|Year : 2020 | Volume
| Issue : 2 | Page : 76-83
Diabetic retinopathy among Omanis: Prevalence and clinical profile
Puspalata Agroiya1, Abdul Hakeem Alrawahi2, Fathimabeebi Pambinezhuth3, Noor Bader Al Busaidi3
1 National Diabetes and Endocrine Centre, Royal Hospital, Seeb, Oman
2 Department of Research and Studies, Oman Medical Specialty Board, Muscat, Oman
3 National Diabetes and Endocrine Centre, Royal hospital, Muscat, Oman
|Date of Submission||30-Sep-2019|
|Date of Decision||13-Nov-2019|
|Date of Acceptance||16-Dec-2019|
|Date of Web Publication||28-May-2020|
National Diabetes and Endocrine Centre, Royal Hospital, P C 111, P. O. Box 1331, Seeb, Muscat
Source of Support: None, Conflict of Interest: None
| Abstract|| |
PURPOSE: The aim of this study is to describe the prevalence, severity and clinical profile of diabetic retinopathy (DR) among Omani diabetic patients attending a tertiary care hospital.
MATERIALS AND METHODS: This is a retrospective study involving the record review of diabetic patients attending the diabetes retina clinic of the National Diabetes and Endocrine Centre in the period between June 2015 and May 2016. Retinal evaluation of 442 native patients was conducted using direct ophthalmological examination and digital photography. DR was graded using the Early Treatment DR Study criteria. The statistical analysis was conducted using SPSS, version 20.
RESULTS: The estimated total prevalence of DR was 31% (95% confidence interval: 26.6–35.3). Mild nonproliferative diabetic retinopathy (NPDR) constitutes 21.3%, while moderate-to-severe NPDR and proliferative diabetic retinopathy constitute 4.5% and 5.2%, respectively. The prevalence of vision-threatening diabetic retinopathy (VTDR) and diabetic maculopathy was 15.4% and 13.3%, respectively. Retinopathy was significantly associated with age, diabetes duration, Type 2 diabetes mellitus, coexisting comorbidities or complications, systolic blood pressure, glycated hemoglobin (HbA1c), fasting blood sugar, triglycerides, and albumin/creatinine ratio. In the regression analysis, age (P = 0.02), duration (P < 0.001), and HbA1c (P < 0.001) were independently associated with DR.
CONCLUSIONS: The prevalence of DR and VTDR among Omani diabetics is high. Age, duration of diabetes, and HbA1c are the risk factors for the development of DR among Omanis. This emphasizes the importance of planning resources for different modalities of treatment of DR to face the future challenge.
Keywords: Diabetic retinopathy, Oman, prevalence, risk factors, vision-threatening diabetic retinopathy
|How to cite this article:|
Agroiya P, Alrawahi AH, Pambinezhuth F, Al Busaidi NB. Diabetic retinopathy among Omanis: Prevalence and clinical profile. Oman J Ophthalmol 2020;13:76-83
|How to cite this URL:|
Agroiya P, Alrawahi AH, Pambinezhuth F, Al Busaidi NB. Diabetic retinopathy among Omanis: Prevalence and clinical profile. Oman J Ophthalmol [serial online] 2020 [cited 2020 Sep 23];13:76-83. Available from: http://www.ojoonline.org/text.asp?2020/13/2/76/285297
| Introduction|| |
Diabetic retinopathy (DR) is a serious microvascular complication of diabetes mellitus (DM)., With remarkable rise in the prevalence of DM and DR worldwide, timely screening and intervention is crucial to prevent vision-threatening complications. Almost two-thirds of all Type 2 and almost all Type 1 diabetics are expected to develop diabetic DR over a period of time.,, DR prevalence figures showed high variation worldwide, depending on many factors including screening techniques employed (direct ophthalmological examination or digital photography). In the USA, the prevalence rate using direct ophthalmological screening was 40.3% and 33.2% in two different studies,, while it was reported to be 27.9% in other developing countries. Considerable variation in the prevalence rate was also observed in studies using retinal photography in DR screening, ranging from 19% in the UK among newly diagnosed type DM patients, 29% in the USA, 34.6% in Sweden, and 10.1% in developing countries.
In Oman, there is documented rise in the prevalence of diabetes across the years.,,, In addition, previous studies from Oman have shown a considerable variation in DR prevalence among diabetics. In this regard, while it was noted to be around 14.4% in one study, it was observed to be as high as 42.4% in another study., In addition, nearly 10% of DR cases in Oman have vision-threatening diabetic retinopathy (VTDR), requiring laser and/or intravitreal injections (IVIs) of antiangiogenic factors.
However, studies addressing DR among Omanis are still limited. In addition, previous studies have used either direct ophthalmological examination or digital photography alone to diagnose DR, which may affect the true figure of prevalence.
Thus, in this study, we aim to describe the prevalence and clinical profile of DR among Omani diabetic population who attended the diabetes retina clinic of the National Diabetic and Endocrine Centre (NDEC) during 2015–2016, using both direct ophthalmological examination and digital photography. Such a study might influence the policy makers to plan the preventive and therapeutic services.
| Materials and Methods|| |
This is a cross-sectional hospital-based study conducted at NDEC, which is a tertiary care center which receives patients from all secondary care centers of Oman with mainly uncontrolled DM. Our study involved the record review related to all pediatric and adult DM cases (Type 1 and Type 2) who attended diabetes retina clinic of the NDEC during the period from June 2015 to May 2016. Only expatriates were excluded. All data were collected from the NDEC health information system.
The required sample size for this study was calculated to be 368 based on the maximum expected prevalence (from previous studies) of around 42%, confidence interval (CI) of 95% and error of 5%. All referred patients from adult and pediatric diabetes clinic of NDEC underwent thorough ocular evaluation to screen for DR at diabetes retina clinic of NDEC.
The visual acuity of each eye was recorded separately using Snellen distant vision chart at 6 m and classified according to the International Council of Ophthalmology visual standards. An ophthalmologist evaluated the anterior segment with a biomicroscope, and the intraocular pressure (IOP) was measured by either an applanation or indentation tonometer. The retinal examination with + 90 D Volk lens and panretinal indirect ophthalmoscope, fundus photography, and subsequent grading of DR category was carried out by the same ophthalmologist after pupil dilatation. We used 3D optical coherence tomography (OCT)-2000 (FA plus) OCT machine and TRC50DX Type 1A retinal camera from TOPCON to take 2 digital images per eye. Participants were seated in a dark room for the retinal imaging. One image was centered on the macula and the second on the optic nerve.
DR was defined and classified by the presence of one or more retinal microaneurysms or retinal blot hemorrhages with or without more severe lesions (hard exudates, cotton wool spots, intraretinal microvascular abnormalities, venous beading, retinal neovascularization, preretinal or vitreous hemorrhage, and fibrovascular proliferation) according to the Early Treatment Diabetic Retinopathy Study (ETDRS) grading standards. DR was further categorized as nonproliferative diabetic retinopathy and proliferative diabetic retinopathy (NPDR and PDR), depending on the presence or absence of retinal neovascularization or abnormal growth of new retinal blood vessels into the vitreous. All patients with photocoagulation scars and post-IVI antivascular endothelial growth factors (VEGFs) therapy were categorized according to their pretreatment status, such as PDR and diabetic maculopathy, respectively. Diabetic macular edema (DME), which is the main feature of diabetic maculopathy, was defined according to the ETDRS criteria as any detectable retinal thickening due to fluid accumulation. The presence or absence of diabetic maculopathy was detected by the use of OCT; however, no further grading was done for such patients in the current study. VTDR was defined as the presence of severe NPDR, PDR, or DME. The DR status was labeled according to the worse eye.
Other details including age, gender, body mass index (BMI), systolic blood pressure and diastolic blood pressure (SBP and DBP), duration of diabetes, and type of diabetes (which included either insulin-dependent diabetes mellitus or noninsulin-dependent diabetes mellitus [NIDDM] according to the classification laid down by the WHO) were collected from the data system. Associated systemic comorbidities (hypertension and dyslipidemia), macrovascular complications in the form of cardiovascular accident, ischemic heart disease, coronary artery disease and peripheral vascular disease, microvascular complications including peripheral neuropathy, diabetic foot, and nephropathy were recorded by referring physician. Several laboratory parameters such as fasting blood sugar (FBS) and random blood sugar, lipid profile (total cholesterol levels, high-density lipoproteins [HDLs], low-density lipoproteins [LDL], and triglycerides [TGs]), glycated hemoglobin (HbA1c), and albumin/creatinine ratio (ACR) were also considered in the study.
The data were analyzed using IBM SPSS Statistics for Windows, Version 20.0. (Armonk, NY: IBM Corp). Descriptive measures were expressed as percentages and/or means with standard deviations. Associations were tested using univariate and multivariate tests. For univariate analysis, Chi-square, independent t-test, and ANOVA were used according to the nature of variables. For multivariate analysis, binary logistic regression was used to adjust for confounders. The level of statistical significance was set at P < 0.05. All variables with P ≤ 0.25 in the univariate logistic regression were considered candidate variables for binary logistic regression models.
This study was approved by the Research Ethics Committee of the Center of Studies and Research of the Ministry of Health, Oman.
| Results|| |
After excluding all expatriates, the final sample size included in this study was 442 subjects with 882 eyes which comprised 61.5% of females. Age of the patient cohort ranged from 8 to 76 years with a mean of 39.3 ± 16.5 years. Type 2 DM patients accounted for 62.2%, while 31.4% and 0.9% accounted for type 1 and gestational DM, respectively. The duration of diabetes ranged from 0 to 32 years with a mean duration of 8.46 ± 6.2 years. The mean BMI of study sample was 30.6 ± 8.2 ranging from 14 to 69. Detailed descriptives are shown in [Table 1].
Hypertension and dyslipidemia were seen in 7% and 21.3% of cases, respectively. Microvascular complications were seen in 21% of patients. The mean SBP and DBP of study population was 130.4 ± 19.9 and 78.1 ± 12.2 mm of Hg, respectively. The HbA1c ranged between 4% and 17% with a mean HbA1c of 8.4 ± 2.4.
The prevalence of DR among the study sample was 31% (95% CI: 26.6–35.3). VTDR was seen in 15.4% of cases. Of the 137 cases of DR, 94 (21.3%) had mild NPDR, 20 (4.5%) had moderate-to-severe nonproliferative DR, and 23 (5.2%) had PDR. Diabetic maculopathy was noted in 59 (13.3%) in addition to the retinopathy changes.
A vision of 6/18 or better in the eye with worse vision was recorded in 85.1% of patients. High IOP (>21 mm of hg) was recorded in 14.1% of subjects either in one eye (6.6%) or both eyes (7.5%). Of the 137 retinopathy cases, 23 subjects (5.2%) received laser therapy and 0.7% received IVI anti VEGFs.
As illustrated in [Table 2], though women had higher rates of DR (32.7%) than men (28.3%), the difference was not statistically significant (P = 0.40). The prevalence of DR was significantly higher among patients with a longer duration of diabetes than with the shorter duration (P < 0.001). The mean age among DR group (including proliferative and nonproliferative) was significantly higher compared to the DR-free group (P ≤ 0.001).
|Table 2: Associations between clinical and laboratory characteristics and diabetic retinopathy|
Click here to view
According to the univariate analysis, retinopathy in general was significantly higher among Type 2 diabetics (37.8%) compared to Type 1 diabetics (20.2%) (P = 0.001). In addition, the prevalence of DR was generally higher in those with single or multiple comorbidities/complications (P < 0.001). The mean SBP among DR group (including proliferative and nonproliferative) was significantly higher compared to the DR-free group (P ≤ 0.001). With respect to this, both NPDR and PDR were more prevalent among patients with higher SBP (>140 mmHg; P < 0.001). There was a significant difference in the mean HbA1c between the DR free and DR-groups (P = 0.02). In this regard, the difference in the mean HbA1c level between DR-free and NPDR groups was significant (P = 0.02), whereas this difference was not significant between DR-free and PDR group (P = 0.96). The mean FBS among DR group was significantly higher compared to the DR-free group (P = 0.03). The difference in the mean TGs level between DR-free and NPDR groups was significant (P = 0.02); however, this difference was not significant between DR-free and PDR groups (P = 0.30). In general, ACR was found to be associated with DR (P < 0.001). However, this association was observed for PDR (P < 0.001) as the mean ACR among patients with NPDR was not different compared to DR-free patients (P = 0.09).
In multivariate logistic regression analysis, we found age (P = 0.02), duration (P < 0.001), and HbA1c (P < 0.001) to be independently associated with DR.
On the other hand, there was no significant association of DR with gender, obesity level, DBP, total cholesterol levels, HDL, LDL, best-corrected visual acuity (BCVA), and IOP.
| Discussion|| |
This study was conducted to assess the prevalence and clinical profile of DR in a sample of diabetic population of Oman. As the magnitude of DM and DR on rise in Oman and worldwide, information about the current status of this vision-threatening complication is very crucial in order to reduce visual disabilities and improve the quality of life of people with diabetes.
The prevalence of DR in our study was 31% which approximates the overall global prevalence (35.4%)., However, a wide variation in DR prevalence is noted among Omani diabetic population in different studies (14.4% and 42.4%)., This difference in prevalence could be attributed to different sample size and setting, sample characteristics, and age cutoff involved in different studies. In addition, different methods of screening employed may be another factor.
In Middle East, the DR prevalence has been reported to be between 12.1% and 36.8% in three different studies conducted in Saudi Arabia and Iran,,, whereas a higher DR prevalence was observed in western countries in Europe and US (7.6%–93.6%). This disparity can be attributed to a longer life expectancy in the developed world. At this point, it is noteworthy that a higher DR prevalence in developed economies reflects better health coverage, making it a debatable issue whether low prevalence is better than higher prevalence.
In the present study, mild NPDR was noted in 21.3% of the total sample, moderate–severe NPDR in 4.5% of patients, which is similar to earlier figures observed in a study conducted locally. However, the prevalence of PDR was noted to be lower than previous figures. This drop in PDR frequency can be attributed to multidisciplinary timely interventions to reverse or delay long-term poor visual outcomes from DM.
In this study, the prevalence of VTDR was 15.4% which is higher than global prevalence of 11.72%. However, a similar trend was noted in Saudi Arabia and Iran,,, ranging between 11.1%–17.5%.,, In Nepal, a recent work shows VTDR prevalence of 14.4%. This is in contrast to low prevalence observed in Western world (0.59%–5.1%). The high rate of VTDR is of great concern as it may indicate late detection, when it has already progressed to a vision-threatening stage due to poor glycemic control, or that these populations are particularly susceptible to severe DR due to ethnic predisposition.
The diabetic maculopathy rate was 13.3% in our study, which is higher than the global prevalence of 7.48%. In comparison to another local study, the rate of maculopathy was observed to be around half of our observed figure. However, in the Middle East, the diabetic maculopathy rate is documented as high as 20.3% in Saudi Arabia and as low as 4.7% in Iran., A higher prevalence of 15.7% has also been observed in Canada. However, low prevalence rates were noted in India, China, and USA (1.4%, 4%, and 3.8%, respectively).,, This variation may be real due to differences in the distribution of various risk factors in different populations. However, it can also be attributed to differences in the definition of diabetic maculopathy and differences in methodologies applied in different studies. In this regard, the use of OCT for diagnosing DME in the present study might have led to this high prevalence as there is difference in clinical definition of clinically significant macular edema and OCT-detected DME. In addition, diagnosis of DME itself is challenging as there is no consensus on OCT-based severity classification for DME.
One of the important observations in the present study was that 28.7% of patients with DR had a visual acuity of 6/18 or better, which supports the well documented fact that clinically detectable DR does not always impair vision and reinforces the importance of annual retinal screening in all diabetic patients irrespective of their visual status.
In this study, age, duration of diabetes, and HbA1c were independently associated with DR. These findings were similar to various hospital-based and population-based studies in Oman and other countries.,, In this study, there was 2.3- and 4.1-fold increase in the prevalence of any type of DR in middle and older age groups, respectively, when compared to youngest age group. Similar observations were reported in the literature from Saudi Arabia. In Nepal and southern India, the prevalence of DR among the same age group was observed around 49.2% and 25%, respectively. However, the overall prevalence of DR in these two studies was also low compared to the present study, which may explain the lower prevalence in this age group., In contrast, another local study has not picked the association of DR with age, as it was confounded by diabetes duration and could not be regarded as an independent risk factor. As for diabetes duration, many studies have established a positive association between DR and this risk factor, which was independent of adequacy of glycemic control., Similar observation in our study emphasizing this association.
Hyperglycemia is one of the well-known risk factors for DR. In the current study, HbA1c was also found to be independently associated with DR. A graded relationship between the level of glycemia and frequency of retinopathy has been documented in a meta-analysis of three large population-based studies. In addition, tight control of glycemia (HbA1c <7%) was found to reduce the risk of development and progression of DR in both Type 1 and Type 2 diabetes. This highlights the importance of strict glycemic control and routine HbA1c investigations. In this regard, current professional guidelines state that treatment goals of hyperglycemia are to be anywhere between <6.5 and <7.5% of HbA1c. However, the authors from a recently published Cochrane review do not recommend any specific treatment target, instead emphasize on individualized treatment goals based on age, disease progression, risk of hypoglycemic episodes, and psychological factors of the patient.
While most of literature worldwide including one study from Oman suggests a higher prevalence of DR among type 1 diabetic patients compared to type 2 diabetics,,,,,, to our surprise, the present study depicts significantly higher rates of retinopathy among Type 2 diabetics compared to Type 1 diabetics. However, this association was excluded by the multivariate analysis. Higher rates of DR among Type 2 diabetics were also noted in another study conducted in Oman. One of the key reasons for this finding might be the fact that large proportions of patients with Type 1 diabetes were screened early during the course of disease.
A number of clinical and laboratory risk factors such as hypertension and dyslipidemia, macrovascular and microvascular complications of DM, SBP, FBS, TGs, and ACR were also associated with an increased risk for any grade of DR, as demonstrated in various literature, but in the current study, they lost their significance in multivariate analysis.,,, On the other hand, similar to some studies,,, or in contrast with others,,,,, gender, BMI, DBP, total cholesterol levels, HDL, and LDL did not show significant association with the occurrence of DR in this study. Differences in such association results across different studies may be due to differences in the nature of the study designs, which was a cross-sectional and retrospective in nature in our situation. In addition, the differences in inclusion and exclusion criteria across different studies such as including or excluding Type 1 diabetic patients in various studies may be another explanation. In addition, differences in ethnic and genetic susceptibility to conventional risk factors in different populations is a third explanation. Furthermore, no significant association of BCVA and IOP with occurrence of DR was observed in this study, which is consistent with results described in literature from different parts of world.
The well-documented details about DR category in the patients' clinical records, and the large sample size included, have made this work more valid and reliable. However, the stereoscopic color fundus photography in 7 standard fields (30°) is the gold standard photography method for the detection of DR; it is time-consuming and less practical. Instead, the two-field fundus photography (with sensitivity and specificity of 96% and 89%, respectively) along with clinical ophthalmoscopy was used to provide valid indications of retinopathy. The use of OCT in the current study for the detection of DME in subclinical stage was also an advantage to identify those patients with risk of VTDR. However, diabetic macular ischemia, which is comparatively less common category of diabetic maculopathy, was not screened by gold standard imaging modality of fundus fluorescein angiography or optical coherence tomography angiography in the present study. This study was conducted in a tertiary care center and hence may not represent the primary care setting and the general population. However, the studied sample involved patients from across the country regions and included new and old patients with primarily uncontrolled DM, and therefore, the results may be generalized at least to all patients referred to tertiary care institutions. Because this study included only patients who were referred to diabetes retina clinic during the specified period, the true DR prevalence might be overestimated due to referral bias.
| Conclusions|| |
In summary, our study provides current data on the prevalence of DR and VTDR in a sample of 442 diabetic subjects who were screened with clinical ophthalmoscopy and retinal photography and had their DR category registered in their medical records of a tertiary care center. Our findings indicate a high prevalence of DR which is comparable to global figures. This study also highlights the importance of age, duration of diabetes, and HBA1c as independent risk factors among Omanis. It is necessary to continue with cribbage and strict glycemic control in order to decrease the prevalence of DR. In addition, effective DR screening tools that include digital fundus photographs could be a solution to enhance early detection of vision-threatening retinopathy in future. However, in view of higher rates of VTDR and macular involvement, resources for laser therapy and antiangiogenic treatment should be planned with special focus on care for diabetic maculopathy.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Cheung N, Wong TY. Diabetic retinopathy and systemic vascular complications. Prog Retin Eye Res 2008;27:161-76.
Liew G, Wong TY, Mitchell P, Cheung N, Wang JJ. Retinopathy predicts coronary heart disease mortality. Heart 2009;95:391-4.
Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: Estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047-53.
Prevention of Blindness from Diabetic Retinopathy. Report of a WHO Consultation. Geneva: Prevention of Blindness from Diabetic Retinopathy; 2005.
Guidelines for the Comprehensive Management of Diabetic Retinopathy in India. A VISION 2020 the Right to Sight India Publication; 2008.
Kempen JH, O'Colmain BJ, Leske MC, Haffner SM, Klein R, Moss SE, et al
.; Eye Diseases Prevalence Research Group. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol 2004;122:552-63.
Wong TY, Klein R, Islam FM, Cotch MF, Folsom AR, Klein BE, et al
. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol 2006;141:446-55.
Ruta LM, Magliano DJ, Lemesurier R, Taylor HR, Zimmet PZ, Shaw JE. Prevalence of diabetic retinopathy in Type 2 diabetes in developing and developed countries. Diabet Med 2013;30:387-98.
Kostev K, Rathmann W. Diabetic retinopathy at diagnosis of type 2 diabetes in the UK: A database analysis. Diabetologia 2013;56:109-11.
Zhang X, Saaddine JB, Chou CF, Cotch MF, Cheng YJ, Geiss LS, et al
. Prevalence of diabetic retinopathy in the United States, 2005-2008. JAMA 2010;304:649-56.
Olafsdottir E, Andersson DK, Dedorsson I, Stefánsson E. The prevalence of retinopathy in subjects with and without type 2 diabetes mellitus. Acta Ophthalmol 2014;92:133-7.
Asfour MG, Lambourne A, Soliman A, Al-Behlani S, Al-Asfoor D, Bold A, et al
. High prevalence of diabetes mellitus and impaired glucose tolerance in the Sultanate of Oman: Results of the 1991 national survey. Diabet Med 1995;12:1122-5.
Asfour MG, Samantray SK, Dua A, King H. Diabetes mellitus in the sultanate of Oman. Diabet Med 1991;8:76-80.
Al-Lawati JA, Al Riyami AM, Mohammed AJ, Jousilahti P. Increasing prevalence of diabetes mellitus in Oman. Diabet Med 2002;19:954-7.
Al Riyami A, Elaty MA, Morsi M, Al Kharusi H, Al Shukaily W, Jaju S. Oman world health survey: Part 1 – Methodology, sociodemographic profile and epidemiology of non-communicable diseases in Oman. Oman Med J 2012;27:425-43.
Khandekar R, Al Lawatii J, Mohammed AJ, Al Raisi A. Diabetic retinopathy in Oman: A hospital based study. Br J Ophthalmol 2003;87:1061-4.
El Haddad OA, Saad MK. Prevalence and risk factors for diabetic retinopathy among Omani diabetics. Br J Ophthalmol 1998;82:901-6.
Sivaprasad S, Gupta B, Gulliford MC, Dodhia H, Mohamed M, Nagi D, 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:e32182.
Visual Standards, Aspects and Ranges of Vision Loss, with Emphasis on Population Surveys. Report Prepared for the International Council of Ophthalmology, at the 29th
International Congress of Ophthalmology, Sydney, Australia; April, 2002.
Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs – An extension of the modified Airlie House classification: ETDRS report number 10. Ophthalmology 1991;98 Suppl 5:786-806.
Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al
. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012;35:556-64.
World Health Organisation Study Group on Diabetes Mellitus. Technical Report Series Number 727. Geneva: WHO; 1985.
Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond) 2015;2:17.
Al Ghamdi AH, Rabiu M, Hajar S, Yorston D, Kuper H, Polack S. Rapid assessment of avoidable blindness and diabetic retinopathy in Taif, Saudi Arabia. Br J Ophthalmol 2012;96:1168-72.
Al-Rubeaan K, Abu El-Asrar AM, Youssef AM, Subhani SN, Ahmad NA, Al-Sharqawi AH, et al
. Diabetic retinopathy and its risk factors in a society with a type 2 diabetes epidemic: A Saudi National Diabetes Registry-based study. Acta Ophthalmol 2015;93:e140-7.
Papakonstantinou E, Tsinopoulos I, Dimitrakos S, Dehghan MH, Katibeh M, Ahmadieh H, et al
. Prevalence and risk factors for diabetic retinopathy in the 40 to 80 years old population in Yazd, Iran: The Yazd Eye Study. J Diabetes 2015;7:139-41.
Thapa R, Joshi DM, Rizyal A, Maharjan N, Joshi RD. Prevalence, risk factors and awareness of diabetic retinopathy among admitted diabetic patients at a tertiary level hospital in Kathmandu. Nepal J Ophthalmol 2014;6(11). doi:10.3126/nepjoph.v6i1.10760.
Nathoo N, Ng M, Rudnisky CJ, Tennant MT. The prevalence of diabetic retinopathy as identified by teleophthalmology in rural Alberta. Can J Ophthalmol 2010;45:28-32.
Raman R, Rani PK, Reddi Rachepalle S, Gnanamoorthy P, Uthra S, Kumaramanickavel G, et al
. Prevalence of diabetic retinopathy in India: Sankara Nethralaya diabetic retinopathy epidemiology and molecular genetics study report 2. Ophthalmology 2009;116:311-8.
Xie XW, Xu L, Wang YX, Jonas JB. Prevalence and associated factors of diabetic retinopathy. The Beijing Eye Study 2006. Graefes Arch Clin Exp Ophthalmol 2008;246:1519-26.
Varma R, Bressler NM, Doan QV, Gleeson M, Danese M, Bower JK, et al
. Prevalence of and risk factors for diabetic macular edema in the United States. JAMA Ophthalmol 2014;132:1334-40.
Thapa R, Twyana SN, Paudyal G, Khanal S, van Nispen R, Tan S, et al
. Prevalence and risk factors of diabetic retinopathy among an elderly population with diabetes in Nepal: The Bhaktapur Retina Study. Clin Ophthalmol 2018;12:561-8.
Nirmalan PK, Katz J, Robin Al, Tielsch JM, Namperumalsamy P, Kim R, et al
. Prevalence of vitreo-retinal disorders in a rural population of southern India: The Aravind Comprehensive eye Study. Arch Ophthalmol 2004;122:581-6.
Narendran V, John RK, Raghuram A, Ravindran RD, Nirmalan PK, Thulasiraj RD. Diabetic retinopathy among self-reported diabetics in southern India: A population based assessment. Br J Ophthalmol 2002;86:1014-8.
Wong TY, Liew G, Tapp RJ, Schmidt MI, Wang JJ, Mitchell P, et al
. Relation between fasting glucose and retinopathy for diagnosis of diabetes: Three population-based cross-sectional studies. Lancet 2008;371:736-43.
Mohamed Q, Gillies MC, Wong TY. Management of diabetic retinopathy: A systematic review. JAMA 2007;298:902-16.
Fullerton B, Jeitler K, Seitz M, Horvath K, Berghold A, Siebenhofer A. Intensive glucose control versus conventional glucose control for type 1 diabetes mellitus. Cochrane Database Syst Rev 2014;2014:CD009122.
Pedro RA, Ramon SA, Marc BB, Juan FB, Isabel MM. Prevalence and relationship between diabetic retinopathy and nephropathy, and its risk factors in the North-East of Spain, a population-based study. Ophthalmic Epidemiol 2010;17:251-65.
Bertelsen G, Peto T, Lindekleiv H, Schirmer H, Solbu MD, Toft I, et al
. Tromsø eye study: Prevalence and risk factors of diabetic retinopathy. Acta Ophthalmol 2013;91:716-21.
Knudsen LL, Lervang HH, Lundbye-Christensen S, Gorst-Rasmussen A. The North Jutland County Diabetic Retinopathy Study: Population characteristics. Br J Ophthalmol 2006;90:1404-9.
Dedov I, Maslova O, Suntsov Y, Bolotskaia L, Milenkaia T, Besmertnaia L. Prevalence of diabetic retinopathy and cataract in adult patients with type 1 and type 2 diabetes in Russia. Rev Diabet Stud 2009;6:124-9.
Thomas RL, Distiller L, Luzio SD, Chowdhury SR, Melville VJ, Kramer B, et al
. Ethnic differences in the prevalence of diabetic retinopathy in persons with diabetes when first presenting at a diabetes clinic in South Africa. Diabetes Care 2013;36:336-41.
Segal P, Treister G, Yalon M, Sandak R, Berezin M, Modan M. The prevalence of diabetic retinopathy: Effect of sex, age, duration of disease and mode of therapy. Diabetes Care 1983;6:149-51.
Araki A, Ito H, Hattori A, Inoue J, Sato T, Shiraki M, et al
. Risk factors for development of retinopathy in elderly Japanese patients with diabetes mellitus. Diabetes Care 1993;16:1184-6.
Zhou Y, Zhang Y, Shi K, Wang C. Body mass index and risk of diabetic retinopathy: A meta-analysis and systematic review. Medicine (Baltimore) 2017;96:e6754.
Cetin EN, Bulgu Y, Ozdemir S, Topsakal S, Akın F, Aybek H, et al
. Association of serum lipid levels with diabetic retinopathy. Int J Ophthalmol 2013;6:346-9.
Jerneld B, Algvere P. Relationship of duration and onset of diabetes to prevalence of diabetic retinopathy. Am J Ophthalmol 1986;102:431-7.
Kaštelan S, Tomić M, Antunica AG, Ljubić S, Rabatić JS, Karabatić M. Body mass index: A risk factor for retinopathy in type 2 diabetic patients. Mediators Inflamm 2013;2013:436329.
Idiculla J, Nithyanandam S, Joseph M, Mohan VA, Vasu U, Sadiq M. Serum lipids and diabetic retinopathy: A cross-sectional study. Indian J Endocrinol Metab 2012;16:S492-4.
Scanlon PH, Foy C, Chen FK. Visual acuity measurement and ocular co-morbidity in diabetic retinopathy screening Article. Br J Ophthalmol 2008;92:775-8.
[Table 1], [Table 2]