop some level of retinopathy. 1 DR is the major cause of vision impairment and blindness in people with diabetes. 3 6 The prevalence of DR is expected to grow exponentially as diabetes continues to increase globally. 7,8  
The prevalence of diabetes appears to vary between racial and ethnic groups. 9,10 For example, McBean et al. 11 found the increase in prevalence rates to be the greatest among Hispanics and Asian Americans. The authors attributed the differences to Medicare entitlements in the Hispanic groups and the westernization of lifestyle, particular in diet among Asians. 11 Similar findings have been reported by Harris et al. 12 There have also been suggestions that environmental and socioeconomic factors may contribute to racial disparities in the prevalence of diabetes. 13 For instance, LaVeist et al. 13 found, in integrated communities with similar health risk environments and sociodemographic factors, that the prevalence estimates of diabetes were similar in African Americans and whites. 
Like diabetes, it has also been suggested that the frequency of DR may vary by race/ethnicity. African Americans have a fourfold risk of DR-induced vision impairment compared to non-Hispanic whites. 14 In the LALES study (Los Angeles Latino Eye Study), Latinos were found to have a higher rate of more severe threatening DR than whites (Varma R, et al. IOVS 2005;46:ARVO E-Abstract 1164). 15 Dowse et al. 16 did not find any variation in the prevalence of DR observed in all major ethnic groups in Mauritius. However, although there have been large studies conducted on the epidemiology of DR in Asia, 17 19 none has investigated interracial/ethnic variations in the prevalence and risk factors of DR among the three major Asian groups (Chinese, Malays, and Indians). This information is important, as disparities in health for racial and ethnic groups can represent unequal access to care. 20,21  
In this study we examined the prevalence and risk factors of diabetes and DR in a population-based sample of Chinese, Malays, and Indians living in Singapore. These three ethnic groups represent two thirds of the world's population. Furthermore, Singapore is the ideal location in which to conduct this research because all three groups live in one geographic area, with largely similar environmental and sociodemographic factors. 
Methods
Study Population
The data for this study were from the Singapore Prospective Study Program (SP2), a population-based, cross-sectional study of Chinese, Malays, and Indians aged 24 to 95 years in Singapore. Detailed population selection and methodology have been published elsewhere. 22 Briefly, from 2003 to 2007, 10,747 participants were invited to participate from one of the four previous cross-sectional studies (Fig. 1). 23 26 Trained interviewers administered questionnaires in the homes of the participants. Retinal photography, systemic and ocular examination, and laboratory investigations plus a range of demographic, lifestyle factors, and medical history were collected on 7744 persons. Of these, 2580 declined health screening and 5164 attended. The availability of only one retinal camera resulted in only one in two participants from the group with the largest sample size (i.e., Chinese) being able to have retinal photographs. Participants with ungradable photos and staff and volunteers were also excluded. Only those aged 40 years or more were included, as there were few people younger than 40 with diabetes (n = 12) and even fewer with DR (n = 2), leaving 2919 persons for the final analysis (27.5% of the 7744 eligible participants; Fig. 1). The study complied with the Declaration of Helsinki. Institutional review board approval was granted at each study site, and informed consent was obtained from all eligible participants. 
Figure 1.
 
Number of subjects considered for inclusion in Study SP2, Singapore, 2003–2007.
Figure 1.
 
Number of subjects considered for inclusion in Study SP2, Singapore, 2003–2007.
Retinal Fundus Photography
Details of the method in taking retinal images have been described previously. 27 Briefly, digital fundus photographs were taken using a 45° digital retinal camera (CRDGi with a 10D SLR back; Canon, Tokyo, Japan) after pupil dilation with tropicamide (1%) and phenylephrine (2.5%). Two retinal images of each eye were obtained, one centered at the optic disc and another centered at the fovea, identical with the ETDRS standard fields 1 and 2. 28 Five trained graders, masked to the participants' characteristics, performed the vessel measurements on the optic disc–centered image of the right eye for most participants and on the left eye in persons without gradable right eye images. Retinal photographs with fewer than six acceptable measurements of either vessel type were considered ungradable. 
Measurement of Outcome: Diabetic Retinopathy
The primary outcome of this study was the presence of any retinopathy among participants with diabetes. Diabetes was defined as fasting glucose ≥7 mmol/L, self-reported physician-diagnosed diabetes, or use of glucose-lowering medication. DR was defined according to the ETDRS scale. 29 It was considered present if any of the following characteristic lesions was present: microaneurysms (MA), hemorrhages, cotton wool spots, intraretinal microvascular abnormalities (IRMA), hard exudates (HE), venous bleeding, and new vessels. 17 The presence of DR was then graded according to a scale modified from the Airlie House classification system 29 : level 10, no retinopathy present; level 15, hemorrhage present without any definite MA; level 20, MA only with no other retinopathy lesions present; level 31, MA and one or more of hemorrhage or MA less than standard photograph 2A, hard exudates, venous loops, questionable cotton wool spots, IRMA, or venous beading; level 41, MA and one or more of cotton wool spots or IRMA less than standard photograph 8A; level 51, MA and one or more of venous beading, hemorrhage, MA of 2A or more, or IRMA of 8A or more; level 60, fibrous proliferation with no other proliferative lesions; level 61 through 64, laser scatter photocoagulation scars with retinopathy levels 31 through 51; level 65, proliferative DR less than high-risk characteristics, as defined in the Diabetic Retinopathy Study; level 70, proliferative DR with high-risk characteristics; and level 80, total vitreous hemorrhage. 
Measurement of Main Risk Factors
All serum biochemistry tests were performed at the National University Hospital Reference Laboratory. The biochemistry tests included total cholesterol, high-density lipoprotein cholesterol (HDL), low-density lipoprotein (LDL) cholesterol, triglycerides, and fasting plasma glucose. Fasting blood samples measured serum lipids and plasma glucose. During the interview, cardiovascular disease (CVD) was defined as self-reported myocardial infarction, angina, or stroke. Main risk factors of CVD were also assessed: cigarette smoking (currently smoking everyday or on some days) and alcohol consumption (currently consuming alcoholic beverages daily or on some days). Systolic and diastolic blood pressures were measured with a digital automatic blood pressure monitor (Dinamap model Pro100V2; Criticon GmbH, Norderstedt, Germany), after the participant had been seated for at least 5 minutes. Participants classified as having hypertension had a systolic blood pressure of 140 mm Hg or more or a diastolic blood pressure of 90 mm Hg or more at examination, a reported history or a self-reported history of physician-diagnosed hypertension, or use of prescribed antihypertensive medications, or both. Mean arterial blood pressure was calculated as two thirds of the diastolic value plus one third of the systolic value. Body mass index (BMI) was calculated as weight divided by the square of height in meters (kg/m2). 
Statistical Analysis
Characteristics of the study population and risk factors were examined using proportions, means, medians, percentiles, and standard deviations. The χ2 test and t-test were used for univariate associations. Age-standardized prevalence estimates were calculated via the direct method using the 2010 Singapore population census. The prevalences of diabetes and DR were estimated and compared between the three ethnic groups: Chinese, Malay, and Indians. Binary logistic regressions were performed to examine the association of DR with various risk factors in the ethnic groups and were adjusted for age and sex. Interactions between the presence of any DR and each of the potential confounders were explored by including appropriate interaction terms in the model. The Mantel-Haenszel method was used to test for differences between the prevalence estimates of the three ethnic groups (all statistical analyses: Stata, ver. 11.0; StataCorp, College Station, TX). 
Results
Of the 2919 participants over the age of 40 years included in the analyses, 401 (13.7%) reported having diabetes, and of these, 107 (26%) were found to have DR (Chinese, n = 29; Malays, n = 33; and Indians, n = 45). The characteristics of the study participants, overall and by race/ethnicity, are shown in Table 1. The overall mean (SD) age of the total cohort was 53 (±9.0) years. Among the three ethnicities, Indians consumed alcohol more than once a month, had a higher prevalence of heart disease, longer duration of diabetes, and higher HbA1c levels. The Malays were more likely to have a secondary level education or lower; earn a household income below $4000; reside in government housing; be a current smoker; have a higher BMI, serum creatinine levels, and systolic blood pressure; and be unemployed. 
Table 1.
 
Baseline Characteristics of the SP2, Study Participants by Ethnicity
Table 1.
 
Baseline Characteristics of the SP2, Study Participants by Ethnicity
Characteristics All Participants (n = 2919*) Chinese (n = 1633) Malays (n = 658) Indians (n = 628) P
Sex, male 1384 (47.4) 743 (45.5) 331 (50.3) 310 (49.4) 0.062
Age, >40 years 53.0 ± 9.0 53.0 ± 9.1 52.4 ± 8.8 53.4 ± 8.8 0.107
Education, secondary level and below 2165 (74.2) 1144 (70.1) 552 (83.9) 469 (74.7) <0.0001
Received more than 10 years of education, Y/N 826 (28.3) 522 (32.0) 122 (18.5) 182 (29.0) <0.0001
Employed, Y/N 1928 (66.1) 1117 (68.5) 404 (61.4) 407 (64.8) 0.004
Household income, ≤4000/month 1187 (66.8) 538 (57.4) 339 (83.1) 310 (71.6) <0.0001
Resides in government housing, HDB 2443 (83.7) 1272 (77.9) 615 (93.5) 556 (88.5) <0.0001
Current smoker, Y/N 353 (58.6) 163 (57.2) 112 (60.2) 78 (59.5) 0.787
Frequency of alcohol use, more than once a month 363 (62.0) 257 (58.9) 7 (70.0) 99 (70.7) 0.039
Heart disease, Y/N 86 (2.95) 27 (1.7) 17 (2.6) 42 (6.7) <0.0001
Duration of diabetes, y 9.5 ± 8.9 8.8 ± 7.0 8.4 ± 9.3 10.8 ± 10.0 0.139
High cholesterol, Y/N 972 (36.0) 538 (35.4) 210 (35.1) 224 (38.2) 0.447
BMI, kg/m2 24.5 ± 4.4 23.1 ± 3.5 26.6 ± 4.8 26.1 ± 4.7 <0.0001
Glycated hemoglobin (HbA1c),% 6.1 ± 1.1 5.9 ± 0.8 6.2 ± 1.3 6.5 ± 1.5 <0.0001
Creatinine, μmol/L 80.2 ± 22.7 78.7 ± 20.7 82.5 ± 28.2 81.7 ± 21.0 0.0002
Systolic blood pressure, mm Hg 134.3 ± 20.5 132.4 ± 20.3 139.2 ± 20.4 134.3 ± 20.4 <0.0001
Prevalence rates were age-standardized to the overall Singapore Census 2010 data. 30 The overall age-standardized prevalence of diabetes was 13.8%. In univariate analyses, the prevalence of DM was 11.5%, 17.1%, and 21.6% in the Chinese, Malays, and Indians, respectively (P < 0.0001). Among the persons with diabetes (n = 107), the age-standardized prevalence of DR was 25.4% overall and 20.1% in the Chinese, 24.8% in the Malays, and 28.9% in the Indians (P = 0.290; Figs. 2 and 3). 
Figure 2.
 
Age-standardized prevalence of diabetes by ethnicity.
Figure 2.
 
Age-standardized prevalence of diabetes by ethnicity.
Figure 3.
 
Age-standardized prevalence of DR among diabetics by ethnicity.
Figure 3.
 
Age-standardized prevalence of DR among diabetics by ethnicity.
In robustly adjusted regression models, race disappeared as a significant risk factor for DM (Table 2; P = 0.062). On the other hand, high cholesterol (odds ratio [OR], 0.33; 95% confidence interval [CI], 0.20–0.53), BMI (OR, 1.08; CI, 1.02–1.14), HbA1c (OR, 27.95; CI, 18.26–42.79), peripheral artery disease (PAD; OR, 2.74; CI, 1.14–6.55), and LDL cholesterol (OR, 0.58; CI, 0.44–0.76) were found to be independently associated with DM (Table 2). When stratified by race (Table 3), HbA1c was found to be statistically significant (P < 0.001) across all three racial groups. More risk factors were found in the Chinese group than in the Malay or Indian groups: age (OR, 1.05; CI, 1.00–1.90), BMI (OR, 1.10; CI, 1.01–1.21), HbA1c (OR, 30.4; CI, 16.13–57.37), and PAD (OR, 6.26; CI, 1.84–21.3), whereas high cholesterol (OR, 0.43; CI, 0.26–0.71), and HbA1c (OR, 22.89; CI, 10.55–49.66) were found in the Malays, and only HbA1c was significant in the Indian group (OR 14.16; CI 7.15, 28.04). 
Table 2.
 
Risk Factors for Diabetes in the SP2 Population
Table 2.
 
Risk Factors for Diabetes in the SP2 Population
Risk Factors Age- and Sex-Adjusted Odds Ratio 95% CI P Multivariate Odds Ratio 95% CI P *
Race 0.68 0.55–0.80 <0.001 1.31 0.99–1.75 0.062
Age, y 1.33 1.08–1.65 0.008 1.04 1.02–1.05 <0.001
Sex, female 1.33 1.08–1.65 0.008 0.96 0.55–1.68 0.887
Systolic blood pressure, mm Hg 1.02 1.01–1.03 <0.001 1.01 1.00–1.02 0.116
Years of education 0.55 0.41–0.74 <0.001 0.69 0.37–1.29 0.245
Housing, private 0.53 0.36–0.76 0.001 0.48 0.24–0.98 0.045
Alcohol, Y/N 0.72 0.54–0.95 0.020 1.24 0.71–2.15 0.455
Stroke, Y/N 0.28 0.12–0.66 0.004 0.55 0.13–2.35 0.426
High cholesterol, Y/N 0.49 0.39–0.62 <0.001 0.33 0.20–0.53 <0.0001
BMI, kg/m2 1.10 1.07–1.13 <0.001 1.08 1.02–1.14 0.008
HbA1c, %† 22.91 16.13–32.55 <0.001 27.95 18.26–42.79 <0.001
Peripheral artery disease, Y/N 2.06 1.34–3.16 <0.001 2.74 1.14–6.55 0.024
Triglycerides, mmol/L 1.41 1.25–1.59 <0.001 0.85 0.63–1.15 0.297
High-density lipoprotein cholesterol, mmol/L 0.36 0.24–0.53 <0.001 1.56 0.64–3.82 0.328
Low-density lipoprotein cholesterol, mmol/L 0.72 0.64–0.83 <0.001 0.58 0.44–0.76 <0.0001
C Reactive Protein, mg/L 1.01 1.00–1.03 0.038 0.96 0.92–1.00 0.058
Creatinine, μmol/L 1.01 1.00–1.01 0.025 1.00 1.00–1.01 0.406
Table 3.
 
Risk Factors for Diabetes in the SP2 Population Stratified by Race
Table 3.
 
Risk Factors for Diabetes in the SP2 Population Stratified by Race
Risk Factors Chinese Malays Indians
Multivariate Odds Ratio (95% CI) P Multivariate Odds Ratio (95% CI) P Multivariate Odds Ratio (95% CI) P
Age, years 1.05 (1.00–1.90) 0.034
Sex, male 0.77 (0.31–1.95) 0.584
Married, Y/N
Education, secondary and below, Y/N
Unemployed, Y/N
Income, >4000/month 0.63 (0.22–1.80) 0.387
Private housing, Y/N 0.60 (0.24–1.45) 0.256 0.82 (0.22–3.03) 0.771
Smoking, Y/N
Alcohol, Y/N
Reported heart disease, Y/N
Reported stroke, Y/N 0.17 (0.02–1.35) 0.093
SBP, mm Hg 1.01 (0.99–1.03) 0.464 0.49 (0.18–1.32) 0.158
High cholesterol, Y/N 0.70 (0.46–1.08) 0.112 0.43 (0.26–0.71) 0.001 0.97 (0.87–1.08) 0.597
BMI, kg/m2 1.10 (1.01–1.21) 0.038 1.09 (1.00–1.18) 0.046 0.97 (0.87–1.08) 0.597
HbA1c, %* 30.4 (16.13–57.37) <0.001 22.89 (10.55–49.66) <0.001 14.16 (7.15–28.04) <0.001
Chronic kidney disease (CKD), Y/N 2.02 (0.48–8.49) 0.334
Creatinine, μmol/L 0.99 (0.97–1.01) 0.473
Triglycerides, mmol/L 0.96 (0.54–1.70) 0.879 1.21 (0.77–1.91) 0.394 0.97 (0.49–1.92) 0.935
High-density lipoprotein cholesterol, mmol/L 1.42 (0.34–5.99) 0.633 1.46 (0.31–6.82) 0.634
C-reactive protein, mg/L
>1 Reported comorbidities, Y/N
Peripheral artery disease (PAD), Y/N 6.26 (1.84–21.3) 0.003
Dyslipidemia, Y/N 0.75 (0.35–1.59) 0.453
Table 4 shows the overall associations of various demographic, metabolic, and socioeconomic risk factors for DR in the population with diabetes. In multivariate analysis, the independent risk factors for the presence of DR were higher serum creatinine level (OR 1.01; CI 1.00–1.03), longer diabetes duration (OR 1.05; CI 1.01–1.09), and higher HbA1c level (OR 1.25; CI 1.01–1.55). P interaction between these risk factors (creatinine: P = 0.7188; HbA1c: P = 0.8277; duration of diabetes: P = 0.8840) and DR demonstrated that race was not a risk factor and that the association of risk factors with DR were not modified by race. 
Table 4.
 
Risk Factors for Diabetic Retinopathy in the SP2 Population
Table 4.
 
Risk Factors for Diabetic Retinopathy in the SP2 Population
Risk factors Age- and Sex-Adjusted Odds Ratio 95% CI P Multivariate Odds Ratio 95% CI P *
Chinese 1.00 Reference Reference 1.00 Reference Reference
Malay 1.53 1.11–2.10 0.009 1.86 0.77–4.50 0.170
Indian 1.85 1.36–2.52 <0.001 1.76 0.83–3.73 0.142
Age, y 1.02 1.01–1.03 0.003 1.00 0.96–1.03 0.908
Sex, male 1.47 1.13–1.91 0.004 1.78 0.85–3.74 0.128
Creatinine, μmol/L 1.01 1.00–1.02 <0.001 1.01 1.00–1.03 0.043
HbA1c, % 1.45 1.32–1.59 <0.001 1.25 1.01–1.55 0.036
Duration of diabetes, y 1.06 1.03–1.10 <0.001 1.05 1.01–1.09 0.011
SBP, mm Hg 1.01 1.01–1.02 <0.001 1.01 0.99–1.03 0.271
Education, y 1.74 1.23–2.45 0.002 1.08 0.43–2.73 0.868
Discussion
This is the first population-based study comparing interracial/ethnic variations in the prevalence and risk factors of diabetes and DR in three major Asian groups aged 40 to 95 years. There was a significant difference in the prevalence of diabetes between the Chinese (20.1%), Malays (24.8%), and Indians (28.9%). However, overall, race was not found to be a risk factor for diabetes and when further stratified by the three ethnic groups, the risk factors were similar across all groups. The prevalence of DR among persons with diabetes was also largely similar among the three ethnic groups. Race again was not found to be an independent risk factor for DR, although creatinine level, longer duration of diabetes, and higher HbA1c level were found to be associated with the outcome. 
Our race-specific DR prevalence rates differed from other population-based studies conducted in Asians. For instance, the prevalence rates among Chinese people aged 45 years and above in the Beijing 31 and Handan eye studies were 27.9% and 43.1%, respectively. 19 Similar studies in India have reported DR prevalence rates of 22.4% 32 and 26.8%. 33 The Singapore Malay Eye Study (SiMES) 17 found the overall prevalence of any retinopathy to be 35.0%. 17 Several reasons could explain these underlying variations. First, the differences could be related to the duration of diabetes, because it is one of the strongest risk factors for DR. Because of the delay in diagnosis of diabetes, the actual diabetes duration is often imprecise. Socioeconomic issues or biases related to care referrals or access (i.e., patterns of access to and utilization of medical care between races and across states or urban and rural areas) may be some of the factors causing the variations. 34 36 For example, in the United Kingdom, the coverage rates of screening and uptake of eye care among ethnic minority groups in inner city areas can be much lower than those for white Europeans. 37  
Many Indian studies and the Handan Eye Study were conducted in predominantly rural regions, where the diagnosis of diabetes is usually delayed for some years, most probably because of a lack of awareness and poor access to health care services. The prevalence of DR in Handan is high and differs approximately 5 years in duration compared to that in some Western countries. 19 This difference could signify that the diagnosis of diabetes is delayed on average about 5 years, so the DR prevalence for 10 years' duration in Handan probably equates to that for 15 years' duration in Western countries. Many Indians develop type 2 diabetes at an earlier age. 38 In fact, the Indians in our study were reported to have a longer duration of diabetes (Table 1), which further suggests that other mechanisms or different pathogeneses are at play. 39  
The prevalence rates for Malays differed from those in the SiMES study, perhaps because of detection biases and methodology differences. Differences between the studies include the graders, the number of retinal photograph fields per eye, and the definitions used to define diabetes. The SiMES study collected nonfasting venous blood samples, whereas in the SP2 study fasting venous blood samples were analyzed. 
Few studies have assessed variations in the prevalence of DR among different races and most have used non-Asian populations. For instance, Raymond et al. 39 found a significantly higher prevalence of DR and higher levels of HbA1c among patients of South Asian ethnicity than in white Europeans in the community. Eberhardt et al. 34 and Harries et al. 40 found that black people had higher levels of HbA1c in two South Carolina communities. When social factors such as low income or geography between the groups were equalized the effect of race was neutralized, suggesting predictors other than race. For example, Lim et al. 41 did not find race to be a predictor of DR within an urban, underserved population of whites, blacks, Hispanics, and Asians. This could also partially explain the underlying reason that our study did not find race to be a risk factor, as all Singaporeans live in a highly contained urbanized geographic area in proximity to one another. Thus, one can postulate that access to care and socioeconomic statuses for instance could be similar. 
Age, lipids, BMI, and glucose are all documented risk factors of diabetes. 42 44 The development of PAD has also been found to be associated with diabetes. 45 Research has shown that LDL and cholesterol can regulate the function and survival of β cells. 46 Thus, dyslipidemias may not only be consequences of but also contributors to the pathogenesis of type 2 diabetes and hence are targets for prevention. 46  
HbA1c and duration of diabetes also remain the classic predictors for the onset and progression of DR regardless of ethnicity and this was confirmed by our present study findings. 16,17,31,36,47,48 Wong et al. 36 showed that the risk factors for DR were similar across four racial/ethnic populations in six U.S. communities. The role of diabetes duration and HbA1c is well described by numerous clinical trials. 49 52 As for creatinine, it is an indicator of chronic kidney disease, 53,54 and there has been evidence showing that diabetic nephropathy may be used as a tell-tale sign of DR, necessitating more intensive ophthalmic care, especially in patients with a longer duration of diabetes. 55 Thus, our findings of creatinine as a possible risk factor are also consistent with those in the existing literature. 
The major strength of our study is that it was a large, population-based sample of three racial and ethnic groups, and information was available for a range of possible confounders. However, this study also has its limitations. First, the number of people with DM and DR was small (n = 107), even though the overall sample size was large. Insufficient statistical power may be the reason underpinning our inability to detect a difference in the prevalence and risk factors of DR among the three ethnic groups. 56 Second, we could not explore the race associations between the different types of DR (i.e., severity, macular edema, and vision-threatening retinopathy) as the numbers were too small. Finally, the analyses were cross-sectional, which limited us in making causational inferences between the variables and the outcome. 
In summary, our study demonstrates significant differences in the prevalence of diabetes between Chinese, Malays, and Indians. We found no race effect, although this may be related to our small sample of people with DM or DR. Future research in this area is warranted. Major risk factors of diabetes are age, lipids, glucose, and PAD. The major risk factors of DR are higher creatinine level, longer diabetes duration, and higher hbA1c level. The risk factors for both diabetes and DR are similar among the three ethnic groups aged 40 years and older. Our study findings imply the importance of optimizing diabetes control and addressing the key risk factors that lead to DR through early prevention, detection, and maintaining a high quality of clinical care. 
Footnotes
 Supported by Biomedical Research Council (BMRC) Grant 08/1/35/19/550 and National Medical Research Council (NMRC) Grant Star/0003/2008, Singapore.
Footnotes
 Disclosure: P.P.C. Chiang, None; E.L. Lamoureux, None; C.Y. Cheung, None; C. Sabanayagam, None; W. Wong, None; E.S. Tai, None; J. Lee, None; T.Y. Wong, None
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Figure 1.
 
Number of subjects considered for inclusion in Study SP2, Singapore, 2003–2007.
Figure 1.
 
Number of subjects considered for inclusion in Study SP2, Singapore, 2003–2007.
Figure 2.
 
Age-standardized prevalence of diabetes by ethnicity.
Figure 2.
 
Age-standardized prevalence of diabetes by ethnicity.
Figure 3.
 
Age-standardized prevalence of DR among diabetics by ethnicity.
Figure 3.
 
Age-standardized prevalence of DR among diabetics by ethnicity.
Table 1.
 
Baseline Characteristics of the SP2, Study Participants by Ethnicity
Table 1.
 
Baseline Characteristics of the SP2, Study Participants by Ethnicity
Characteristics All Participants (n = 2919*) Chinese (n = 1633) Malays (n = 658) Indians (n = 628) P
Sex, male 1384 (47.4) 743 (45.5) 331 (50.3) 310 (49.4) 0.062
Age, >40 years 53.0 ± 9.0 53.0 ± 9.1 52.4 ± 8.8 53.4 ± 8.8 0.107
Education, secondary level and below 2165 (74.2) 1144 (70.1) 552 (83.9) 469 (74.7) <0.0001
Received more than 10 years of education, Y/N 826 (28.3) 522 (32.0) 122 (18.5) 182 (29.0) <0.0001
Employed, Y/N 1928 (66.1) 1117 (68.5) 404 (61.4) 407 (64.8) 0.004
Household income, ≤4000/month 1187 (66.8) 538 (57.4) 339 (83.1) 310 (71.6) <0.0001
Resides in government housing, HDB 2443 (83.7) 1272 (77.9) 615 (93.5) 556 (88.5) <0.0001
Current smoker, Y/N 353 (58.6) 163 (57.2) 112 (60.2) 78 (59.5) 0.787
Frequency of alcohol use, more than once a month 363 (62.0) 257 (58.9) 7 (70.0) 99 (70.7) 0.039
Heart disease, Y/N 86 (2.95) 27 (1.7) 17 (2.6) 42 (6.7) <0.0001
Duration of diabetes, y 9.5 ± 8.9 8.8 ± 7.0 8.4 ± 9.3 10.8 ± 10.0 0.139
High cholesterol, Y/N 972 (36.0) 538 (35.4) 210 (35.1) 224 (38.2) 0.447
BMI, kg/m2 24.5 ± 4.4 23.1 ± 3.5 26.6 ± 4.8 26.1 ± 4.7 <0.0001
Glycated hemoglobin (HbA1c),% 6.1 ± 1.1 5.9 ± 0.8 6.2 ± 1.3 6.5 ± 1.5 <0.0001
Creatinine, μmol/L 80.2 ± 22.7 78.7 ± 20.7 82.5 ± 28.2 81.7 ± 21.0 0.0002
Systolic blood pressure, mm Hg 134.3 ± 20.5 132.4 ± 20.3 139.2 ± 20.4 134.3 ± 20.4 <0.0001
Table 2.
 
Risk Factors for Diabetes in the SP2 Population
Table 2.
 
Risk Factors for Diabetes in the SP2 Population
Risk Factors Age- and Sex-Adjusted Odds Ratio 95% CI P Multivariate Odds Ratio 95% CI P *
Race 0.68 0.55–0.80 <0.001 1.31 0.99–1.75 0.062
Age, y 1.33 1.08–1.65 0.008 1.04 1.02–1.05 <0.001
Sex, female 1.33 1.08–1.65 0.008 0.96 0.55–1.68 0.887
Systolic blood pressure, mm Hg 1.02 1.01–1.03 <0.001 1.01 1.00–1.02 0.116
Years of education 0.55 0.41–0.74 <0.001 0.69 0.37–1.29 0.245
Housing, private 0.53 0.36–0.76 0.001 0.48 0.24–0.98 0.045
Alcohol, Y/N 0.72 0.54–0.95 0.020 1.24 0.71–2.15 0.455
Stroke, Y/N 0.28 0.12–0.66 0.004 0.55 0.13–2.35 0.426
High cholesterol, Y/N 0.49 0.39–0.62 <0.001 0.33 0.20–0.53 <0.0001
BMI, kg/m2 1.10 1.07–1.13 <0.001 1.08 1.02–1.14 0.008
HbA1c, %† 22.91 16.13–32.55 <0.001 27.95 18.26–42.79 <0.001
Peripheral artery disease, Y/N 2.06 1.34–3.16 <0.001 2.74 1.14–6.55 0.024
Triglycerides, mmol/L 1.41 1.25–1.59 <0.001 0.85 0.63–1.15 0.297
High-density lipoprotein cholesterol, mmol/L 0.36 0.24–0.53 <0.001 1.56 0.64–3.82 0.328
Low-density lipoprotein cholesterol, mmol/L 0.72 0.64–0.83 <0.001 0.58 0.44–0.76 <0.0001
C Reactive Protein, mg/L 1.01 1.00–1.03 0.038 0.96 0.92–1.00 0.058
Creatinine, μmol/L 1.01 1.00–1.01 0.025 1.00 1.00–1.01 0.406
Table 3.
 
Risk Factors for Diabetes in the SP2 Population Stratified by Race
Table 3.
 
Risk Factors for Diabetes in the SP2 Population Stratified by Race
Risk Factors Chinese Malays Indians
Multivariate Odds Ratio (95% CI) P Multivariate Odds Ratio (95% CI) P Multivariate Odds Ratio (95% CI) P
Age, years 1.05 (1.00–1.90) 0.034
Sex, male 0.77 (0.31–1.95) 0.584
Married, Y/N
Education, secondary and below, Y/N
Unemployed, Y/N
Income, >4000/month 0.63 (0.22–1.80) 0.387
Private housing, Y/N 0.60 (0.24–1.45) 0.256 0.82 (0.22–3.03) 0.771
Smoking, Y/N
Alcohol, Y/N
Reported heart disease, Y/N
Reported stroke, Y/N 0.17 (0.02–1.35) 0.093
SBP, mm Hg 1.01 (0.99–1.03) 0.464 0.49 (0.18–1.32) 0.158
High cholesterol, Y/N 0.70 (0.46–1.08) 0.112 0.43 (0.26–0.71) 0.001 0.97 (0.87–1.08) 0.597
BMI, kg/m2 1.10 (1.01–1.21) 0.038 1.09 (1.00–1.18) 0.046 0.97 (0.87–1.08) 0.597
HbA1c, %* 30.4 (16.13–57.37) <0.001 22.89 (10.55–49.66) <0.001 14.16 (7.15–28.04) <0.001
Chronic kidney disease (CKD), Y/N 2.02 (0.48–8.49) 0.334
Creatinine, μmol/L 0.99 (0.97–1.01) 0.473
Triglycerides, mmol/L 0.96 (0.54–1.70) 0.879 1.21 (0.77–1.91) 0.394 0.97 (0.49–1.92) 0.935
High-density lipoprotein cholesterol, mmol/L 1.42 (0.34–5.99) 0.633 1.46 (0.31–6.82) 0.634
C-reactive protein, mg/L
>1 Reported comorbidities, Y/N
Peripheral artery disease (PAD), Y/N 6.26 (1.84–21.3) 0.003
Dyslipidemia, Y/N 0.75 (0.35–1.59) 0.453
Table 4.
 
Risk Factors for Diabetic Retinopathy in the SP2 Population
Table 4.
 
Risk Factors for Diabetic Retinopathy in the SP2 Population
Risk factors Age- and Sex-Adjusted Odds Ratio 95% CI P Multivariate Odds Ratio 95% CI P *
Chinese 1.00 Reference Reference 1.00 Reference Reference
Malay 1.53 1.11–2.10 0.009 1.86 0.77–4.50 0.170
Indian 1.85 1.36–2.52 <0.001 1.76 0.83–3.73 0.142
Age, y 1.02 1.01–1.03 0.003 1.00 0.96–1.03 0.908
Sex, male 1.47 1.13–1.91 0.004 1.78 0.85–3.74 0.128
Creatinine, μmol/L 1.01 1.00–1.02 <0.001 1.01 1.00–1.03 0.043
HbA1c, % 1.45 1.32–1.59 <0.001 1.25 1.01–1.55 0.036
Duration of diabetes, y 1.06 1.03–1.10 <0.001 1.05 1.01–1.09 0.011
SBP, mm Hg 1.01 1.01–1.02 <0.001 1.01 0.99–1.03 0.271
Education, y 1.74 1.23–2.45 0.002 1.08 0.43–2.73 0.868
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