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(Investigative Ophthalmology and Visual Science. 2005;46:2328-2333.)
© 2005 by The Association for Research in Vision and Ophthalmology, Inc.
DOI:  10.1167/iovs.05-0019
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Prevalence of Diabetic Retinopathy in Urban India: The Chennai Urban Rural Epidemiology Study (CURES) Eye Study, I

Mohan Rema, Sundaram Premkumar, Balaji Anitha, Raj Deepa, Rajendra Pradeepa, and Viswanathan Mohan

From the Madras Diabetes Research Foundation, Chennai, India.


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
PURPOSE. To assess the prevalence of diabetic retinopathy (DR) in type 2 diabetic subjects in urban India using four-field stereo color photography.

METHODS. The Chennai Urban Rural Epidemiology Study (CURES) is a population-based study conducted on a representative population of Chennai (formerly Madras) city in South India. Individuals ≥20 years in age (n = 26,001) were screened for diabetes. Of the 1529 known diabetic subjects, 1382 (90.4%) participated in the study. Subjects with newly detected diabetes (n = 354) by the oral glucose tolerance test (OGTT) also consented to participate in the study. All the subjects underwent four-field stereo color photography, and retinopathy was graded in the color fundus photographs according to Early Treatment Diabetic Retinopathy Study (ETDRS) criteria.

RESULTS. The overall prevalence of DR in the population was 17.6% (95% confidence interval [CI]: 15.8–19.5), which included 20.8% (95% CI: 18.7–23.1) in known diabetic subjects and 5.1% (95% CI: 3.1–8.0) in subjects with newly detected diabetes. The prevalence of DR was significantly higher in men than in women (21.3% vs. 14.6%; P < 0.0001) and among subjects with proteinuria (P = 0.002). Logistic regression analysis showed that for every 5-year increase in the duration of diabetes, the risk for DR increased 1.89-fold (95% CI: 1.679–2.135; P < 0.0001). For every 2% elevation of glycated hemoglobin (HbA1c), the risk for DR increased by a factor of 1.7 (95% CI: 1.545–1.980; P < 0.0001).

CONCLUSIONS. This study shows that the prevalence of diabetic retinopathy is lower in urban South Indians than in other ethnic groups. However, due to the large number of diabetic subjects, DR is likely to pose a public health burden in India; hence, routine retinal examination is mandatory to detect DR in the early stages.

Diabetic retinopathy (DR) is the leading cause of visual impairment in the Western world, particularly among persons of working age.1 2 It is estimated that DR develops in more than 75% of diabetic patients within 15 to 20 years of diagnosis of diabetes.3 4 Several epidemiologic studies have provided valuable information on the prevalence of DR in Western countries that is useful for identifying subgroups at risk and for the planning of public health policies.5 The Eye Diseases Prevalence Research Group collates data on eye diseases in the United States, and provides information on the health services burden due to eye diseases, including DR.5 However, there is a paucity of data on the prevalence of diabetes-related eye diseases in developing countries such as India, which in fact has the largest number of diabetic individuals in the world.

According to the latest World Health Organization (WHO) report, India has 31.7 million diabetic subjects, and the number is expected to increase to a staggering 79.4 million by 2030.6 Furthermore, type 2 diabetes in Indians differs from that in Europeans in several aspects: The onset is at a younger age,7 obesity is less common,8 and genetic factors appear to be stronger.9 These clinical differences and the rising prevalence of diabetes in India10 warrant well-conducted epidemiologic studies on diabetes-related complications in this population, to assess the health services burden due to diabetes. Although a few studies have been conducted on the prevalence of DR in urban and rural population in India, such studies have had several limitations: some were clinic-based11 12 ; two earlier population-based studies13 14 were limited to self-reported diabetic subjects and involved small sample sizes; retinal examination was performed with direct ophthalmoscopy in both the studies; and the only study in which retinal photography was used restricted this technique to the few patients with retinopathy detected by ophthalmoscopy.13

The limitations of these studies underscore the need for large population-based studies involving a representative sample of the population including both self-reported and newly diagnosed diabetic subjects, by using standard documentation techniques and an international grading system. This formed the basis of the present study.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 References
 
The study subjects were recruited from the urban component of the Chennai Urban Rural Epidemiology Study (CURES). CURES is an ongoing epidemiologic study involving a representative population of Chennai (formerly Madras), in southern India, the fourth largest city in India, with a population of approximately 4.2 million. The city of Chennai is divided into 155 corporation wards representing a socioeconomically diverse group. The methodology of the study has been published elsewhere.15 Briefly, in phase 1, in the urban component of CURES, individuals were screened by a systematic sampling technique from 46 corporation wards representative of the various social tiers in Chennai. Individuals (n = 26,001) aged ≥20 years were screened. The selection criterion was set at 20 years of age because of the younger age at onset of type 2 diabetes in Indians.7 Self-reported diabetic subjects who were receiving drug treatment for diabetes were classified as "known diabetic (KD) subjects." Fasting capillary blood glucose was determined with a glucose meter (One Touch Basic; LifeScan, Johnson & Johnson, Milpitas, CA) in all subjects.

In phase 2 of CURES, all the KD subjects (n = 1529) were invited to the center for detailed studies on vascular complications. In addition, subjects with fasting blood glucose levels in the diabetic range based on the American Diabetes Association (ADA) fasting criteria16 underwent oral glucose tolerance test (OGTT) after a 75-g oral glucose load (dissolved in 250 mL of water). Those confirmed by OGTT to have 2-hour plasma glucose ≥200 mg/dL based on the WHO consulting group criterion17 were labeled "newly detected diabetic (ND) subjects."

Of the total 1529 KD subjects, 1382 participated in the study (response rate: 90.4%), and all had type 2 diabetes as defined by the absence of ketosis and adequate insulin reserve; 354 ND diabetic subjects also participated in the study.

The institutional ethics committee’s approval was obtained and informed consent was obtained from all study subjects, in accordance with the guidelines of the Declaration of Helsinki.

Justification of Sample Size
The sample size was computed based on the following assumptions: Earlier published studies on selected populations in India have suggested that the prevalence of known diabetes in urban areas is ~5.0%.10 To assess the risk factors of DR, a minimum of 200 subjects with retinopathy was necessary. The prevalence of DR obtained in our earlier population-based study (21.4%)18 showed that 1000 diabetic subjects had to be recruited. To obtain 1000 adult (≥20 years) diabetic individuals, the sample size calculated ranged from 16,000 to 24,000, using 99% confidence intervals and 0.5% error. The upper limit of 24,000 was taken as our target. However, considering a study withdrawal rate of 10% among the diabetic subjects we decided to screen 26,000 individuals for the study.10 18 19

Clinical and Biochemical Studies
Anthropometric measurements including weight, height, and waist measurements were obtained using standardized techniques. The body mass index (BMI) was calculated by the usual formula: weight in kilograms divided by height in meters squared. Blood pressure was recorded in the sitting position in the right arm to the nearest 2 mm Hg with a mercury sphygmomanometer (Diamond Deluxe; Industrial Electronic and Products, Electronic Co-op Estate, Pune, India). Two readings were taken 5 minutes apart, and the mean of the two was taken as the final blood pressure reading of the individual.

A fasting blood sample was taken after ensuring 8 hours of overnight fasting for estimation of plasma glucose and serum lipids with an autoanalyzer (Hitachi 912; Roche Diagnostics GmbH, Mannheim, Germany) using kits supplied by the manufacturer. Glycated hemoglobin (HbA1c) was measured by high-pressure liquid chromatography (HPLC), using the variant machine (Bio-Rad, Hercules, CA).

Urine samples were collected in the early morning after an overnight fast. Fourteen subjects refused to give urine samples. Urine creatinine was measured using Jaffe’s method. Urinary protein was measured on spot urine by the sulfosalicylic acid technique.20 Expected protein excretion was calculated by the protein-creatinine ratio method, and overt proteinuria was defined as ≥500 mg/d.20

Ocular Examination
A comprehensive ocular examination was performed on all study subjects by trained optometrists. Visual acuity was recorded with an illuminated Snellen chart. The presenting and best corrected visual acuity was documented separately for each eye.

Retinal Studies
The pupils were dilated with 1 drop of phenylephrine (10%) and tropicamide (1%) in both eyes, and the drops were repeated until the best possible mydriasis was obtained. Four-field stereo color retinal photography was performed by trained and certified photographers who had participated in other international studies with a camera (FF 450 plus camera; Carl Zeiss Meditec, Jena, Germany) and 35-mm color transparencies. The four fields taken were stereoscopic pictures of the macula, disc, and superior temporal and inferior temporal quadrants.21 Thirty-five millimeter color retinal photography was used because of better clarity and the stereo effect, which is not possible with digital photography. If photography of any particular eye or any field was not possible due to inadequate dilatation, inability to cooperate properly, or opacities in the media, these were specified as "missing eyes or fields."

Grading of Retinal Photographs
The photographs were coded with an identification number and assessed in a masked manner to minimize any possible bias. Photographs were viewed against a light board using Donaldson’s stereo viewer and were graded with the ETDRS grading system.22

The minimum criterion for diagnosis of DR was the presence of at least one definite microaneurysm in any field photographed. Photographs were assessed and assigned a retinopathy level, and the final diagnosis for each patient was determined from the grading of the worse eye according to the ETDRS criteria for severity of disease in the individual eye.

Diabetic macular edema (DME) was defined as retinal thickening at or within 1 disc diameter of the center of the macula or the presence of definite hard exudates.23 Clinically significant macular edema (CSME) was diagnosed according to ETDRS criteria, when one or more of the following were detected: retinal thickening involving the center of the macula or within 500 µm of the center; hard exudates at or within 500 µm of the center of the macula associated with the thickening of the adjacent retina; and a zone or zones of retinal thickening that occupied one disc area or more, with any portion of the retinal thickening being located within 1 disc diameter of the center of the macula.23 DME was diagnosed with a macular grid. It may be present in the nonproliferative (NP)DR or the proliferative (P)DR stage. However, once PDR was detected, the final grading was taken as PDR in this study.

Two investigators graded the photographs independently. A subset of photographs of 100 patients was assessed for interobserver variation. The unweighted {kappa} statistic for agreement was 0.97, indicating excellent agreement. If there was disagreement between the two investigators, a third investigator graded the photographs, and that grade was taken as the final diagnosis.

Definitions
Diabetes.
Type 2 diabetes mellitus (DM) was diagnosed by a self-reported history of physician diagnosis or those who were on drug treatment for diabetes (insulin or oral hypoglycemic agents) as KD subjects or by 2-hour postglucose load level of ≥200 mg/dL as ND diabetic subjects.17

Hypertension.
Hypertension was defined as a self-reported history of physician diagnosis or subjects who were receiving drug treatment for hypertension or a systolic blood pressure (SBP) of ≥140 mm Hg and/or diastolic blood pressure (DBP) of ≥90 mm Hg.24

Coronary Artery Disease.
Coronary artery disease (CAD) was diagnosed based on a history of documented myocardial infarction and/or drug treatment for CAD (aspirin or nitrates).

Smoking.
Individuals were classified as nonsmokers or current smokers.

Statistical Analysis
Results are expressed as the mean ± SD. Student’s t-test was used to compare continuous variables, and the {chi}2 test was used to compare proportions among groups. Subjects who would not give urine samples (n = 14) were excluded from the analysis of proteinuria. Logistic regression analysis was performed using DR as the dependent variable to identify the risk factors for DR. P < 0.05 was considered significant. All analysis was performed on computer (SPSS for Windows, ver. 10.0; SPSS Science, Chicago, IL).


   Results
Top
 Abstract
 Methods
 Results
Discussion
 References
 
Of 1529 known diabetic subjects, 1382 (90.4%) responded to the invitation to participate in the study. There were no significant differences in the baseline values between the 1382 responders and the 147 nonresponders (responders versus nonresponders: age, 52 ± 11 years vs. 51 ± 9 years, P = 0.212; men, 46.1% vs. 51.9%, P = 0.195; fasting plasma glucose, 169 ± 72 mg/dL vs. 171 ± 72 mg/dL, P = 0.331; systolic blood pressure: 130 ± 21 mm Hg vs. 128 ± 25 mm Hg, P = 0.351; and diastolic blood pressure, 78 ± 12 mm Hg vs. 77 ± 11 mm Hg, P = 0.333). The remaining analyses are restricted to data from the responders (n = 1382).

Of the 1736 diabetic subjects recruited, color fundus photographs could not be taken in 21 subjects for various reasons, which included opacities in the ocular media, inability to cooperate or unwillingness to undergo photography, among others. Opacities in the ocular media also prevented photography of the right eye of 36 subjects and left eyes of another 36 subjects. However, the eye that could be photographed was taken for the analysis. Hence, 1715 subjects were photographed (1364 KD and 351 ND). The quality of the photographs was excellent to good in 1469 (85.6%) and was satisfactory in the remainder.

The mean age of the study population (n = 1715) was 52 ± 11 years, and 45% (n = 769) of the diabetic subjects were men. Of the subjects, 17.6% were smokers, 5.2% had CAD, and 48.7% had hypertension. KD subjects were older (53 ± 11 years vs. 48 ± 12 years; P < 0.001), had higher fasting plasma glucose (164 ± 71 mg/dL vs. 149 ± 60 mg/dL; P < 0.001) and higher glycated hemoglobin levels (8.8% ± 2.3% vs. 8.3% ± 2.0%; P < 0.001) compared with ND diabetic subjects. The mean duration of diabetes in the KD subjects was 5.9 ± 5.3 years, which was determined from the data obtained from the diabetic individual.

Table 1 presents the prevalence of DR in the study population. The overall prevalence of DR in the population was 17.6% (95% confidence interval [CI]: 15.8–19.5). Among the KD subjects, 20.8% (95% CI: 18.7–23.08) had DR, whereas 5.1% (95% CI: 3.1–8.0) of ND subjects had DR. KD subjects had a higher frequency of all the grades of retinopathy than did ND cases. Prevalence of DME in the total diabetic population was 5.0%, whereas among the KD subjects it was 6.3% and among the ND subjects, 1.1%. The prevalence of CSME was 2.4%.


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  		TABLE 1. Prevalence of DR in the Study Groups

 
Table 2 compares the prevalence of DR in different populations determined by retinal photography.5 25 26 27 28 The prevalence of DR in Indians appeared to be lower than that reported in other populations.


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  		TABLE 2. Prevalence Rates of Diabetic Retinopathy in Different Population Studies

 
Table 3 compares the prevalence of DR in the different categories. There was no linear trend in the prevalence of DR with increase in the age at onset. The prevalence of DR was significantly higher in men, 21.3% (164/769), compared with 14.6% (138/946) in women (P < 0.0001). Of the 1364 subjects with self reported diabetes, 1112 (81.5%) were taking oral hypoglycemic agents, 111 (8.1%) were on insulin, and 141 (10.3%) were on a dietary regimen. Of the subjects on insulin, 46.8% had DR compared with 20.0% in those using oral hypoglycemic agents (P < 0.001).


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  		TABLE 3. Prevalence of DR in the Subgroups Studied

 
The prevalence of DR was higher among subjects with proteinuria (P = 0.002). Among diabetic subjects with hypertension, the prevalence of DR was higher, but this did not reach statistical significance, as was also the case in self-reported subjects with CAD. There was no significant difference in the prevalence of DR between smokers and nonsmokers.

Subjects with retinopathy were older (53 ± 10 years vs. 50 ± 11 years; P = 0.001) and had a longer duration of diabetes (7.9 ± 6.2 years vs. 4.5 ± 4.8 years; P < 0.001), lower body mass index (24 ± 4.1 kg/m2 vs. 25.5 ± 4.3 kg/m2; P < 0.001), higher fasting plasma glucose (192 ± 77 mg/dL vs. 154 ± 65 mg/dL; P < 0.001) and higher HbA1c (9.8% ± 2.3% vs. 8.4% ± 2.2%; P < 0.001) than did the subjects without retinopathy.

Table 4 shows the prevalence of DR in relation to duration of diabetes. Severity of retinopathy proportionally increased with longer duration of diabetes, as shown by the trend {chi}2 analysis (trend {chi}2: 120.7; P < 0.0001).


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  		TABLE 4. Prevalence of DR Relative to the Duration of Diabetes

 
Table 5 presents the result of regression analysis, with DR as the dependent variable. The odds ratio for DR was higher with increases in HbA1c and duration of diabetes. For every 5-year increase in duration of diabetes, the risk for development of DR increased 1.89-fold. For every 2% elevation of HbA1c, the risk for DR increased by a factor of 1.7. The influence of glycemic control on the risk for DR was computed for different duration intervals. For every 2% increase in HbA1c, the risk for DR was higher in those with longer duration of diabetes.


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  		TABLE 5. Regression Analysis with DR as the Dependent Variable

 

   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
References
 
Various population-based studies performed in India during the past 30 years have indicated an increased prevalence of type 2 diabetes. In 1972, the first population-based study on prevalence of diabetes conducted by the Indian Council of Medical Research reported that 2% of the urban Indians were affected by diabetes.29 Recent studies indicate that this statistic has increased to 12%.10 This increase has been attributed to the rapid economic, demographic, and nutritional transition experienced in India,19 30 which has led to lifestyle changes resulting in an increased prevalence of diabetes. However, few studies have attempted to assess the prevalence of diabetic complications in India.13 14 20 31 32 33 In this study, we report the prevalence of DR in type 2 diabetic subjects in an urban population in south India based on a large epidemiologic survey.

This study suggests that the prevalence of DR in Indians is lower than that reported among Europeans. This confirms the findings in earlier, smaller studies in India. A recent study in the neighboring state of Andhra Pradesh in South India, involving KD subjects examined by ophthalmoscopy, reported a 22.4% prevalence of DR,13 whereas a similar study on self-reported diabetic subjects identified by questionnaire in Kerala revealed a prevalence of 26.8%.14 In the present study, the prevalence of DR was 20.8% among KD subjects in the population of Chennai, which is lower than that reported by us in a clinic-based study (34.1%).11 The latter may be a reflection of the referral bias to a specialized tertiary care center for treatment of diabetic eye complications.

The prevalence of DR among ND subjects in this study was 5.1%, which is also lower than the 7.3%, reported earlier in our clinic-based population.12 These data are strikingly lower than those reported in Europe, where the prevalence of retinopathy at diagnosis has been reported to vary from 20% to 35%.4 34 35 In the United Kingdom Prospective Diabetes Study (UKPDS), the prevalence of DR at the time of diagnosis was 35%, but the study subjects in that study were much older than those in the present study (age range, 25–65 years; mean, 53 years). However, even when categorized based on age (>50 years) the prevalence of DR in our study population was lower (8.3%) than that in the UKPDS. Moreover, age does not seem to be a confounding factor, as the Asian Young Diabetes Research (ASDIAB) study, in which young diabetic subjects of age 12 to 40 years were recruited in several Asian countries also showed a lower prevalence of DR in Indians compared with other Asian groups.36 It is noteworthy that the ASDIAB study used the same methods as were used in the present study for retinal photography, and the photographs were graded centrally. This similarity raises the possibility that there are differences in susceptibility to DR in different ethnic groups. Genetic susceptibility to DR is supported by an earlier study by our group that suggested that the siblings of probands with retinopathy had a threefold higher risk of DR than did the siblings of probands without DR.37 The report from the Diabetes Control and Complications Trial (DCCT) Research Group also suggested that the risk of severe retinopathy was high among the relatives of subjects with DR compared with the risk in those without DR.38

Retinopathy was more common among the men in our study. A similar male preponderance has been reported by the UKPDS study,35 the Hyderabad study,13 and a study of Pima Indians.27 However, the reason for this is unclear and merits further investigation.

The prevalence of retinopathy was higher in those on insulin treatment in our study, which is perhaps explained by the fact that subjects with retinopathy may have been preferentially treated with insulin. Similar findings have been reported in the study of Pima Indians27 and in the Beaver Dam study.39 In contrast, in American Indians in Oklahoma, the prevalence of DR was higher in those on oral hypoglycemic agents rather than on insulin treatment.40 In the Wisconsin Epidemiologic Study of Diabetic Retinopathy (WESDR), it was shown that among the older diabetic subjects, after adjustment for HbA1c level, there was no association of insulin treatment with either the incidence or progression of retinopathy.4

The major risk factors for DR in this study were duration of diabetes and degree of glycemic control, consistent with findings in previous studies.41 42 43 Logistic regression analysis revealed that for every 5-year increase in duration of diabetes, the risk for DR was increased by 1.89-fold, whereas a 2% increase in HbA1c resulted in a 1.7-fold increase in risk for DR.

The strengths of this study are that it was based on retinal photography and standard grading techniques, and it was also the first study from India to report on the prevalence of DR using stereo retinal color photography. Moreover, the study included a large representative population, and results could be extrapolated to the whole of urban India. A limitation of the study is that, because it was a cross-sectional study, no information on causality was obtained.

Although the actual percentage of DR observed in the present study is low, if one were to extrapolate these results to all of India, the number would still be quite staggering. Presently there are more than 31.7 million diabetic individuals in India, and if 17.6% have DR, this would translate to more than 5.6 million subjects with DR. Furthermore, the number of diabetic subjects is expected to increase to 79.4 million by 2030, which could translate into a heavy economic burden and compromise the quality of life. This anticipated increase in cases underscores the need for large-scale training of skilled personnel for screening and treatment of diabetic eye disease.

In conclusion, the present study suggests that among urban south Indians studied by us, the prevalence of DR is lower than in other ethnic groups. However, given the large number of diabetic subjects in India, even with the lower prevalence rates, DR still poses an enormous public health and economic burden for India. This emphasizes the need for routine retinal screening of diabetic individuals to detect DR in the early stages.


   Acknowledgements
 
The authors thank the epidemiologic team headed by Shanthi Rani for their help and Manjula Datta, MD (Professor and Head, Department of Epidemiology, Tamil Nadu Dr. MGR Medical University, Chennai) for valuable suggestions.


   Footnotes
 
Supported by the Chennai Willingdon Corporate Foundation.

Submitted for publication January 7, 2005; accepted February 15, 2005.

Disclosure: M. Rema, None; S. Premkumar, None; B. Anitha, None; R. Deepa, None; R. Pradeepa, None; V. Mohan, None

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: Mohan Rema, Department of Ophthalmology, Madras Diabetes Research Foundation, 4 Conran Smith Road, Gopalapuram, Chennai 600 086, India; drrema{at}vsnl.com.


   References
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 Discussion
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