Ophthalmic Epidemiology, 2014; 21(1): 33–38 ! Informa Healthcare USA, Inc. ISSN: 0928-6586 print / 1744-5086 online DOI: 10.3109/09286586.2013.868004
ORIGINAL ARTICLE
Prevalence of Diabetes and Diabetic Retinopathy in a Brazilian Population Silvana Artioli Schellini1, Geraldo Miranda de Carvalho1, Fabricio Salles Rendeiro1, Carlos Roberto Padovani2, and Flavio Eduardo Hirai3 Faculdade de Medicina de Botucatu, 2Instituto de Biocieˆncias, Universidade Estadual Paulista, Botucatu, Sa˜o Paulo State, Brazil, and 3Escola Paulista de Medicina, Universidade Federal de Sa˜o Paulo, Sa˜o Paulo, Sa˜o Paulo State, Brazil
ABSTRACT Purpose: To evaluate the prevalence of type 2 diabetes mellitus and diabetic retinopathy (DR) in a Brazilian population. Methods: Population-based, cross-sectional study conducted in 9 cities located in the Midwest region of the state of Sa˜o Paulo, Brazil, between 2006 and 2007, including 4690 individuals aged 30 years. Diabetes was self-reported and DR was assessed by indirect ophthalmoscopy. Results: The prevalence of type 2 diabetes was 8.68% (95% confidence interval, CI, 7.87–9.48%), and DR was present in 7.62% (95% CI 5.02–10.20%) of participants with self-reported type 2 diabetes. Approximately 35.4% of individuals diagnosed with DR did not know they had diabetes prior to DR diagnosis. Prevalences of low vision and blindness were higher among those with diabetes and DR. Cataract was still a major cause of blindness in this population. Conclusion: This is the first large population-based study on DR in Brazil. High rates of visual impairment were found in persons with type 2 diabetes, but cataract is still one of the main causes of blindness. Large surveys are necessary for public health policy advocacy in developing countries. Keywords: Blindness, diabetes, epidemiology, prevalence, retinopathy
of DR.7,8 Prior to the onset of vision loss many people lack symptoms, worsening the prognosis for those with DR.1 In patients with type 2 diabetes mellitus, DR is present on average 7 years prior to the detection of the disease.9 The main risk factors for the development or progression of DR are elevated glycosylated hemoglobin, the presence of diabetic neuropathy, hypercholesterolemia, and comorbidities such as hypertension, advanced age (over 60 years),10,11 no knowledge of the disease,12 and disease duration which leads to a higher incidence of DR in the elderly.13,14 Despite current knowledge about the disease, its pathogenesis, risk factors, possible treatments, the
INTRODUCTION In 2000, the number of individuals with diabetes worldwide was approximately 171 million, and more than 5 million of these were blind due to diabetic retinopathy (DR), rates which are expected to increase by 2030.1–3 Diabetes is the leading cause of blindness among the economically active.4–6 The problem worsens in locations further from large urban centers, mainly due to a lack of information among people with diabetes regarding the possibility of developing DR and blindness. Some people with diabetes have limited access to information regarding the prevention and diagnosis
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1
Received 18 October 2012; Revised 30 May 2013; Accepted 5 June 2013; Published online 15 January 2014 Correspondence: Silvana Artioli Schellini, DEP. OFT/ORL/CCP – Faculdade de Medicina de Botucatu – UNESP. Cep: 18618-970, Botucatu, SP, Brazil. E-mail: [email protected]
33
34 S. A. Schellini et al. ability to monitor disease progression and the understanding that early diagnosis and treatment prevents blindness, it is estimated in developing countries that half of the population with diabetes do not undergo fundus examination at least once a year.12 In Brazil, population-based studies on the distribution of DR in the general population are lacking, which motivated the present study. Here, we assess the prevalence of type 2 diabetes and DR in the population of the Midwest region of the state of Sa˜o Paulo.
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MATERIALS AND METHODS Sampling Procedure This was a population-based, cross-sectional ophthalmic survey carried out in households of nine cities of Sa˜o Paulo state in Brazil between 2006 and 2007. The study was approved by the Institutional Review Board and Research Ethics Committee of the Botucatu School of Medicine and was conducted according to the tenets of the Declaration of Helsinki. Informed consent was obtained from participants prior to commencement of the study. Census data (Instituto Brasileiro de Geografia e Estatistica, 2000) were used as the sampling frame. The eligible population consisted of permanent, non-institutionalized residents of the selected households. Participants were selected using a random, household cluster sampling technique. Households were identified systematically according to data from the local census: the first house was selected randomly, the next house was the sixth house on the even-numbered side of the street and so on, successively. The randomly selected households received a letter of invitation to participate in the study and were contacted by telephone to schedule an appointment. Those who agreed to participate were contacted by telephone to schedule an appointment at the Local Health Unit in their city, where the examinations were conducted using an Ophthalmic Mobile Unit. All persons in the selected household were eligible to participate in the study. If there was no answer when the examiners contacted the household or if people refused to participate in the research, the first house to the right was selected. If the next household refused to participate, the first house to the left of the initial house was selected, and so on, successively. To determine the prevalence of visual impairment, estimated at approximately 2% with a precision of 0.5% and level of significance of 5%, it was anticipated that 8000 participants would be required for the study. A total of 7655 individuals agreed to participate. Only participants over 30 years were considered for this study (N = 4690).
Data Collection All examinations were conducted using an Ophthalmic Mobile Unit by a single survey team consisting of seven members, including four ophthalmologists. All study personnel underwent training, and all procedures were standardized prior to commencement. Specific observations were performed by one or two members of the team to minimize interobserver variability. A medical and ophthalmic history was obtained from each participant by qualified healthcare workers, including the collection of demographic data (e.g. age, sex, self-identification of ethnicity), ocular complaints, and general systemic and family health details. Each participant received a comprehensive vision and eye examination in which presenting or uncorrected visual acuity (VA) was measured for the right eye, followed by the left eye, with a consistently illuminated tumbling E Snellen chart at 5 m. VA was then retested with the participants’ existing refraction. If corrected VA was 520/20, objective refraction using a streak retinoscope, trial frames and lenses was performed by the same two ophthalmologists, and best-corrected VA (BCVA) was recorded. If the subject was unable to read the largest letter at 5 m with subjective refraction, testing was repeated at 1 m. If the subject was unable to read the largest letter at 1 m, then VA was recorded as count fingers, hand movements, light perception, or no light perception. Intraocular pressure (IOP) was measured using a non-contact pneumotonometer (CT-60 computerized tonometer, Topcon, Tokyo, Japan), and the mean of three measurements was recorded. If IOP was 425 mmHg then the measurements were repeated using a Goldman tonometer coupled to a slit lamp. Tropicamide 1% with or without phenylephrine 2.5% was instilled for pupil dilatation. Slit lamp biomicroscopy (Shin-Nippon SL101, Tokyo, Japan) with a 90-diopter (D) Volk lens was used for fundus examination. When the media was not clear, the exam was repeated using a Schepens indirect binocular ophthalmoscope with a 20D Volk lens.
Definitions Visual impairment was defined according to the World Health Organization: individuals with BCVA better than 20/60 (0.3) were considered normal; those with BCVA 520/60 were considered to have low vision; and those with BCVA 520/400 (0.05) were considered to be blind. The diagnosis of diabetes was based on self-report. Interviewers asked if the participant had had diabetes since childhood or if it developed during adulthood (type 2). Those who developed diabetes during Ophthalmic Epidemiology
Diabetic Retinopathy in Brazil 35
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childhood (type 1, n = 15) were excluded from the analysis. Assessment of DR was based on ophthalmoscopy in which the following signs of disease were considered: microhemorrhages, hard exudates or cotton wool spots and vascular abnormalities. Patients with abnormalities suggestive of DR were referred to the Botucatu Medical School’s ophthalmology service for confirmation, treatment or monitoring. Hypertension was defined when self-reported by the participant or if on medication. Age was categorized into decades from 30–39 years through to 70 years and over. Race was categorized by self-identification into white, mixed, black, and Asian.
Statistical Analysis The prevalence of DR was calculated based on the sampling design, which was approximated as a onestage cluster design where each household was considered the primary sampling unit. Households were randomly selected, and thus, point prevalence was unbiased. Results are presented as mean and standard deviation or frequency and proportion. Continuous and categorical data were compared using Student’s t-test and 2 test, respectively. Analysis of the association between DR and VA was performed with the variable VA as a binary variable (0.7 versus 50.7), which was then used as the dependent variable in logistic regression models, and odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. Covariables included in the multivariable-adjusted analysis were age, sex, presence of hypertension and cataract. All p values 50.05 were considered statistically significant. All analyses were performed using Stata statistical package version 10 (StataCorp, College Station, Texas, USA).
RESULTS Overall, 4690 subjects, aged 30 years or older, were considered for the present study. The mean age was 51.8 ± 13.6 years, 63.6% were female, and the large majority self-reported as white (91.5%). A total of 185 subjects (3.9%) self-reported as having type 2 diabetes, and 222 subjects (4.7%) self-reported as having type 2 diabetes with associated hypertension. The prevalence of diabetes in this population was 8.68% (n = 407, 95% CI 7.87–9.48%). Table 1 shows comparisons between the characteristics of individuals diagnosed with and those without diabetes. Individuals with type 2 diabetes were older (p50.001), had higher IOP (p = 0.003) and worse VA (p50.001). Of the 48 participants (1.02%) diagnosed with DR, 31 (64.6%) knew they had diabetes. The prevalence of !
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TABLE 1. Characteristics of individuals diagnosed with and without diabetes in the study population, Sa˜o Paulo, Brazil. Diabetes Variable Mean age, years (SD), Age, % 30–39 years 40–49 years 50–59 years 60–69 years 70+ years Sex, % Female Male Ethnicity, % White Mixed Black Asian Mean intraocular pressure, mmHg (SD) Visual acuity, % 0.7 or better 0.3–0.6 0.05–0.2 50.05
No (n = 4283)
Yes (n = 407)
51.2 (13.6)
58.1 (12.2)
22.2 28.4 23.0 14.4 12.0
6.4 19.2 28.5 26.8 19.1
63.3 36.7
66.6 33.4
91.7 6.7 1.2 0.4 13.4 (2.9)
89.7 8.1 1.2 1.0 13.8 (3.3)
85.1 9.1 4.5 1.3
75.2 13.3 9.1 2.5
p Value 50.001 50.001
0.194
0.328
0.003 50.001
SD, standard deviation
DR in those with diabetes was 7.62% (95% CI 5.02– 10.20%). The mean age of individuals with DR was 58.8 ± 10.7 years, similar to those without DR (58.0 ± 12.3 years, p = 0.752). Approximately 67.7% of DR patients were female (versus 66.5% of those without DR, p = 0.887), and 96.8% were white (versus 89.1% of those without DR, p = 0.755; Table 2). Most individuals in the study had BCVA 0.7, with higher proportions of visual impairment and blindness in patients with DR (p = 0.016). The presence of cataract was the most common ophthalmological disorder and was detected in 8.8% of those without DR compared to 9.7% among individuals with DR (p = 0.865). Table 3 shows the multivariable-adjusted analysis of the association between VA and DR. Participants with DR had a 70% higher chance of having VA worse than 0.7, compared to those without DR, adjusted for age, sex, hypertension and cataract (OR 1.70, 95% CI 0.77–3.78). However, the association was not statistically significant. Age and sex were not significantly associated with lower VA. On the other hand, the presence of cataract was associated with a more than 11 times increased chance of having lower VA when compared to those without cataract (OR 11.18, 95% CI 4.72–26.47, adjusted for the other factors in the model).
36 S. A. Schellini et al. TABLE 2. Characteristics of individuals with type 2 diabetes mellitus according to the presence or absence of diabetic retinopathy, Sa˜o Paulo, Brazil.
TABLE 3. Multivariable-adjusted analysis of the association between visual impairment and the presence of diabetic retinopathy among individuals with type 2 diabetes mellitus, Sa˜o Paulo, Brazil.
Diabetic retinopathy
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Variable Mean age, years (SD) Age, % 30–39 years 40–49 years 50–59 years 60–69 years 70+ years Sex, % Female Male Ethnicity, % White Mixed Black Asian Mean intraocular pressure, mmHg (SD) Visual acuity, % 0.7 0.3–0.6 0.05–0.2 50.05 Visual acuity, % Normal Low vision Blind Hypertension, % No Yes Cataract, % No Yes
No (n = 376)
Yes (n = 31)
p Value
58.0 (12.3)
58.8 (10.7)
0.752
6.4 19.4 28.5 26.3 19.4
6.4 16.1 29.0 32.3 16.2 0.887
66.5 33.5
67.7 32.3 0.755
89.1 8.5 1.3 1.1 13.6 (3.3)
96.8 3.2 0 0 12.9 (2.1)
76.3 13.6 7.7 2.4
61.3 9.7 25.8 3.2
76.3 21.3 2.4
61.3 35.5 3.2
44.7 55.7
54.8 45.2
91.2 8.8
90.3 9.7
Diabetic retinopathy No Yes Age, every 5 years Sex Male Female Hypertension No Yes Cataract No Yes
Odds ratioa
95% CI
p Value
1.00 1.70 1.02
0.77–3.78 0.94–1.18
0.190 0.520
1.00 1.57
0.95–2.61
0.077
1.00 1.09
0.93–1.28
0.260
1.00 11.18
4.72–26.47
0.001
CI, confidence interval All variables listed in the table (age, gender, hypertension, and cataract) were included in the model. a
0.298 0.016
0.016
0.275
0.865
SD, standard deviation
DISCUSSION The number of individuals with type 2 diabetes in Brazil and worldwide is growing each year, with an associated increase in prevalence of DR.4,15 In order to better target DR treatment, the epidemiological characteristics of populations must be known. Therefore, this paper analyzes the urban population of small towns in the Midwest region of the state of Sa˜o Paulo, Brazil, where we found the prevalence of diabetes to be 8.6%. A similar DR study conducted in rural Korea showed a prevalence of 6.2%,16 while in the US, DR is present in 4.4% of the general population.17 Brazil is considered to be one of the most mixed populations in the world. Race was classified according to self-report and the majority of subjects in our study considered themselves to be white. In countries with more defined racial groups, such as England, DR was detected in 38% of those of European descent, 52.4% of blacks and 42.3% of Asians.18
There are several methods to screen populations for DR such as the use of direct and indirect ophthalmoscopy,12,16 and methods based on fundus photography with a digital camera19 and even methods using telemedicine.20 The gold standard for DR classification has been the use of fundus photography.12 However, the sensitivity of indirect ophthalmoscopy in the detection of DR is 82% with 95% specificity. It can be considered a valid method for screening, especially in large studies due to its ease of handling and low cost when compared to traditional fundus cameras. It is noted that fundus photography increases the chance of detection of DR, especially those at earlier stages. One study in the United States used fundus photography for screening. This study found a higher detection rate of DR cases, and one of the reasons could have been due to this more accurate method of fundus evaluation.17 However, in studies with a high volume of examinations and limited budget where the population is examined in their place of residence, indirect ophthalmoscopy is often used and it could be considered an acceptable method of examination. Among individuals with diabetes in our sample, DR was present in 7.6%. A study conducted in northeastern Brazil found that DR was present in 24% of those living in the capital city and 39% of the population in other locations within the state.7 The prevalence of DR with type 2 diabetes in Canada is 40%,21 the prevalence in Saudi Arabia varies from 30.2–36.1%,3,22 the prevalence in the USA is 28.5%,17 and the prevalence in Australia is 21.9%.23 Thus, our prevalence rates were substantially lower compared to the prevalence rates in the national and international literature. One reason for this lower prevalence could be due to the diagnostic methods employed. Ophthalmic Epidemiology
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Diabetic Retinopathy in Brazil 37 Despite a lower rate of diabetes in the studied population, the data do not reflect that this population is generally in better health because 35.4% of the individuals who were diagnosed with DR did not know they had diabetes. The number of individuals who were diagnosed with DR but did not know they had diabetes is higher than that reported in the American literature, with rates ranging from 0.6–20%.24 This fact reinforces the need for screening and increased awareness of diabetes and DR, especially because individuals with diabetes could be asymptomatic, and DR may be present before the diagnosis of diabetes is established.16 Visual impairment could be an important issue among those with diabetes.8 The number of individuals with DR that were considered visually impaired (either with low vision or blind) was higher among those with DR. In our study, 38.7% of individuals with DR had either low vision or were blind, a rate higher than similar reports in the US, which varied between 8.3% and 9% for visual impairment.14 In England, the prevalence for visual impairment was 3.4% and 0.39% for blindness.25 However, in Yemen, the rate of blindness in those with diabetes was 16%.26 We further explored the relationship of VA, DR, and cataract in our sample by calculating the prevalence of visual impairment among those with DR without cataract: in those without DR, 17.2% had low vision and 0.9% were blind; in those with DR, 35.7% had low vision and 3.6% were blind. Therefore, cataract had an impact on VA among individuals without DR but little on those with DR. On the other hand, cataract is still one of the main causes of blindness in developing nations and strongly associated with visual impairment as shown in our multivariable model. Other risk factors such as age, sex, and hypertension were not significantly associated with visual impairment in our study. Findings regarding sex are controversial.13,14 A study in the Netherlands found no difference between men and women,11 while in Saudi Arabia, women had a higher prevalence of DR compared to men.3 Age along with duration of diabetes are risk factors for the development of DR.19 DR occurs with higher frequency after long periods of exposure to hyperglycemia and with the presence of other aggravating factors, such as hypertension.14 In our study, we did not find age to be a risk factor for either DR or visual impairment. The association of hypertension with diabetes has been consistently identified as an important risk factor. Hypertension is associated with disease severity and poor prognosis. In our study, a higher proportion of patients with hypertension had DR. This finding has also been reported by others11 but was not statistically significant. Controlled blood pressure was associated with severity of DR in other !
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studies in the US.10,13,17 During 7 years of follow-up visits in individuals with type 2 diabetes, it was observed that systolic and diastolic blood pressures less than 150 mmHg and 85 mmHg, respectively, promoted a reduction of 34% in the progression of DR and a 47% loss of VA.6 Vascular changes, which are common in diabetes and blindness, are considered the most severe outcome, but it is difficult to estimate the proportion of blindness that can be attributed to diabetes. It is known that blindness is 25 times more common in populations with diabetes than in those without.15 Because the definition of hypertension in our study was based on self report and use of medication, our findings should be interpreted with caution. One of the mains strengths of our study is that the evaluations were conducted on a representative, randomized sample population, using a standardized protocol and trained staff. This population could be considered representative of the great majority of populations across the country. To our knowledge there are no population-based data on DR in Brazil. Limitations include the use of self-reported diagnosis for diabetes and hypertension, lack of fundus photography and classification of DR. However, such surveys provide additional information about the study area, providing real data for the development of public health programs on diabetes and its complications. In this population from the Midwest region of the state of Sa˜o Paulo, Brazil, the prevalence of diabetes was 8.68%, and 7.62% of these had DR. Approximately 35.4% of individuals who had a clinical diagnosis of DR did not know they had diabetes. Visual impairment and blindness were more prevalent in individuals with diabetes compared to those without, reinforcing the need for public health policies to address this issue in Brazil.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This study was supported by FAPESP – Fundac¸a˜o de Amparo a Pesquisa do Estado de Sa˜o Paulo, Brazil, Grant number 2000/13713-5.
REFERENCES 1. Bragge P, Gruen RL, Chau M, et al. Screening for presence or absence of diabetic retinopathy – a meta-analysis. Arch Ophthalmol 2011;129(4):435–444. 2. Zhang X, Saaddine JB, Chou CF, et al. Prevalence of diabetic retinopathy in the United States, 2005–2008. JAMA 2010;304(6):649–656.
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38 S. A. Schellini et al. 3. El-Bab MF, Shawky N, Al-Sisi A, Akhtar M. Retinopathy and risk factors in diabetic patients from Al-Madinah Al-Munawarah in the Kingdom of Saudi Arabia. Clin Ophthalmol 2012;6(1):269–276. 4. Ministry of Health. Diabetes Mellitus. Basic guide to diagnosis and treatment. Brasilia: Brazilian Society of Diabetes. 1996:5–7. 5. Chew EY, Klein ML, Ferris 3rd FL, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22. Arch Ophthalmol 1996; 114(9):1079–1084. 6. Klein R, Klein BEK. Are individuals with diabetes seeing better? A long-term epidemiological perspective. Diabetes 2010;59(8):1853–1860. 7. Escaria˜o PHG, Arantes TEF, Figueiroa-Filho NC, et al. Epidemiologia e diferenc¸as regionais da retinopatia diabe´tica em Pernambuco, Brasil (Epidemiology and regional differences of diabetic retinopathy in Pernambuco State, Brazil). Arq Bras Oftalmol 2008;71(2):172–175. 8. Ramos SR, Sabbag FP, Busato D, et al. Retinopatia diabe´tica: estudo de uma associac¸a˜o de diabe´ticos (Diabetic retinopathy: a study of an association of diabetics). Arq Bras Oftalmol 1999;62(6):7357. 9. Harris MI. Undiagnosed NIDDM: clinical and public health issues. Diabetes Care 1993;16:642–652. 10. Davis MD, Fisher MR, Gangnon RE, et al. Risk factors for high-risk proliferative diabetic retinopathy and severe visual loss: Early Treatment Diabetic Retinopathy Study Report 18. Invest Ophthalmol Vis Sci 1998;39(2):233–252. 11. Van Leiden HA, Dekker JM, Moll AC, et al. Risk factors for incident retinopathy in a diabetic and nondiabetic population. The Hoorn Study. Arch Ophthalmol 2003;121:245–251. 12. Rani PK, Raman R, Sharma V, et al. Analysis of a comprehensive diabetic retinopathy screening model for rural and urban diabetics in developing countries. Br J Ophthalmol 2007;91(11):1425–1429. 13. Klein R, Klein B, Moss S, et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984; 102(4):527–532. 14. Roy MS, Klein R, O’Colmain BJ, et al. The prevalence of diabetic retinopathy among adult type 1 diabetic persons in the United States. Arch Ophthalmol 2004;122(4):546–551.
15. Bosco A, Lera´rio AC, Soriano D, et al. Retinopatia diabe´tica. Arq Bras Endocrinol Metabol 2005;49(2):217–227. 16. Kim JH, Kwon HS, Park YM, et al. Prevalence and associated factors of diabetic retinopathy in Rural Korea: the Chungju metabolic disease cohort study. J Korean Med Sci 2011;26(8):1068–1073. 17. Kempen JH, O’Colmain BJ, Leske MC, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol 2004;122(4):552–563. 18. Sivaprasad S, Gupta B, Gulliford MC, et al. Ethnic variations in the prevalence of Diabetic Retinopathy in people with Diabetes attending screening in the United Kingdom (DRIVE UK). PLoS ONE 2012;7(3):e32182. doi:10.1371/journal.pone.0032182. 19. Thomas RL, Dunstan F, Luzio SD, et al. Incidence of diabetic retinopathy in people with type 2 diabetes mellitus attending the Diabetic Retinopathy Screening service for Wales: retrospective analysis. BMJ 2012;344:e874 doi: 10.1136/bmj.e874 (Published 22 February 2012). 20. Alawi EA, Ahmed AA. Screening for diabetic retinopathy: the first Telemedicine approach in a primary care setting in Bahrain. Middle East Afr J Ophthalmol 2012;19(3):295–298. 21. Ross SA, McKenna A, Mozejko S, Fick GH. Diabetic retinopathy in native and nonnative Canadians. Exp Diab Res 2007; 2007:Article ID 76271, 6 pages. doi:10.1155/2007/ 76271. 22. Alqurashi KA, Aljabri KS, Bokhari SA. Prevalence of diabetes mellitus in a Saudi community. Ann Saudi Med 2011;31(1):19–23. 23. Tapp RJ, Shaw JE, Harper CA, et al; Aus Diab Study Group. The prevalence of and factors associated with diabetic retinopathy in the Australian population. Diabetes Care 2003;26(6):1731–1737. 24. Scanlon PH, Foy C, Chen FK. Visual acuity measurement and ocular co-morbidity in diabetic retinopathy screening. Br J Ophthalmol 2008;92(6):775–778. 25. Sivaprasad S, Gupta B, Gulliford MC, et al. Ethnic variation in the prevalence of Visual impairment in people attending diabetic retinopathy screening in the United Kingdom (DRIVE UK). PLoS ONE 7(6):e39608. doi:10.1371/journal.pone.0039608. 26. Bamashmus MA, Gunaid AA, Khandekar RB. Diabetic retinopathy, visual impairment and ocular status among patients with diabetes mellitus in Yemen: a hospital-based study. Indian J Ophthalmol 2009;57(4):293–298.
Ophthalmic Epidemiology
ORIGINAL ARTICLE
Prevalence of Diabetes and Diabetic Retinopathy in a Brazilian Population Silvana Artioli Schellini1, Geraldo Miranda de Carvalho1, Fabricio Salles Rendeiro1, Carlos Roberto Padovani2, and Flavio Eduardo Hirai3 Faculdade de Medicina de Botucatu, 2Instituto de Biocieˆncias, Universidade Estadual Paulista, Botucatu, Sa˜o Paulo State, Brazil, and 3Escola Paulista de Medicina, Universidade Federal de Sa˜o Paulo, Sa˜o Paulo, Sa˜o Paulo State, Brazil
ABSTRACT Purpose: To evaluate the prevalence of type 2 diabetes mellitus and diabetic retinopathy (DR) in a Brazilian population. Methods: Population-based, cross-sectional study conducted in 9 cities located in the Midwest region of the state of Sa˜o Paulo, Brazil, between 2006 and 2007, including 4690 individuals aged 30 years. Diabetes was self-reported and DR was assessed by indirect ophthalmoscopy. Results: The prevalence of type 2 diabetes was 8.68% (95% confidence interval, CI, 7.87–9.48%), and DR was present in 7.62% (95% CI 5.02–10.20%) of participants with self-reported type 2 diabetes. Approximately 35.4% of individuals diagnosed with DR did not know they had diabetes prior to DR diagnosis. Prevalences of low vision and blindness were higher among those with diabetes and DR. Cataract was still a major cause of blindness in this population. Conclusion: This is the first large population-based study on DR in Brazil. High rates of visual impairment were found in persons with type 2 diabetes, but cataract is still one of the main causes of blindness. Large surveys are necessary for public health policy advocacy in developing countries. Keywords: Blindness, diabetes, epidemiology, prevalence, retinopathy
of DR.7,8 Prior to the onset of vision loss many people lack symptoms, worsening the prognosis for those with DR.1 In patients with type 2 diabetes mellitus, DR is present on average 7 years prior to the detection of the disease.9 The main risk factors for the development or progression of DR are elevated glycosylated hemoglobin, the presence of diabetic neuropathy, hypercholesterolemia, and comorbidities such as hypertension, advanced age (over 60 years),10,11 no knowledge of the disease,12 and disease duration which leads to a higher incidence of DR in the elderly.13,14 Despite current knowledge about the disease, its pathogenesis, risk factors, possible treatments, the
INTRODUCTION In 2000, the number of individuals with diabetes worldwide was approximately 171 million, and more than 5 million of these were blind due to diabetic retinopathy (DR), rates which are expected to increase by 2030.1–3 Diabetes is the leading cause of blindness among the economically active.4–6 The problem worsens in locations further from large urban centers, mainly due to a lack of information among people with diabetes regarding the possibility of developing DR and blindness. Some people with diabetes have limited access to information regarding the prevention and diagnosis
20 14
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1
Received 18 October 2012; Revised 30 May 2013; Accepted 5 June 2013; Published online 15 January 2014 Correspondence: Silvana Artioli Schellini, DEP. OFT/ORL/CCP – Faculdade de Medicina de Botucatu – UNESP. Cep: 18618-970, Botucatu, SP, Brazil. E-mail: [email protected]
33
34 S. A. Schellini et al. ability to monitor disease progression and the understanding that early diagnosis and treatment prevents blindness, it is estimated in developing countries that half of the population with diabetes do not undergo fundus examination at least once a year.12 In Brazil, population-based studies on the distribution of DR in the general population are lacking, which motivated the present study. Here, we assess the prevalence of type 2 diabetes and DR in the population of the Midwest region of the state of Sa˜o Paulo.
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MATERIALS AND METHODS Sampling Procedure This was a population-based, cross-sectional ophthalmic survey carried out in households of nine cities of Sa˜o Paulo state in Brazil between 2006 and 2007. The study was approved by the Institutional Review Board and Research Ethics Committee of the Botucatu School of Medicine and was conducted according to the tenets of the Declaration of Helsinki. Informed consent was obtained from participants prior to commencement of the study. Census data (Instituto Brasileiro de Geografia e Estatistica, 2000) were used as the sampling frame. The eligible population consisted of permanent, non-institutionalized residents of the selected households. Participants were selected using a random, household cluster sampling technique. Households were identified systematically according to data from the local census: the first house was selected randomly, the next house was the sixth house on the even-numbered side of the street and so on, successively. The randomly selected households received a letter of invitation to participate in the study and were contacted by telephone to schedule an appointment. Those who agreed to participate were contacted by telephone to schedule an appointment at the Local Health Unit in their city, where the examinations were conducted using an Ophthalmic Mobile Unit. All persons in the selected household were eligible to participate in the study. If there was no answer when the examiners contacted the household or if people refused to participate in the research, the first house to the right was selected. If the next household refused to participate, the first house to the left of the initial house was selected, and so on, successively. To determine the prevalence of visual impairment, estimated at approximately 2% with a precision of 0.5% and level of significance of 5%, it was anticipated that 8000 participants would be required for the study. A total of 7655 individuals agreed to participate. Only participants over 30 years were considered for this study (N = 4690).
Data Collection All examinations were conducted using an Ophthalmic Mobile Unit by a single survey team consisting of seven members, including four ophthalmologists. All study personnel underwent training, and all procedures were standardized prior to commencement. Specific observations were performed by one or two members of the team to minimize interobserver variability. A medical and ophthalmic history was obtained from each participant by qualified healthcare workers, including the collection of demographic data (e.g. age, sex, self-identification of ethnicity), ocular complaints, and general systemic and family health details. Each participant received a comprehensive vision and eye examination in which presenting or uncorrected visual acuity (VA) was measured for the right eye, followed by the left eye, with a consistently illuminated tumbling E Snellen chart at 5 m. VA was then retested with the participants’ existing refraction. If corrected VA was 520/20, objective refraction using a streak retinoscope, trial frames and lenses was performed by the same two ophthalmologists, and best-corrected VA (BCVA) was recorded. If the subject was unable to read the largest letter at 5 m with subjective refraction, testing was repeated at 1 m. If the subject was unable to read the largest letter at 1 m, then VA was recorded as count fingers, hand movements, light perception, or no light perception. Intraocular pressure (IOP) was measured using a non-contact pneumotonometer (CT-60 computerized tonometer, Topcon, Tokyo, Japan), and the mean of three measurements was recorded. If IOP was 425 mmHg then the measurements were repeated using a Goldman tonometer coupled to a slit lamp. Tropicamide 1% with or without phenylephrine 2.5% was instilled for pupil dilatation. Slit lamp biomicroscopy (Shin-Nippon SL101, Tokyo, Japan) with a 90-diopter (D) Volk lens was used for fundus examination. When the media was not clear, the exam was repeated using a Schepens indirect binocular ophthalmoscope with a 20D Volk lens.
Definitions Visual impairment was defined according to the World Health Organization: individuals with BCVA better than 20/60 (0.3) were considered normal; those with BCVA 520/60 were considered to have low vision; and those with BCVA 520/400 (0.05) were considered to be blind. The diagnosis of diabetes was based on self-report. Interviewers asked if the participant had had diabetes since childhood or if it developed during adulthood (type 2). Those who developed diabetes during Ophthalmic Epidemiology
Diabetic Retinopathy in Brazil 35
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childhood (type 1, n = 15) were excluded from the analysis. Assessment of DR was based on ophthalmoscopy in which the following signs of disease were considered: microhemorrhages, hard exudates or cotton wool spots and vascular abnormalities. Patients with abnormalities suggestive of DR were referred to the Botucatu Medical School’s ophthalmology service for confirmation, treatment or monitoring. Hypertension was defined when self-reported by the participant or if on medication. Age was categorized into decades from 30–39 years through to 70 years and over. Race was categorized by self-identification into white, mixed, black, and Asian.
Statistical Analysis The prevalence of DR was calculated based on the sampling design, which was approximated as a onestage cluster design where each household was considered the primary sampling unit. Households were randomly selected, and thus, point prevalence was unbiased. Results are presented as mean and standard deviation or frequency and proportion. Continuous and categorical data were compared using Student’s t-test and 2 test, respectively. Analysis of the association between DR and VA was performed with the variable VA as a binary variable (0.7 versus 50.7), which was then used as the dependent variable in logistic regression models, and odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. Covariables included in the multivariable-adjusted analysis were age, sex, presence of hypertension and cataract. All p values 50.05 were considered statistically significant. All analyses were performed using Stata statistical package version 10 (StataCorp, College Station, Texas, USA).
RESULTS Overall, 4690 subjects, aged 30 years or older, were considered for the present study. The mean age was 51.8 ± 13.6 years, 63.6% were female, and the large majority self-reported as white (91.5%). A total of 185 subjects (3.9%) self-reported as having type 2 diabetes, and 222 subjects (4.7%) self-reported as having type 2 diabetes with associated hypertension. The prevalence of diabetes in this population was 8.68% (n = 407, 95% CI 7.87–9.48%). Table 1 shows comparisons between the characteristics of individuals diagnosed with and those without diabetes. Individuals with type 2 diabetes were older (p50.001), had higher IOP (p = 0.003) and worse VA (p50.001). Of the 48 participants (1.02%) diagnosed with DR, 31 (64.6%) knew they had diabetes. The prevalence of !
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TABLE 1. Characteristics of individuals diagnosed with and without diabetes in the study population, Sa˜o Paulo, Brazil. Diabetes Variable Mean age, years (SD), Age, % 30–39 years 40–49 years 50–59 years 60–69 years 70+ years Sex, % Female Male Ethnicity, % White Mixed Black Asian Mean intraocular pressure, mmHg (SD) Visual acuity, % 0.7 or better 0.3–0.6 0.05–0.2 50.05
No (n = 4283)
Yes (n = 407)
51.2 (13.6)
58.1 (12.2)
22.2 28.4 23.0 14.4 12.0
6.4 19.2 28.5 26.8 19.1
63.3 36.7
66.6 33.4
91.7 6.7 1.2 0.4 13.4 (2.9)
89.7 8.1 1.2 1.0 13.8 (3.3)
85.1 9.1 4.5 1.3
75.2 13.3 9.1 2.5
p Value 50.001 50.001
0.194
0.328
0.003 50.001
SD, standard deviation
DR in those with diabetes was 7.62% (95% CI 5.02– 10.20%). The mean age of individuals with DR was 58.8 ± 10.7 years, similar to those without DR (58.0 ± 12.3 years, p = 0.752). Approximately 67.7% of DR patients were female (versus 66.5% of those without DR, p = 0.887), and 96.8% were white (versus 89.1% of those without DR, p = 0.755; Table 2). Most individuals in the study had BCVA 0.7, with higher proportions of visual impairment and blindness in patients with DR (p = 0.016). The presence of cataract was the most common ophthalmological disorder and was detected in 8.8% of those without DR compared to 9.7% among individuals with DR (p = 0.865). Table 3 shows the multivariable-adjusted analysis of the association between VA and DR. Participants with DR had a 70% higher chance of having VA worse than 0.7, compared to those without DR, adjusted for age, sex, hypertension and cataract (OR 1.70, 95% CI 0.77–3.78). However, the association was not statistically significant. Age and sex were not significantly associated with lower VA. On the other hand, the presence of cataract was associated with a more than 11 times increased chance of having lower VA when compared to those without cataract (OR 11.18, 95% CI 4.72–26.47, adjusted for the other factors in the model).
36 S. A. Schellini et al. TABLE 2. Characteristics of individuals with type 2 diabetes mellitus according to the presence or absence of diabetic retinopathy, Sa˜o Paulo, Brazil.
TABLE 3. Multivariable-adjusted analysis of the association between visual impairment and the presence of diabetic retinopathy among individuals with type 2 diabetes mellitus, Sa˜o Paulo, Brazil.
Diabetic retinopathy
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Variable Mean age, years (SD) Age, % 30–39 years 40–49 years 50–59 years 60–69 years 70+ years Sex, % Female Male Ethnicity, % White Mixed Black Asian Mean intraocular pressure, mmHg (SD) Visual acuity, % 0.7 0.3–0.6 0.05–0.2 50.05 Visual acuity, % Normal Low vision Blind Hypertension, % No Yes Cataract, % No Yes
No (n = 376)
Yes (n = 31)
p Value
58.0 (12.3)
58.8 (10.7)
0.752
6.4 19.4 28.5 26.3 19.4
6.4 16.1 29.0 32.3 16.2 0.887
66.5 33.5
67.7 32.3 0.755
89.1 8.5 1.3 1.1 13.6 (3.3)
96.8 3.2 0 0 12.9 (2.1)
76.3 13.6 7.7 2.4
61.3 9.7 25.8 3.2
76.3 21.3 2.4
61.3 35.5 3.2
44.7 55.7
54.8 45.2
91.2 8.8
90.3 9.7
Diabetic retinopathy No Yes Age, every 5 years Sex Male Female Hypertension No Yes Cataract No Yes
Odds ratioa
95% CI
p Value
1.00 1.70 1.02
0.77–3.78 0.94–1.18
0.190 0.520
1.00 1.57
0.95–2.61
0.077
1.00 1.09
0.93–1.28
0.260
1.00 11.18
4.72–26.47
0.001
CI, confidence interval All variables listed in the table (age, gender, hypertension, and cataract) were included in the model. a
0.298 0.016
0.016
0.275
0.865
SD, standard deviation
DISCUSSION The number of individuals with type 2 diabetes in Brazil and worldwide is growing each year, with an associated increase in prevalence of DR.4,15 In order to better target DR treatment, the epidemiological characteristics of populations must be known. Therefore, this paper analyzes the urban population of small towns in the Midwest region of the state of Sa˜o Paulo, Brazil, where we found the prevalence of diabetes to be 8.6%. A similar DR study conducted in rural Korea showed a prevalence of 6.2%,16 while in the US, DR is present in 4.4% of the general population.17 Brazil is considered to be one of the most mixed populations in the world. Race was classified according to self-report and the majority of subjects in our study considered themselves to be white. In countries with more defined racial groups, such as England, DR was detected in 38% of those of European descent, 52.4% of blacks and 42.3% of Asians.18
There are several methods to screen populations for DR such as the use of direct and indirect ophthalmoscopy,12,16 and methods based on fundus photography with a digital camera19 and even methods using telemedicine.20 The gold standard for DR classification has been the use of fundus photography.12 However, the sensitivity of indirect ophthalmoscopy in the detection of DR is 82% with 95% specificity. It can be considered a valid method for screening, especially in large studies due to its ease of handling and low cost when compared to traditional fundus cameras. It is noted that fundus photography increases the chance of detection of DR, especially those at earlier stages. One study in the United States used fundus photography for screening. This study found a higher detection rate of DR cases, and one of the reasons could have been due to this more accurate method of fundus evaluation.17 However, in studies with a high volume of examinations and limited budget where the population is examined in their place of residence, indirect ophthalmoscopy is often used and it could be considered an acceptable method of examination. Among individuals with diabetes in our sample, DR was present in 7.6%. A study conducted in northeastern Brazil found that DR was present in 24% of those living in the capital city and 39% of the population in other locations within the state.7 The prevalence of DR with type 2 diabetes in Canada is 40%,21 the prevalence in Saudi Arabia varies from 30.2–36.1%,3,22 the prevalence in the USA is 28.5%,17 and the prevalence in Australia is 21.9%.23 Thus, our prevalence rates were substantially lower compared to the prevalence rates in the national and international literature. One reason for this lower prevalence could be due to the diagnostic methods employed. Ophthalmic Epidemiology
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Diabetic Retinopathy in Brazil 37 Despite a lower rate of diabetes in the studied population, the data do not reflect that this population is generally in better health because 35.4% of the individuals who were diagnosed with DR did not know they had diabetes. The number of individuals who were diagnosed with DR but did not know they had diabetes is higher than that reported in the American literature, with rates ranging from 0.6–20%.24 This fact reinforces the need for screening and increased awareness of diabetes and DR, especially because individuals with diabetes could be asymptomatic, and DR may be present before the diagnosis of diabetes is established.16 Visual impairment could be an important issue among those with diabetes.8 The number of individuals with DR that were considered visually impaired (either with low vision or blind) was higher among those with DR. In our study, 38.7% of individuals with DR had either low vision or were blind, a rate higher than similar reports in the US, which varied between 8.3% and 9% for visual impairment.14 In England, the prevalence for visual impairment was 3.4% and 0.39% for blindness.25 However, in Yemen, the rate of blindness in those with diabetes was 16%.26 We further explored the relationship of VA, DR, and cataract in our sample by calculating the prevalence of visual impairment among those with DR without cataract: in those without DR, 17.2% had low vision and 0.9% were blind; in those with DR, 35.7% had low vision and 3.6% were blind. Therefore, cataract had an impact on VA among individuals without DR but little on those with DR. On the other hand, cataract is still one of the main causes of blindness in developing nations and strongly associated with visual impairment as shown in our multivariable model. Other risk factors such as age, sex, and hypertension were not significantly associated with visual impairment in our study. Findings regarding sex are controversial.13,14 A study in the Netherlands found no difference between men and women,11 while in Saudi Arabia, women had a higher prevalence of DR compared to men.3 Age along with duration of diabetes are risk factors for the development of DR.19 DR occurs with higher frequency after long periods of exposure to hyperglycemia and with the presence of other aggravating factors, such as hypertension.14 In our study, we did not find age to be a risk factor for either DR or visual impairment. The association of hypertension with diabetes has been consistently identified as an important risk factor. Hypertension is associated with disease severity and poor prognosis. In our study, a higher proportion of patients with hypertension had DR. This finding has also been reported by others11 but was not statistically significant. Controlled blood pressure was associated with severity of DR in other !
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studies in the US.10,13,17 During 7 years of follow-up visits in individuals with type 2 diabetes, it was observed that systolic and diastolic blood pressures less than 150 mmHg and 85 mmHg, respectively, promoted a reduction of 34% in the progression of DR and a 47% loss of VA.6 Vascular changes, which are common in diabetes and blindness, are considered the most severe outcome, but it is difficult to estimate the proportion of blindness that can be attributed to diabetes. It is known that blindness is 25 times more common in populations with diabetes than in those without.15 Because the definition of hypertension in our study was based on self report and use of medication, our findings should be interpreted with caution. One of the mains strengths of our study is that the evaluations were conducted on a representative, randomized sample population, using a standardized protocol and trained staff. This population could be considered representative of the great majority of populations across the country. To our knowledge there are no population-based data on DR in Brazil. Limitations include the use of self-reported diagnosis for diabetes and hypertension, lack of fundus photography and classification of DR. However, such surveys provide additional information about the study area, providing real data for the development of public health programs on diabetes and its complications. In this population from the Midwest region of the state of Sa˜o Paulo, Brazil, the prevalence of diabetes was 8.68%, and 7.62% of these had DR. Approximately 35.4% of individuals who had a clinical diagnosis of DR did not know they had diabetes. Visual impairment and blindness were more prevalent in individuals with diabetes compared to those without, reinforcing the need for public health policies to address this issue in Brazil.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This study was supported by FAPESP – Fundac¸a˜o de Amparo a Pesquisa do Estado de Sa˜o Paulo, Brazil, Grant number 2000/13713-5.
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38 S. A. Schellini et al. 3. El-Bab MF, Shawky N, Al-Sisi A, Akhtar M. Retinopathy and risk factors in diabetic patients from Al-Madinah Al-Munawarah in the Kingdom of Saudi Arabia. Clin Ophthalmol 2012;6(1):269–276. 4. Ministry of Health. Diabetes Mellitus. Basic guide to diagnosis and treatment. Brasilia: Brazilian Society of Diabetes. 1996:5–7. 5. Chew EY, Klein ML, Ferris 3rd FL, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22. Arch Ophthalmol 1996; 114(9):1079–1084. 6. Klein R, Klein BEK. Are individuals with diabetes seeing better? A long-term epidemiological perspective. Diabetes 2010;59(8):1853–1860. 7. Escaria˜o PHG, Arantes TEF, Figueiroa-Filho NC, et al. Epidemiologia e diferenc¸as regionais da retinopatia diabe´tica em Pernambuco, Brasil (Epidemiology and regional differences of diabetic retinopathy in Pernambuco State, Brazil). Arq Bras Oftalmol 2008;71(2):172–175. 8. Ramos SR, Sabbag FP, Busato D, et al. Retinopatia diabe´tica: estudo de uma associac¸a˜o de diabe´ticos (Diabetic retinopathy: a study of an association of diabetics). Arq Bras Oftalmol 1999;62(6):7357. 9. Harris MI. Undiagnosed NIDDM: clinical and public health issues. Diabetes Care 1993;16:642–652. 10. Davis MD, Fisher MR, Gangnon RE, et al. Risk factors for high-risk proliferative diabetic retinopathy and severe visual loss: Early Treatment Diabetic Retinopathy Study Report 18. Invest Ophthalmol Vis Sci 1998;39(2):233–252. 11. Van Leiden HA, Dekker JM, Moll AC, et al. Risk factors for incident retinopathy in a diabetic and nondiabetic population. The Hoorn Study. Arch Ophthalmol 2003;121:245–251. 12. Rani PK, Raman R, Sharma V, et al. Analysis of a comprehensive diabetic retinopathy screening model for rural and urban diabetics in developing countries. Br J Ophthalmol 2007;91(11):1425–1429. 13. Klein R, Klein B, Moss S, et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984; 102(4):527–532. 14. Roy MS, Klein R, O’Colmain BJ, et al. The prevalence of diabetic retinopathy among adult type 1 diabetic persons in the United States. Arch Ophthalmol 2004;122(4):546–551.
15. Bosco A, Lera´rio AC, Soriano D, et al. Retinopatia diabe´tica. Arq Bras Endocrinol Metabol 2005;49(2):217–227. 16. Kim JH, Kwon HS, Park YM, et al. Prevalence and associated factors of diabetic retinopathy in Rural Korea: the Chungju metabolic disease cohort study. J Korean Med Sci 2011;26(8):1068–1073. 17. Kempen JH, O’Colmain BJ, Leske MC, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol 2004;122(4):552–563. 18. Sivaprasad S, Gupta B, Gulliford MC, et al. Ethnic variations in the prevalence of Diabetic Retinopathy in people with Diabetes attending screening in the United Kingdom (DRIVE UK). PLoS ONE 2012;7(3):e32182. doi:10.1371/journal.pone.0032182. 19. Thomas RL, Dunstan F, Luzio SD, et al. Incidence of diabetic retinopathy in people with type 2 diabetes mellitus attending the Diabetic Retinopathy Screening service for Wales: retrospective analysis. BMJ 2012;344:e874 doi: 10.1136/bmj.e874 (Published 22 February 2012). 20. Alawi EA, Ahmed AA. Screening for diabetic retinopathy: the first Telemedicine approach in a primary care setting in Bahrain. Middle East Afr J Ophthalmol 2012;19(3):295–298. 21. Ross SA, McKenna A, Mozejko S, Fick GH. Diabetic retinopathy in native and nonnative Canadians. Exp Diab Res 2007; 2007:Article ID 76271, 6 pages. doi:10.1155/2007/ 76271. 22. Alqurashi KA, Aljabri KS, Bokhari SA. Prevalence of diabetes mellitus in a Saudi community. Ann Saudi Med 2011;31(1):19–23. 23. Tapp RJ, Shaw JE, Harper CA, et al; Aus Diab Study Group. The prevalence of and factors associated with diabetic retinopathy in the Australian population. Diabetes Care 2003;26(6):1731–1737. 24. Scanlon PH, Foy C, Chen FK. Visual acuity measurement and ocular co-morbidity in diabetic retinopathy screening. Br J Ophthalmol 2008;92(6):775–778. 25. Sivaprasad S, Gupta B, Gulliford MC, et al. Ethnic variation in the prevalence of Visual impairment in people attending diabetic retinopathy screening in the United Kingdom (DRIVE UK). PLoS ONE 7(6):e39608. doi:10.1371/journal.pone.0039608. 26. Bamashmus MA, Gunaid AA, Khandekar RB. Diabetic retinopathy, visual impairment and ocular status among patients with diabetes mellitus in Yemen: a hospital-based study. Indian J Ophthalmol 2009;57(4):293–298.
Ophthalmic Epidemiology
