JOURNAL
Current Issue
Journal Archive
.............................................................
July/August 2016 -
Volume 14, Issue 6
Download print-friendly version
........................................................
From the Editor

Editorial
A. Abyad (Chief Editor)
   
........................................................
Original Contribution / Clinical Investigation

<-- Middle East Primary Care Research Network-->
Frequency of Job-Related Burn-out in Family Physicians working in General / Family Practice in the Middle East
[pdf version]
Abdulrazak Abyad, Bader Almustafa, Abbas Ali Mansour, Manal S Al-Mutar, Thamer Al Hilfi, Seyed Habib Olla Kavari

<-- Saudi Arabia -->
Effect of Ginger and its Extract on Blood Sugar and on Kidney Function of Type I Diabetic Rats
[pdf version]
Abdulsalam, K.A., El gabry, E.K., Alkalifa, A.S

<-- Saudi Arabia-->
Prevalence of Diabetic Retinopathy among Newly Diagnosed Type 2 Diabetes Mellitus Patients in Abha City, Saudi Arabia
[pdf version]
Awad S. Alsamghan, Safar Abadi Al-Saleem, Mohammad A. Alshibli, Hassan M. Al-Musa

........................................................
Medicine and Society

<-- Yemen -->
The prevalence of metabolic syndrome in Yemeni patients with hypothyroidism
[pdf version]
Bamashmos M.A. Atef, Z.A.

<-- Pakistan -->
Prevalence and determinants of Unintended Pregnancy: Systematic Review
[pdf version]
Sumera Aziz Ali, Shiyam Sunder Tikmani, Waris Qidwai

........................................................
Education and Training




<-- Australia -->
Principles of Surgery - Ano rectal region: Anal abscess and fistula
[pdf version]
Maurice Brygel

Chief Editor -
Abdulrazak Abyad MD, MPH, MBA, AGSF, AFCHSE
.........................................................

Editorial Office -
Abyad Medical Center & Middle East Longevity Institute
Azmi Street, Abdo Center,
PO BOX 618
Tripoli, Lebanon
Phone: (961) 6-443684
Fax:     (961) 6-443685
Email: aabyad@cyberia.net.lb
.........................................................

Publisher -
Lesley Pocock
medi+WORLD International
11 Colston Avenue,
Sherbrooke 3789
AUSTRALIA
Phone: +61 (3) 9005 9847
Fax: +61 (3) 9012 5857
Email: lesleypocock@mediworld.com.au
.........................................................

Editorial Enquiries -
abyad@cyberia.net.lb
.........................................................

Advertising Enquiries -
lesleypocock@mediworld.com.au
.........................................................

While all efforts have been made to ensure the accuracy of the information in this journal, opinions expressed are those of the authors and do not necessarily reflect the views of The Publishers, Editor or the Editorial Board. The publishers, Editor and Editorial Board cannot be held responsible for errors or any consequences arising from the use of information contained in this journal; or the views and opinions expressed. Publication of any advertisements does not constitute any endorsement by the Publishers and Editors of the product advertised.

The contents of this journal are copyright. Apart from any fair dealing for purposes of private study, research, criticism or review, as permitted under the Australian Copyright Act, no part of this program may be reproduced without the permission of the publisher.
July / August 2016 - Volume 14, Issue 6

Prevalence of Diabetic Retinopathy among Newly Diagnosed Type 2 Diabetes Mellitus Patients in Abha City, Saudi Arabia



 Awad S. Alsamghan,
Safar Abadi Al-Saleem,
Mohammad A. Alshibli,
Hassan M. Al-Musa

Correspondence:
Dr. Awad S. Alsamghan
Family & Community Medicine
College of Medicine
King Khalid University,
Abha, Kingdom of Saudi Arabia
Contact #: 0503750084
Email: awadalsamghan@gmail.com

Abstract


Objectives: To estimate the prevalence of DR and to compare the difference in the prevalence rate according to different patient's characteristics among newly diagnosed type 2 diabetic patients in Abha, Kingdom of Saudi Arabia.

Study design: A cross sectional study

Methods: This study was conducted at the ophthalmology clinic in Abha General Hospital, Saudi Arabia. All newly diagnosed diabetic type 2 patients attending primary health care centers in Abha during the period of study (39 PHCCs) were referred to the ophthalmology department in Abha General Hospital for diabetic retinopathy screening until the required sample size was reached. After adequate mydriasis, the examination of the posterior segment was carried out using slit-lamp biomicroscope with 90-dioptor lens. The intraocular pressure was measured using applanation tonometry. Diabetic retinopathy was classified using Friedman's standards.

Results: The study included 393 newly diagnosed type 2 diabetic patients. Their age ranged between 21 and 96 years with a mean of 52.9 years and standard deviation of 11.8 years. Female patients represented (242) 61.6% of them. The prevalence of diabetic retinopathy among newly diagnosed type 2 diabetic patients was (13) 3.3%. All DR cases were classified using Friedman's standards as background or non-proliferative diabetic retinopathy. The prevalence of DR among female newly diagnosed type 2 diabetic patients was (13) 5.4% compared to none among males. This difference was statistically significant, p=0.002. The prevalence of DR was (13) 4.3% among not working type 2 diabetic patients compared to none among working patients. This difference was statistically significant, p=0.027. Intra-ocular pressure was within normal values for all patients in both eyes.

Conclusion: The prevalence of retinopathy in newly diagnosed type 2 diabetes mellitus patients was found to be relatively low in this study compared to international studies.

Key words: Diabetic retinopathy; Diabetes mellitus; Prevalence; Diagnosis; Ophthalmology

INTRODUCTION

Diabetic retinopathy (DR) is a complication of diabetes mellitus (DM) that affects the blood vessels of the retina and leads to blindness. The progression of retinopathy is gradual, advancing from mild abnormalities, characterized by increased vascular permeability, to moderate and severe non-proliferative diabetic retinopathy, characterized by the growth of new blood vessels on the retina and posterior surface of the vitreous.(1)

Individuals with diabetes are 25 times more likely to become blind than individuals without this disease.(2) In many developed countries, diabetic retinopathy is the leading cause of new cases of visual impairment and blindness among adults aged 20-74 years.(3) Among people who have type 2 diabetes, around 21% have retinopathy at diagnosis,3 and more than 60% have diabetic retinopathy during the first two decades of the disease.(4)

The Wisconsin epidemiological study of diabetic retinopathy (WESDR) concluded that 1.6% of those diagnosed with type 2 DM were legally considered blind. For type 2 DM, blindness was related to retinopathy in 33% of the cases.(5) The prevalence of DR is probably around 30% in type 2 DM, but notably was above this level in five out of six studies reported from the Asian and pacific island nations of the Western Pacific Region.(6) The annual incidence of retinopathy requiring ophthalmological follow up or treatment has been reported to average 1.5% after one year.(7) The same source estimates that 6-9% of patients with proliferative retinopathy or severe non-proliferative disease would become blind each year.(7) Moreover, growing evidence also suggests that after 15 years of diabetes, approximately 2% of patients develop blindness, while about 10% develop severe visual handicap.(7) Thus, the early detection of sight-threatening retinopathy and the timely intervention with laser photocoagulation has been shown to be effective in preventing severe visual loss.

Diabetes-related blindness is a personal catastrophe to the individual and costs the United States approximately $500 million annually.(8) However, risk of vision loss due to diabetic retinopathy can be reduced by effective control of serum glucose and blood pressure and by its early detection and timely treatment.(9-11) The efficacy and cost-effectiveness of early detection and treatment of diabetic retinopathy is well established.(12, 13)

Several factors have been identified as determinants for the development of DR and its progression; including, type and duration of DM, age, gender, glycemic control, hypertension, body mass index (BMI), smoking, serum lipids and presence of microalbuminuria (MA)(14-18).

METHODOLOGY

Study design: A cross-sectional method.

Study setting: This study was conducted at the ophthalmology clinic in Abha General Hospital, Aseer region, Saudi Arabia.

Study population: Newly diagnosed diabetic type 2 patients attending primary health care centers (39 PHCCs) in Abha during the period of study from September 2013 until April 2014. They were requested to participate in the study. They were referred to the ophthalmology department in Abha General Hospital for diabetic retinopathy screening.

Sample size and sampling technique: The sample size was estimated to determine the prevalence of diabetic retinopathy among newly diagnosed diabetic patients type 2 of 12% (according to average of previous regional studies in the literature), with a 3% absolute error (25% of prevalence) and finite population correction, at 95% level of confidence. The newly diagnosed type 2 diabetic patients in Abha in 2012 was 3059 patients.

Using the single proportion equation for dichotomous variables in Raosoft software package, and the previous information to answer the following questions: What margin of error can you accept? (3%); What confidence level do you need? (95%); What is the population size? (3059) and What is the response distribution? (12%). Accordingly, the required sample size is 393 patients.(19)

All newly diagnosed type 2 diabetic patients referred to the ophthalmology department in Abha General Hospital were invited to be included in the study until the required sample size was reached.

Inclusion criteria: Diabetic type 2 patients who were diagnosed within two years, All ages (more than 20 years old), Both genders.

Exclusion criteria: Those who refused to participate in the study, With chronic debilitating diseases (hypertension, asthma …) and With serious eye problems (cataract, glaucoma…)

Study tool and procedure:
All patients referred to ophthalmologists at the Abha General Hospital underwent detailed eye examination. After adequate mydriasis, the examination of the posterior segment was carried out using slit-lamp biomicroscope with 90-dioptor lens. The intraocular pressure was measured using applanation tonometry.

Diabetic retinopathy was classified using Friedman's (2005) standards, and was as follows:

i) Background or non-proliferative diabetic retinopathy: haemorrhages, exudates, cotton wool spots, microaneurysms, intraretinal microvascular abnormalities, venous beading;
ii) Severe NPDR ("4-2-1 rule"): defined as any one of the following: 4 quadrants of hemorrhages/MAs, 2 quadrants of venous beading, 1 quadrant of IRMA;
iii) Very Severe NPDR: defined as 2 or more of the above;
iv) Proliferative (PDR): neovascularization (NV) of disc or elsewhere;
v) High-risk proliferative (HR-PDR): defined as any one of the following:
1. NVD > 1/4 to 1/3 disc area,
2. Any NVD with vitreous haemorrhage,
3. NVE > 1/2 disc area with vitreous haemorrhage.(20)

Then, a data collection sheet was filled in by the researcher including the following:
- Demographic variables including: age, gender, marital status, job and educational level;
- Medical history including diabetic complications other than DR, diabetic coma, treatment and treatment satisfaction;
- Ophthalmological examination regarding DR and its grade was done by the ophthalmologist.

Data management and statistical analysis:
SPSS package, version 20 was used for data entry and analysis. Descriptive statistics were applied as follows: Frequency and percentage were used to describe categorical variables while mean and standard deviation were used to describe continuous variables. Chi-square test was applied to test for the association and/or difference between categorical variables. Fisher exact test was applied instead of chi-square test in case of small frequencies. Differences were considered statistically significant when the p-value was less than 0.05.

RESULTS

The study included 393 newly diagnosed type 2 diabetic patients. Their age ranged between 21 and 96 years with a mean of 52.9 and standard deviation of 11.8 years. More than half of them 213 (56%) were over 50 years. Female patients represented 242 (61.6%) of them. The majority of them 256 (90.6%) were married. Most of them 299 (76.1%) were not working. Among working patients 94 (23.9%), governmental employees 28 (29.8%) and teachers 27 (28.7%) were the most common reported jobs. Slightly less than half of them 186 (47.3%) were illiterate and 49 (12%) finished university and postgraduate studies (Table 1).

Table 1: Personal characteristics of newly diagnosed type 2 diabetic patients who participated in the study (n=393)


The prevalence of diabetic complications (other than diabetic retinopathy) among newly diagnosed type 2 diabetic patients was 7(1.8%). This complication was diabetic neuropathy.

Newly diagnosed type 2 diabetic patients had history of diabetic coma which accounted for 12 (3.1%). Regarding treatment among newly diagnosed type 2 diabetic patients, oral hypoglycemic drugs were the most commonly reported 270 (76.6%), followed by diet regimen 76 (27.2%). Insulin was the line of treatment among 12 (3.1%) of them while a combination of oral hypoglycemic drugs and insulin was the type of treatment for 4 (1%) of them.

Almost two-thirds 272 (69.2%) of type 2 diabetic patients were very satisfied with their disease therapy while 97 (24.7%) were somewhat satisfied with it.

Diabetic Retinopathy
The prevalence of diabetic retinopathy among newly diagnosed type 2 diabetic patients was 13 (3.3%). All DR cases were classified using Friedman's standards as background or non-proliferative diabetic retinopathy.

The prevalence of DR was 4 (6.5%) among newly diagnosed type 2 diabetic patients over 60 years compared to none among those aged between 20 and 40 years. However, the difference was not statistically significant, p=0.210 (Table 2).

Table 2: Prevalence of diabetic retinopathy according to personal characteristics, diabetes therapy and satisfaction therapy


The prevalence of DR was 13 (3.7%) among married newly type 2 diabetic patients compared to none among singles, divorced and widowed patients. However, the difference was not statistically significant, p=0.706 (Table 2).

DR was more reported among lower educated diabetic type 2 patients 9 (4.8%) and 4 (4.5%) among illiterate and primary educated patients compared to none of higher educated patients. However, this difference was not statistically significant, p=0.215 (Table 2).

The prevalence of DR among female newly diagnosed type 2 diabetic patients was 13 (5.4%) compared to none among males. This difference was statistically significant, p=0.002 (Table 3).

Table 3: Prevalence of diabetic retinopathy according to patient`s gender, job status, diabetic complications


The prevalence of DR was 13 (4.3%) among not working type 2 diabetic patients compared to none among working patients. This difference was statistically significant, p=0.027 (Table 3).

There was no statistically significant association between DR and other diabetic complications among newly diagnosed type 2 diabetic patients, p=0.789. Also, there was no statistically significant association between DR and history of diabetic coma among newly diagnosed type 2 diabetic patients, p=0.664. DR was more reported among diabetic type 2 patients treated by oral hypoglycemic drugs (4.8%) compared to none among patients treated by diet regimen, insulin and a combination of insulin and oral hypoglycaemic drugs. However, this difference was not statistically significant, p=0.190. There was no statistically significant association between DR and satisfaction of diabetic patients with their therapy, p=0.113 (Table 3).

Intra-ocular Pressure
Intra-ocular pressure was within normal values for all patients in both eyes (10 mmHg and 21 mmHg).

DISCUSSION

The prevalence of retinopathy in patients with newly diagnosed Type 2 diabetes mellitus was found to be relatively lower in this study (3.3%) compared to international data.

Diabetes Prevention Program Research Group(21) reported 12.6% prevalence of retinopathy in recent onset diabetes in the diabetes prevention programme. Wahab et al in Pakistan reported that 15% (95% CI 14.7, 15.3) of patients were found to have diabetic retinopathy within two months of diagnosis of type 2 diabetes mellitus.(22)

Multiple clinic-based studies conducted on newly diagnosed diabetes patients have shown varied prevalence; Abdollahi et al.(23) from Iran reported 13.8%, Agarwal et al.(24) reported 11.7%, while Rema and associates reported 5.1% and 7.3% respectively.(25,26) Klein et al.(27) reported the prevalence of 10.2% in newly discovered type 2 diabetic patients in Beaver Dam Eye Study. Kohar and associates(28) have reported 39% and 35% prevalence of retinopathy in men and women respectively in the United Kingdom Prospective Diabetes Study.

In a study on 1640 Pima Indians of 15 years and older, 18% of those with two-hour post-load plasma glucose levels of equal to or greater than 200 mg/dl had some evidence of retinopathy.(29)

Two studies performed in Australia showed the prevalence of diabetic retinopathy in newly diagnosed type 2 non-treated diabetic patients to be 14%-20%.(30, 31)

In Kenya, overall, the prevalence of diabetic retinopathy and clinically significant macular oedema was 30.4% and 8.7% respectively among newly diagnosed black African patients.(32)

The differences in the reported prevalence of retinopathy in people with newly discovered type 2 diabetes might be due to variation in the time between onset and detection of diabetes. This could be a result of socioeconomic factors, which determine the access to and availability of medical care, the health care seeking behaviour of the specific group studied, as well as variation in the definitions used to define the presence of diabetes.

The low prevalence in the current study could be attributed to the fact that the Saudi health system is free of charge and results in early diagnosis of diabetic patients. Similarly, in a population-based study in Denmark, the prevalence of DR was reported to be 5%-8%. They suggested that the low prevalence is due to the Danish health system which is free of charge and results in early diagnosis of diabetic patients.(33)

In accordance with others,(22,34) DR was more prevalent among older diabetic patients in the present survey although it is not statistically significant. This could be due to the small number of patients (n=13) who developed DR in the present study. In addition, the present study reports a significant association between prevalence of DR and female gender and not working status. This could be due to the confounding effect of age with these two factors. Again, due to the small number of patients who developed DR, we could not perform Logistic regression analysis to control for the effect of age on the development of DR.

Evaluation of diabetic patients who sought ophthalmologic consult for the first time in Farabi Hospital in Iran showed that 48.4% of patients were diagnosed as non-PDR and 45.4% of them were PDR.23 In the present study, all DR cases were classified using Friedman's standards as background or non-proliferative diabetic retinopathy.

In addition, the average time to seek ophthalmologic consult after diagnosis of diabetes mellitus was 11.5± 5.5 years in Farabi Hospital`s study. All the data revealed that those patients designated as newly diagnosed diabetes mellitus have had the disease for a significant duration of time and after diagnosis of their disease their ophthalmologic examination was postponed until it was too late for effective treatment of diabetic retinopathy. It is believed that undiagnosed type 2 diabetes mellitus may occur 4-12 years before its clinical diagnosis and that diabetes may be present for five years before the onset of retinopathy.(35,36) Undiagnosed type 2 diabetes is thus not a benign condition. The unknown duration (years) of undiagnosed diabetes in our patients is likely to be a more important contributory factor to retinopathy than the known (weeks) duration of diagnosis. This is further supported in the present study by the fact that patients with diabetic retinopathy were older than those without.

This existence of DR among newly diagnosed diabetic type 2 patients may be also due to the fact that patients are more likely to consult a medical doctor than eye care professionals in dealing with signs and symptoms of medical conditions such as DM. Optometrists are also more likely perceived by patients as professionals who deal more with refractive conditions rather than medical problems, especially amongst the elderly population. However, the role of optometrists as part of primary health care in the screening and management of diabetic retinopathy has been recognized and documented in the National Service Framework in Britain and the Strategy Implementation plan in Australia.(37,38)

Among important limitations of the present study, we did not include other factors that could be associated with the development of DR in newly diagnosed diabetic patients such as glycemic control, hypertension, body mass index (BMI), smoking, serum lipids and presence of microalbuminuria (MA) due to lack of sufficient time and resources. Due to the cross-sectional nature of the survey, we cannot draw definitive causal conclusions about the observed relationships between demographic and disease characteristics and DR.

CONCLUSION


The prevalence of retinopathy in newly diagnosed type 2 diabetes mellitus patients was found to be relatively low in this study. The prevalence was significantly higher among female and not working patients. All DR cases were classified using Friedman's standards as background or non-proliferative diabetic retinopathy. Intra-ocular pressure was within normal values for all patients.

RECOMMENDATIONS

Although, we reported a relatively low prevalence rate of diabetic retinopathy, there is a need for intensifed efforts for early diagnosis of type 2 diabetes mellitus and careful fundus biomicroscopic examination of all newly diagnosed type 2 diabetics in our community where diabetes type 2 is highly prevalent.

1. Population-based studies are suggested with larger sample sizes to determine a better estimation of DR prevalence among Saudi newly diagnosed diabetic patients and study its associated risk factors.
2. There should be emphasis for all optometrists to become competent in the diagnosis and management of ocular manifestations of systemic conditions such as diabetes.
3. Further prospective longitudinal studies are recommended for diabetic patients free from DR at the onset to confirm the causal association between DR and possible associated factors as well as to enable a more precise determination of the onset of diabetic retinopathy.
4. Screening program for early diagnosis of type 2 diabetes mellitus, and consequently diminishing its complications including retinopathy, should be encouraged.

Ethical and administrative considerations: All the necessary official permissions were fully obtained before study conduction. The collected data were kept strictly confidential and used only for research purposes. Verbal informed consent was obtained from all participants.

REFERENCES

1. Diabetes Care. Diabetic Retinopathy. American Diabetes Association Journals, 2000; 73-6.
2. U-Din J, Qureshi M, Khan A, Khan M, Ahmad K. Prevalence of diabetic retinopathy among individuals screened positive for diabetes in five community-based eye camps in Northern Karachi, Pakistan. Journals of Ayub Medical College: Abbottabad, 2006; 40-3
3. Diabetes Care. Standards of medical care for patients with Diabetes mellitus. American Diabetes Association Journals, 2003; 49.
4. Fong D, Aiello L, Gardner, T, Ferris F, Klein R, et al. Diabetic retinopathy. American Diabetes Association Journals, 2004; 27(10): 2540-53.
5. Klein R, Klein B, Moss S. The Wisconsin epidemiological study of diabetic retinopathy: a review. Diabetes Metabolism Review, 1989: 5(7): 559-70.
6. Diabetes Atlas - International Diabetes Federation (IDF). Retrieved from International Diabetes Federation: 2012; http://www.idf.org/diabetesatlas/5e/middle-east-and-north-africa
7. Amos A, McCarty D, Zimmet P. The rising global burden of diabetes and its complications: estimates and projections to the year 2010. Diabetic Medicine; a Journal of the British Diabetic Association, 1997; 14 (Supp3): S1-85.
8. Javitt J, Aiello L, Chiang Y, Ferris F, Canner J, Greenfield S. Preventive eye care in people with diabetes is cost-saving to the federal government: implications for health-care reform. Diabetes Care, 1994; 17(8): 909-17.
9. National Diabetes Data Group. Diabetes in America. 1995; (Vol. 2nd ed). Bethesda, MD, Maryland: NIH Publications.
10. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The New England Journal of Medicine, 1993; 329(14): 977-86.
11. UK Prospective Diabetes Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. British Medical Journal 1998; 703-13.
12. Vijan S, Hofer T, Hayward R. Cost-utility analysis of screening intervals for diabetic retinopathy in patients with type 2 diabetes mellitus. JAMA, 2000; 283(7): 889-96.
13. Javitt J, Aiello L. Cost-effectiveness of detecting and treating diabetic retinopathy. Annals of Internal Medicine Journals, 1996; 124(1PT2): 164-9.
14. Cai X, Wang F, Ji L. Risk Factors of Diabetic retinopathy in type 2 diabetic patients. Chinese Medical Journal (English Edition), 2006;119(10): 822-6.
15. Waked N, Nacouzi R, Haddad N, Zain R. Epidemiology of diabetic retinopathy in Lebanon. Journal Francais D Ophtalmologie (J Fr Ophtalmol), 2006; 29(3): 289-95.
16. Mwendwa F, Otieno C, Kayima J, Amayo E, Otieno P. Risk factor profile and the occurrence of microvascular complications in short-term type 2 diabetes mellitus at Kenyatta National Hospital, Nairobi. East African Medical Journal, 2005; 82(12 Suppl): S163-72.
17. Herrera-Bombo J, Aguilar-Diosdado M, Hawkins F, Campos M, Moreno A, et al. Is increasing urinary albumin a better marker for microvascular than for macrovascular complication of type 2 diabetes mellitus? Nephron Clinical Practice - Karger Publisher, 2005; 116-21.
18. Parving H, Lewis J, Rayid M, Remuzzi G. Demand investigators. Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: a global perspective. Kidney Int, 2006; 69(11): 2057-63.
19. Raosoft ® Sample Size Calculator. Retrieved from Raosoft ®: http://www.raosoft.com/samplesize.html. 2013
20. Freidman NJ, Kaiser PK, Trattler WB. Review of Ophthalmology 2005; (Vol 1st edition). Pennsylvania, Philadelphia: Elsevier. Inc.
21. Diabetes Prevention Program Research Group. The prevalence of retinopathy in impaired glucose tolerance and recent-onset diabetes in the Diabetes Prevention Program. Diabetic Med 2007; 24: 137-44.
22. Wahab S, Mahmood N, Shaikh Z, Kazmi WH. Frequency of retinopathy in newly diagnosed type 2 diabetes patients. JPMA 2008; 58: 557-61.
23. Abdollahi A, Malekmadani M H, Mansoori M R, Bostak A, Abbaszadeh M R, Mirshahi A. Prevalence of diabetic retinopathy in patients with newly diagnosed type II diabetes mellitus. Acta Medica Iranica 2006; 44: 415-9.
24. Agarwal S, Raman R, Kumari RP, Deshmukh H, Paul PG, Gnanamoorthy P, et al. Diabetic retinopathy in type II diabetics detected by targeted screening versus newly diagnosed in general practice. Ann Acad Med Singapore 2006; 35: 531-5.
25. Rema M, Premkumar S, Anitha B, Deepa R, Pradeepa R, Mohan V. Prevalence of diabetic retinopathy in urban India: the Chennai Urban Rural Epidemiology Study (CURES) eye study, I. Invest Ophthalmol Vis Sci 2005; 46: 2328-33.
26. Rema M, Deepa R, Mohan V. Prevalence of retinopathy at diagnosis among type 2 diabetic patients attending a diabetic center in South India. Br J Ophthalmol 2000; 84: 1058-60.
27. Klein R, Klein BE, Moss SE, Linton KL. The Beaver Dam Eye Study. Retinopathy in adults with newly discovered and previously diagnosed diabetes mellitus. Ophthalmology 1992; 99: 58-62.
28. Kohner EM, Aldington SJ, Stratton IM, Manley SE, Holman RR, Mathews DR, et al. United Kingdom Prospective Diabetes Study, 30: diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors. Arch Ophthalmol 1998; 116: 297-303.
29. Dorf A, Ballintine EJ, Bennett PH, Miller M. Retinopathy in Pima Indians. Relationships to glucose level, duration of diabetes, age at diagnosis of diabetes, and age at examination in a population with a high prevalence of diabetes mellitus. Diabetes. 1976; 25(7): 554-60.
30. Owens DR, Volund A, Jones D, Shannon AG, Jones IR, Birtwell AJ, et al. Retinopathy in newly presenting non-insulin-dependent (type 2) diabetic patients. Diabetes Res. 1988; 9(2): 59-65.
31. Nguyen HT, Luzio SD, Dolben J, West J, Beck L, Coates PA, Owens DR. Dominant risk factors for retinopathy at clinical diagnosis in patients with type II diabetes mellitus. J Diabetes Complications. 1996; 10(4): 211-19.
32. Nkumbe HE, Kollmann KH, Gaeckle HC. Assessment of diabetic retinopathy in newly diagnosed black Kenyan type 2 diabetics. East Afr Med J. 2010; 87(3): 109-14.
33. de Fine Olivarius N, Nielsen NV, Andreasen AH. Diabetic retinopathy in newly diagnosed middle-aged and elderly diabetic patients. Prevalence and interrelationship with microalbuminuria and triglycerides. Graefes Arch Clin Exp Ophthalmol. 2001; 239(9): 664-72.
34. Talu S, Kaucsar E, Soreanu A. Diabetic retinopathy in newly diagnosed patients with type II diabetes mellitus. Oftalmologia. 2002; 54(3): 27-30.
35. Ramachandran A, Snehalatha C, Vijay V. Viswanathan M. Diabetic retinopathy at the time of diagnosis of NIDDM in south Indian subjects. Diabetes Res. Clin. Pract. 1996; 32: 111-14.
36. Harris, MI, Klein R, Welborn TA, Knuiman MW. Onset of NIDDM occurs at least 4-7 years before clinical diagnosis. Diabetes Care. 1992; 15: 815-19.
37. Layland B. National diabetes visual impairment program. Clin Exp Optom 2001; 84: 1-3.
38. Verma L, Gunjan P, Terwari HK, Gupta SK, Murthy GVS, Sharma N. Screening for diabetic retinopathy by non-ophthalmologist: an effective public health tool. Acta Ophthalmologica Scandinavica 2003; 81: 373-7.

.................................................................................................................