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Prevalence of Vitreoretinal Disorders in a Rural Population of Southern India
The Aravind Comprehensive Eye Study
Praveen K. Nirmalan, MD, MPH;
Joanne Katz, PhD;
Alan L. Robin, MD;
James M. Tielsch, PhD;
Perumalsamy Namperumalsamy, MD;
Ramasamy Kim, MD;
V. Narendran, MD;
Rengappa Ramakrishnan, MD;
Ramasamy Krishnadas, MD;
Ravilla D. Thulasiraj, MBA;
Eric Suan, MD
Arch Ophthalmol. 2004;122:581-586.
ABSTRACT
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Objective To determine the magnitude of vitreoretinal disorders in a rural southern Indian population.
Methods Cluster sampling was used to identify individuals 40 years and older in Tamil Nadu in southern India. Demographic details, vision measurement and refraction using logMAR charts, anterior segment slitlamp examination, dilated posterior segment slitlamp examination using a 78-diopter (D) lens, and indirect ophthalmoscopy using a 20-D lens were performed.
Results Complete retinal data were available for 4917 (95.5%) of the 5150 persons examined. The prevalence of any vitreoretinal disorder was 10.4% (95% confidence interval [CI], 9.5%-11.3%). The population prevalence of bilateral blindness among persons with vitreoretinal disorders was 0.3% (95% CI, 0.2%-0.5%). The prevalence of diabetic retinopathy was 0.5% (95% CI, 0.3%-0.7%) in the general population and 10.5% (95% CI, 6.5%-14.5%) in patients with diabetes mellitus. Only 6.7% of individuals with diabetic retinopathy had previous ophthalmic examinations. The prevalences of early and late age-related macular degeneration were 2.7% (95% CI, 2.2%-3.2%) and 0.6% (95% CI, 0.4%-0.8%), respectively.
Conclusions Vitreoretinal diseases appear to be a major public health problem in India. Emphasis on diabetic screening, diabetic therapy, and appropriate laser therapy of diabetic retinopathy must be explored.
INTRODUCTION
Nearly 80% of the considerable burden of blindness in India is attributed to curable causes, such as cataracts and refractive errors.1 A recent study2 found that retinal disorders are an important cause of blindness in India. It is estimated that there will be 244 million people (14.9% of the population) 65 years and older by 2050 compared with 42 million (4.5% of the population) in 1995.3 This shift in demographics is likely to be accompanied by a shift in the prevalence of retinal diseases as major causes of blindness in India. Several studies4-7 report on the prevalence of diabetic retinopathy (DR) in urban populations of India; however, there is a lack of information on the prevalence of DR in rural India. Although age-related macular degeneration (AMD) is a major cause of blindness in European-derived populations and has been previously reported8-13 at a lower prevalence in pigmented populations, there is no information on the prevalence of AMD in India. Such information is essential to understand the magnitude of the problem and the need for services, including rehabilitation. This article reports on the prevalence of vitreoretinal disorders in a rural population of southern India.
METHODS
The Aravind Comprehensive Eye Study is a population-based prevalence study of vision and other eye diseases in a rural population 40 years and older in 3 districts—Madurai, Tirunelveli, and V.O Chidambaranar—in the state of Tamil Nadu in southern India. The study design and methods are described in detail elsewhere.14 In brief, 50 representative clusters were selected from these 3 districts by using stratified, multistage cluster sampling. Demographic details were collected from all enumerated individuals after completion of a door-to-door survey by trained interviewers. All individuals 40 years and older were invited to the base hospital (Aravind Eye Hospital, Madurai, India) for comprehensive eye examinations, which included initial and best-corrected distance and near visual acuity using illiterate E LogMAR charts, slitlamp biomicroscopy for the external eye and anterior segment, applanation tonometry for intraocular pressures, gonioscopy using a Goldmann single-mirror contact lens (Ocular Instruments Inc, Bellevue, Wash), and slitlamp lens grading using the Lens Opacities Classification System III.15 All participants with open anterior chamber angles determined by gonioscopy using the Schaffer classification had their pupils dilated with either 1% tropicamide or 10% phenylephrine hydrochloride. Participants who had dilation deferred because of occludable or narrow angles underwent dilated examinations after laser iridotomy on the same day or on a subsequent day. Fundus examinations after dilation were performed using a 78-diopter (D) lens at the slitlamp and indirect ophthalmoscopy with a 20-D lens. Determination of retinal disorders was primarily based on clinical evidence, and supportive laboratory investigations were not always performed for logistical reasons. Retinal photography was not attempted because of cost and logistics. All findings were confirmed by a fellowship-trained retinal specialist.
Three levels of informed consent were used in this study—community, household, and individual. Meetings were held with community leaders and all health-related personnel in the area to explain the purpose of the study. Once approval was obtained at these meetings, the study was fully explained to all adults in the household to address any concerns and to secure consent for the household to participate. Before screening and definitive examinations, the study was explained in detail to all potential participants, the consent statement was read to each individual, and their voluntary consent was solicited. All informed consent was verbally obtained, as a substantial proportion of this population is illiterate. We did not obtain thumbprints as this was considered problematic because many villagers have been conned into giving away property by providing thumbprints to documents that they could not read. The study was approved, and annually reapproved, by the Committee on Human Research at the Johns Hopkins Bloomberg School of Public Health and by the Ethical Review Committee of the Aravind Eye and Children's Hospitals. This investigation adhered to the tenets of the Declaration of Helsinki.
The assessment of diabetes mellitus was based on either the use of diabetic medications or a postprandial blood sugar level of 180 mg/dL or greater ( 10.0 mmol/L). We did not measure glycosylated hemoglobin levels as this measurement was not available at the time of the study in southern India. Based on fundus findings, regardless of a history of diabetes mellitus or glucose levels, we used the modified classification of DR based on the retinopathy levels used by Klein et al16 to categorize persons with DR. Briefly, DR was classified as nonproliferative (levels 1-3), preproliferative (levels 4 and 5), or proliferative (levels 6 and 7).16 The presence of clinically significant macular edema was assessed using a 90-D lens at the slitlamp. The presence of retinal photocoagulation scars was assessed using indirect ophthalmoscopy.
We classified epiretinal membranes based on the method used by Klein et al17 and the more recent Blue Mountains Eye Study.18 We identified 2 types of epiretinal membranes: an early "cellophane macular reflex," described as a "glinting water silk, shifting light reflex" due to a thin layer of preretinal cells, initially causing little distortion of the retinal surface, and a later stage of premacular fibrosis, occurring as the membrane thickens and contracts, with the appearance of superficial retinal folds or traction lines, becoming opaque or gray.19
Age-related macular degeneration was assessed independent of visual acuity measurements using a slitlamp with a 78-D lens after adequate pupillary dilation was achieved. Age-related macular degeneration was defined according to the international classification20 developed by the International ARM Epidemiological Study Group. Briefly, drusen were defined as discrete whitish-yellow spots external to the neuroretinal pigment epithelium or retinal pigment epithelium (RPE). The largest drusen determined the grade for maximum drusen size and predominant drusen type. Type was based on the size of drusen, uniformity of appearance across the breadth, and the sharpness of edges. Soft distinct drusen have uniform density and sharp edges, and soft indistinct drusen have decreasing density from the center outward and fuzzy edges. Pigmentary abnormalities included either increased pigmentation associated with drusen or depigmentation or hypopigmentation of the RPE, more sharply demarcated than drusen, without any visibility of choroidal vessels associated with drusen. Geographic atrophy was defined as any sharply delineated approximately round or oval area of hypopigmentation or depigmentation or apparent absence of the RPE in which choroidal vessels are more visible than in surrounding areas, at least 175 µm. Exudative AMD was defined as the presence of any of the following: (1) RPE detachments or serous detachment of the sensory retina, (2) subretinal or sub-RPE neovascular membranes, (3) subretinal hemorrhages, and (4) epiretinal, subretinal, intraretinal, or sub–pigment epithelial scar or glial tissue or fibrinlike deposits. Early AMD was defined as the presence of soft large drusen (>125 µm) with pigment epithelial abnormalities, as described previously herein. Late AMD was defined as the presence of signs of exudative AMD or geographic atrophy.
We defined systemic hypertension as either a measured systolic blood pressure of 140 mm Hg or greater or a diastolic blood pressure of 90 mm Hg or greater or current use of systemic antihypertensive medications. We analyzed serum cholesterol level as a categorical variable; values greater than 200 mg/dL (>5.17 mmol/L) were considered high. We used height and weight measurements of individual participants to calculate body mass index (BMI) (calculated as weight in kilograms divided by height [meters squared]). We classified individuals as lean if the BMI was less than 20 for men and less than 19 for women, as normal if the BMI was 20 to 25 for men and 19 to 24 for women, as overweight if the BMI was 25 to 30 for men and 24 to 29 for women, and as obese if the BMI was greater than 30 for men and greater than 29 for women.21 We elicited a history of smoking; the duration of smoking was estimated for current smokers from the age at which participants started smoking and the current age and for past smokers from the age at which participants started smoking and the age at which they stopped smoking. Data regarding the number of cigarettes or beedis (a beedi is tobacco rolled in dried leaves) smoked per day was elicited for current and past smokers and was used to estimate smoking-years. We classified smoking-years as zero years, low (below the 25th percentile), medium (25th-75th percentile), and high (above the 75th percentile).
Statistical analysis was performed using a software package (Stata version 7.0; Stata Corp, College Station, Tex). The 95% confidence intervals (CIs) of the prevalence estimates were calculated using a Poisson approximation of the binomial distribution. Bivariate and multivariate analyses were used to look for associations between risk factors and early and late AMD.
RESULTS
We performed comprehensive clinical examinations on 5150 (93%) of the 5339 enumerated individuals 40 years and older. Of the 5150 individuals examined, complete retinal data were available for 4917 (95.5%). Media opacities, particularly age-related cataracts, were the major reason for not having adequate retinal data. The median age of these 4917 persons was 50.0 years (range, 40-90 years; mean, 52.5 years), and 55.0% were women. Participants without retinal data available were more likely to be older (aged 60 years; P <.001). There were no differences in sex between those who had retinal data available and those who did not.
Increasing age was associated with vitreoretinal disorders (P <.001) (Table 1). There were no significant differences in the age-adjusted prevalence of vitreoretinal disorders between sexes. The prevalence of various vitreoretinal disorders in this population, by eyes, is given in Table 2. The prevalence of any vitreoretinal disorder, including AMD, was 10.8% (95% CI, 9.9%-11.8%); after excluding AMD, the prevalence was 8.2% (95% CI, 7.4%-9.0%).
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Table 1. Age and Sex Distribution of Vitreoretinal Diseases in the Study Population
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Table 2. Prevalence of Vitreoretinal Disorders, Excluding Age-Related Macular Degeneration, in 789 Eyes (402 Individuals)
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Diabetes mellitus was present in 142 persons (4.0%) younger than 60 years, 59 (4.9%) aged 60 to 69 years, and 27 (6.5%) aged 70 years and older (overall population prevalence, 4.4%; 95% CI, 3.8%-5.0%). Diabetic retinopathy was present in 14 persons (0.4%) younger than 60 years, 6 (0.6%) aged 60 to 69 years, and 4 (1.2%) aged 70 years or older (overall population prevalence, 0.5%; 95% CI, 0.3%-0.7%). The population prevalence was 0.4% (95% CI, 0.3%-0.7%) for nonproliferative DR, 0.04% (95% CI, 0.005%-0.15%) for preproliferative DR, 0.06% (95% CI, 0.01%-0.18%) for proliferative DR, and 0.06% (95% CI, 0.01%-0.18%) for clinically significant macular edema. Among people with diabetes mellitus, the prevalence of nonproliferative DR was 9.2% (95% CI, 5.7%-14.1%), of preproliferative DR was 0.9% (95% CI, 0.1%-3.2%), and of proliferative DR was 1.3% (95% CI, 0.2%-3.8%). Among those who were aware of their diabetic status, 58.3% had clinical evidence of DR. Only 12.5% of those with DR in this study had a previous ophthalmic examination, including 6.7% who were aware of their diabetic status.
An epiretinal membrane was present in 14 persons (population prevalence, 0.3%; 95% CI, 0.2%-0.5%). We did not find Eales disease in any eye.
The prevalence of early and late AMD increased significantly with increasing age (P <.001) (Table 3). There was no evidence that sex was associated with either early or late AMD after adjusting for age (P = .70) (Table 3). The median age of individuals with any AMD was 58 years (range, 40-82 years), and 52.9% were women. The age-specific prevalence of AMD was 1.3% (95% CI, 0.1%-1.9%) for those aged 40 to 49 years, 3.9% (95% CI, 2.9%-5.0%) for those aged 50 to 59 years, 5.0% (95% CI, 3.8%-6.5%) for those aged 60 to 69 years, and 6.9% (95% CI, 4.4%-10.3%) for those 70 years and older. The prevalence of early AMD was 2.7% (95% CI, 2.2%-3.2%), and that of late AMD was 0.6% (95% CI, 0.4%-0.8%). The age-adjusted (adjusted to the population estimates for 2000 for India [from the US Census Bureau, International Data Base, October 2002 version]) prevalence of AMD was 3.1% (95% CI, 2.7%-3.6%).
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Table 3. Prevalence of Soft Drusen, Pigmentary Changes, Geographic Atrophy, and Exudative Changes in the Study Population by Age and Sex*
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Soft large drusen greater than 125 µm were present in 95 persons (population prevalence, 1.9%; 95% CI, 1.6%-2.4%), pigmentary changes were present in 40 persons (0.8%; 95% CI, 0.6%-1.1%), exudative changes were present in 6 persons (0.1%; 95% CI, 0.0%-0.3%), and geographic atrophy was present in 23 persons (0.5%; 95% CI, 0.3%-0.7%). Exudative changes were not found in individuals younger than 60 years.
Systemic hypertension (odds ratio [OR], 1.19; 95% CI, 0.8-1.7), diabetes mellitus (OR, 1.12; 95% CI, 0.5-2.3), history of smoking (OR, 0.90; 95% CI, 0.6-1.3), and smoking-years (OR, 0.92; 95% CI, 0.6-1.3) were not significantly associated with AMD. Serum cholesterol levels greater than 200 mg/dL (>5.17 mmol/L) were protective on univariate analysis for early AMD (OR, 0.44; 95% CI, 0.3-0.8). Adjustment for multiple risk factors did not change the observed associations to any appreciable degree (Table 4).
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Table 4. Multiple Logistic Regression Analyses for Associations With AMD
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Of the 1834 eyes with initial visual acuity worse than 6/60 in both eyes, 56 (3.1%) had any retinal disorder present. After best correction, 127 persons with AMD (78.9%) had visual acuity of 6/18 or better, 4 (2.5%) had visual acuity between 6/60 and 3/60, and 1 (0.6%) had visual acuity worse than 3/60. After best correction, 1 person with DR (4.4%) had visual acuity worse than 6/60. Overall, 19 persons (3.5%) with any vitreoretinal disorder had visual acuity worse than 6/60 after best correction. However, the prevalence of bilateral blindness attributable to vitreoretinal diseases was 0.3% (95% CI, 0.1%-0.5%).
COMMENT
Population-based data on the magnitude of disease is essential to plan for required services. Previous studies2, 4-7 from India have merely mentioned that retinal disorders cause blindness or have focused on DR.
The lack of fundus photographs is a limitation of this study. However, all participants were subject to a dilated fundus examination using slitlamp biomicroscopy with a 78-D lens and indirect ophthalmoscopy with a 20-D lens, and all findings were confirmed by a fellowship-trained retinal specialist. It is possible that we may have underestimated the prevalence of vitreoretinal disorders in the absence of fundus photographs. Five percent of individuals who had comprehensive eye examinations did not have complete retinal data available. These persons were statistically significantly older than participants and were more likely to have retinal disorder. Therefore, the total prevalence reported may be an underestimate, although there is no indication of selection bias in the age-sex analyses.
A population prevalence of bilateral blindness of 0.3% after best correction among persons with vitreoretinal disorders suggests that vitreoretinal disorders may not currently be a major public health problem in India. This prevalence is similar to the 0.2% (95% CI, 0.1%-0.3%) reported by another study2 in a different state in India. However, the relatively higher prevalence of any vitreoretinal disorder, including AMD (10.8%; 95% CI, 9.9%-11.8%), in older age groups is indicative of the potential for vitreoretinal disorders to contribute to the burden of blindness in India as the population demographics shift toward aging. The population older than 65 years is expected to be 137 million by 2021 (compared with 42 million in 1995).22 It is also estimated that there will be a rapid increase in the number of persons with diabetes mellitus—approximately 57 million patients with diabetes mellitus in India by 2025 compared with 19 million in 1995.23 The challenge the ophthalmic health care system in India may face is evident when we consider that if even as low as 5% to 10% of the estimated 57 million individuals with diabetes mellitus (by 2025) develop severe retinopathy, approximately 3 to 6 million persons may require laser or surgical intervention for severe DR within the next 2 decades. Getting these people into the eye care delivery system at an appropriate time to preserve vision could be a major challenge, especially considering that only 6.7% of those who were aware of their diabetic status had visited an ophthalmologist (and none of the visits occurred in the year immediately preceding this study). This suggests the need for increased awareness in the community regarding vitreoretinal diseases and their potential for causing blindness and the need for improved networking between internists and ophthalmologists to ensure that all those with systemic diseases that have a potential for affecting the eye receive an ophthalmic examination, including dilated fundus examinations.
The association of AMD with increasing age in this study is similar to other studies in different populations.24-27 We did not find statistically significant sex differences in the prevalence of AMD, and neither did we find an association between cigarette smoking or systemic hypertension and AMD. There have been conflicting findings on the association of smoking with AMD.28-32
Serum cholesterol levels greater than 200 mg/dL (>5.17 mmol/L) were found to be protective for early AMD in our study. However, this study was limited in that we did not measure individual lipid components other than cholesterol. The Beaver Dam Eye Study33 did not show any association between AMD and serum cholesterol levels. Body mass index was not statistically significantly associated with AMD in our study population after adjusting for other factors, in contrast to the POLA (Pathologies Oculaires Liées à l'Age) study,27 which reported ORs of 2.3 (95% CI, 1.0-2.5) for late AMD and 1.5 (95% CI, 1.1-2.3) for pigmentary changes among obese individuals (BMI >30). Other population-based studies34-35 have shown increased risk as BMI increases, but these results were not statistically significant. The differences in association of risk factors such as serum cholesterol level, diabetes mellitus, and BMI in the study population compared with other populations may be related to a lower prevalence of these risk factors in this rural southern Indian population. Less than 25% of our population had a serum cholesterol level greater than 200 mg/dL (>5.17 mmol/L), less than 5% had diabetes mellitus, and less than 8% were obese.
Currently available therapies for AMD are not curative and are priced much higher than services for other easily treatable conditions, such as cataracts or refractive errors, in India. The relatively low affordability of therapeutic services for AMD and the low potential of current treatment modalities to preserve vision will mean that a sizable number of patients with AMD may remain visually impaired or blind. Therefore, greater emphasis should be placed on rehabilitative and low-vision services, an underdeveloped specialty area in India.
We did not find any cases of Eales disease in the study sample, suggesting that the population prevalence of this disease may actually be much lower than previously believed. There could be several reasons for this. First, Eales disease is more common at a younger age, usually in the early to middle 30s, and our study population was 40 years and older. In addition, more diagnostic laboratory tests are available now and have led to the identification of specific entities that were likely to be classified as Eales disease in the past.
Strategies to address the issue of vitreoretinal disorders in India, besides focusing on infrastructure development, including trained personnel and low-vision and rehabilitative services, should also look at current ophthalmic practices in India. Residency programs need to be more comprehensive in nature to include training for certain levels of interventions for vitreoretinal diseases, including lasers. Dilated fundus examinations, at least at baseline, have to be made mandatory for all patients unless otherwise contraindicated. Such examinations should use slitlamp biomicroscopy and indirect ophthalmoscopy. Eye care programs and practitioners need to develop wider networks with internists and physicians to ensure that ophthalmic examinations are performed in patients with systemic illness associated with ocular complications, most notably diabetes mellitus. Further studies are required to understand the changing trends in vitreoretinal diseases in India and their risk factors so that effective preventive strategies can be formulated.
AUTHOR INFORMATION
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Corresponding author: Alan L. Robin, MD, Lake Falls Professional Building, 6115 Falls Rd, Suite 333, Baltimore, MD 21209-2226 (e-mail: glaucomaexpert{at}cs.com).
Submitted for publication June 16, 2003; final revision received November 24, 2003; accepted December 8, 2003.
From Aravind Medical Research Foundation, Aravind Eye Care System, Madurai, India (Drs Nirmalan, Namperumalsamy, Kim, Narendran, Ramakrishnan, and Krishnadas and Mr Thulasiraj); the Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Md (Drs Katz, Robin, and Tielsch); the Dana Center for Preventive Ophthalmology, Johns Hopkins University Schools of Medicine and Public Health (Drs Katz and Tielsch); the Department of Ophthalmology, Johns Hopkins University School of Medicine (Dr Robin); and the Department of Ophthalmology, University of Maryland School of Medicine, Baltimore (Dr Suan). The authors have no relevant financial interest in this article.
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