ORIGINAL RESEARCH

 

Clinical characteristics and associated factors of diabetic retinopathy in Sudanese patients

 

 

Nuha M. Muhjoub^{I, II}; Saif H. Alrasheed^{III, IV}; Yazan Gammoh^I; Abdelaziz M. Elmadina^III

^IDepartment of Optometry Science, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman, Jordan
^IIDepartment of Medical Photography, Faculty of Optometry and Visual Sciences, Al-Neelain University, Khartoum, Sudan
^IIIDepartment of Optometry, College of Applied Medical Sciences, Qassim University, Buraydah, Saudi Arabia
^IVDepartment of Binocular Vision, Faculty of Optometry and Visual Sciences, Al-Neelain University, Khartoum, Sudan

Correspondence

 

 

---

ABSTRACT

BACKGROUND: Diabetic retinopathy (DR) is a leading cause of vision loss and preventable blindness, particularly in middle- and high-income countries
AIM: This study aimed to assess the characteristics and associated factors of DR in Sudanese patients with type 2 diabetes mellitus (DM
SETTING: A cross-sectional hospital-based study included 119 patients with type 2 DM was conducted at EL-Walidain Eye Hospital, Khartoum, Sudan, from February 2021 to May 2021
METHODS: A non-mydriatic digital fundus camera was used for fundus photography, and Scottish Diabetic Retinopathy Grading Scheme was used for the final classification of DR
RESULTS: Females comprised 53.8% of patients, mean age of 58.8 ± 8.5 years. Uncontrolled DM was found in 37.8% with a mean duration of 10.5 ± 4.8 years. Myopia was the most common refractive error found in 57.8% of the uncontrolled group, followed by emmetropia (17.8%). Whereas in the controlled group, 47.3% were hyperopic and 39.2% were myopic. Maculopathy grade M1 was found to be 37.8% in the uncontrolled group and 18.9% in the controlled group, with no significant difference (p = 0.361). Conversely, the difference in retinopathy between the two groups was statistically significant (p = 0.043
CONCLUSION: Decreased vision and increased retinopathy were associated with an increase in patients' age. More widespread diabetes awareness and screening programmes to improve diabetes management and control in Sudan and other developing countries
CONTRIBUTION: This study observed maculopathy grade M1 and myopia were more common in uncontrolled DM, and vision function was inversely correlated with age (p < 0.05

Keywords: diabetes mellitus; retinopathy; maculopathy; diabetic retinopathy; Sudan.

---

 

 

Introduction

Diabetes mellitus (DM) is a metabolic disorder that causes high blood sugar levels because of problems with insulin: a hormone that regulates blood sugar.^1,2 There are two main types of DM: type 1 and type 2. Type 1 DM, commonly called juvenile-onset or insulin-dependent DM, usually starts in childhood. Whereas Type 2, known as adult-onset or non-insulin-dependent DM, typically develops after the age of 40 years and becomes more common with the advancement of age.^2,3 Type 2 DM is more prevalent and often associated with lifestyle factors like diet and physical activity. According to the World Health Organization (WHO), around 462 million people worldwide have DM, most of them living in low- and middle-income countries where access to healthcare is limited.^4,5,6,7 Sub-Saharan Africa experiencing a diabetes epidemic that leads to considerable health problems, including preventable visual loss caused by diabetic retinopathy (DR).⁸

Diabetic retinopathy is an eye disease that causes damage to the retina and is considered as the primary cause of vision loss and avoidable blindness among adults aged 20-74 years, especially in middle- and high-income countries.⁹ In 2020, it was estimated that about 103.12 million adults worldwide suffer from DR, 28.54 million people have vision-threatening DR, and 18.83 million persons have clinically significant macular oedema. By 2045, these numbers are expected to increase by approximately 30% - 50%; with 160.50 million persons predicted to suffer from DR, 44.82 million people will have vision-threatening DR, and 28.61 million will have macular oedema.^{10,11,12,13,14,15} A study was conducted to assess the prevalence and incidence of DR and diabetic maculopathy in African countries. It was reported that prevalence range in patients with diabetes for DR was 30.2% - 31.6%, proliferative DR 0.9% - 1.3% and any maculopathy 1.2% - 4.5%.¹⁶ Diabetic retinopathy has two stages: non-proliferative diabetic retinopathy (NPDR) and proliferative diabetic retinopathy (PDR). The NPDR is the initial stage where small blood vessels in the retina leak fluid or blood, leading to retinal enlargement and the formation of deposits called exudates.^8,9,10 Whereas the PDR is the most advanced stage of DR, in this condition, new blood vessels begin to grow on the surface of the retina, but they are fragile and can bleed into the vitreous, resulting in severe vision loss and even blindness.^11,12

The grading system for DR helps eye care professionals to monitor and manage the progression of the condition, enabling timely intervention to preserve vision. It involves various stages, ranging from mild to severe. The widely used grading system is the Early Treatment Diabetic Retinopathy Study (ETDRS) classification, as follows: The stages include no apparent retinopathy (NDR); this stage occurs in the early years of DM and shows no visible signs of DR. In mild NPDR, microaneurysms appear in the retina's blood vessels, but vision is usually not significantly affected. In moderate NPDR, alongside microaneurysms, there is a greater presence of haemorrhage exudates in the retina, and vision may be mildly affected. Whereas in severe NPDR, this stage reveals more pronounced changes, including significant haemorrhages and other signs of blood vessel damage, and vision is more likely to be affected.^12,17,18 Conversely, the Scottish Grading protocol is used to grade the severity of retinopathy and maculopathy. Retinopathy is graded from R0 to R4, while maculopathy has separate grades from M0 to M2. R6 is a grade for poor-quality images that cannot be graded. If patients have technical failures during photography, they need to undergo further screening using slit lamp biomicroscopy.¹⁹

Previous studies^19,20,21 reported that detecting DR through screening requires an approximately 30-min examination of the ocular fundus, which helps to identify the condition early on and improve treatment outcomes. Early management delays the consequences that lead to vision impairment or lessens the likelihood of worsening the impairment.^19,20,21 The management of DR involves medical and surgical interventions. Treatment options include controlling blood sugar levels and using anti-vascular endothelial growth factor (VEGF) drugs such as ranibizumab or aflibercept, which are injected into the eye to treat diabetic macular oedema and PDR.^21,22 As well as other medical modalities used to manage DR, such as statins, renal compromise, the use of angiotensin-converting enzyme (ACE) inhibitors or Ag II inhibitors. This study was conducted to assess the clinical characteristics and associated factors of DR in Sudanese patients attending a not-for-profit tertiary eye care centre.

 

Methods

Study design

This was a cross-sectional hospital-based study conducted at the retina clinic of EL-Walidain Eye Charity Hospital in Khartoum city in the period from February to May 2021. EL-Walidain Eye Charity Hospital is a specialised eye centre that treats patients from various regions and backgrounds across Sudan.

Sample

The study included 119 patients who were already diagnosed with type 2 diabetes. They were selected from patients who came to the hospital seeking eye care, and their ages ranged from 40 years to 75 years. The sample included 64 females and 55 males from different regions of Sudan, who attended the retina clinic in El-Walidain Charity Eye Hospital and were willing to participate in the study.

Inclusion criteria

The study included adults aged 40-75 years old with type 2 DM as the inclusion criteria. Individuals below 40 years of age and pregnant women were excluded from the study, and any person who had previous eye surgery was also not included in the study.

Data collection procedures

For all diabetic patients who visited the retina clinic, their demographic information was collected. The investigator asked the patients to provide background and personal information, as well as the patients' medical history and common diabetes symptoms. This included a review of both the ocular and systemic status of the patient, along with the diabetic history, including duration of diabetes, blood sugar control, medical status and family history. Participants were subjected to comprehensive ocular examinations. Slit lamp biomicroscopy was used to examine the anterior segment of the eye. Visual acuity (VA), best-corrected visual acuity (BCVA) and pinhole were estimated by Snellen's E-test type. The refractive status of the eye was evaluated by an autorefractometer (Nidek, Gamagori, Japan). Finally, for the patient's posterior segment examination, the study used seven-field fundus photography. The seven fields from 1 to 7 are the optic disc, macula, temporal to the macula, superior temporal, inferior temporal, superior nasal and inferior nasal, respectively. The VISUCAM^® 500 (Zeiss GMBH, Jena); a non-mydriatic digital fundus camera, which allows taking photographs through pupils as small as 3.3 mm, was used for imaging and evaluating the retina thoroughly for the presence of DR. Based on the Scottish Diabetic Retinopathy Grading Scheme (SDRGS)¹⁹ screening and referral programme for DR that was adapted for use in Sudan, fundus images were analysed, diabetic and macular retinopathy were graded and action was taken as seen in Table 1.

Microaneurysms were recorded by viewing them in colour and red free. Intraretinal microvascular abnormality (IRMA) was recorded when visible on colour images without enlarging the image area.

Data analysis

Descriptive and comparative statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) for Windows version 24 (SPPS Inc., Chicago, IL, United States). Data were reported as mean ± standard deviation (s.d.). Pearson's correlation was used to find the relationship between dependent and independent variables among the study population. A p-value of ˂ 0.05 was considered to be statistically significant with a 95% confidence level (CL).

Ethical considerations

Ethical permission for the study was obtained from the Ethics Committee of Al-Neelain University (approval No. 21-01-12). The study was conducted according to the Declaration of Helsinki guidelines. Participants in the research provided verbal consent after receiving detailed information about the study. They had the right to withdraw at any stage without facing any penalties. Patients' confidentiality was maintained by assigning codes to the participants' information.

 

Results

Demographic information

This study included 119 patients with DM type 2 whose ages ranged from 40 years to 75 years, with a mean age of 58.8 ± 8.5 years. About 55 of them were males (31 controlled DM type 2 and 24 with uncontrolled DM type 2), and 64 were females (43 controlled DM type 2 and 21 with uncontrolled DM type 2). Diabetes mellitus duration was significantly different (p < 0.001) between the controlled group, whose duration ranged from 1 years to 19 years with a mean of 7.1 ± 4.5 years and the uncontrolled group, whose duration ranged from 1 years to 20 years with a mean of 10.5 ± 4.8 years. Mean and s.d. of blood sugar level using cumulative haemoglobin HbA1C for controlled and uncontrolled MD were 5.93 ± 1.1 and 7.89 ± 2.1, respectively, p = 0.0001.

Distribution of visual acuity and refractive error among participants

Refractive error among the participants showed the following: 47.3%, 12.2%, 39.2% and 1.4% of the controlled group were hyperopes, myopes, emmetropes and of no fundus reflex, respectively. While in the uncontrolled group, 13.3%, 57.18%, 17.8% and 11.1% were hyperopes, myopes, emmetropes and had no fundus reflex, respectively. Paired samples T test showed non-significant differences between unaided VA and BCVA of right and left eyes for both controlled and uncontrolled eyes (p > 0.05), as shown in Table 2. Unaided VA was found to be strongly inversely correlated with age (p < 0.05), while BCVA was found to be weakly inversely correlated with age (p > 0.05). Table 3 shows the distribution of methods used to control DM among participants.

 

 

 

 

Maculopathy grading among the participants

Regarding maculopathy, most of the patients with controlled DM, 58 (78.4%), had no maculopathy; only 14 (18.9%) had grade M1 of maculopathy. While in the patients with uncontrolled DM, no maculopathy was found in 23 (51.1%), and grade M1 maculopathy was found in 17 (37.2%). Maculopathy among the patients with controlled and uncontrolled DM was statistically not significant (p = 0.361), as shown in Table 4.

 

 

Retinopathy grading among the participants

Retinopathy grading among the participants with controlled DM showed the following: 20 (27%) had mild retinopathy, 13 (17.6%) had moderate retinopathy and 8 (10.8%) had severe retinopathy. Whereas in the uncontrolled group, 10 (22.2%) had mild retinopathy, 9 (20.0%) had moderate retinopathy. Nine (20.0%) had severe retinopathy, and 5 (11.1%) had proliferative retinopathy. The difference in retinopathy between patients with controlled and uncontrolled DM was statistically significant (p = 0.043), as shown in Table 5. Table 6 shows the distribution of photocoagulation among participants.

 

 

 

 

Discussion

Diabetic retinopathy is a common eye disorder worldwide, especially among people living in low- and middle-income countries.⁹ If left unmanaged, DR may lead to visual impairment and blindness.⁹ It is crucial to acknowledge that there are substantial ethnic-based differences in the clinical features and contributing factors of DR, with higher prevalence observed across people of African descent.²³ Thus, our present study was conducted to assess the clinical characteristics and associated factors of DR in Sudanese patients with DM type 2 seeking eye care.

An earlier study showed that decreased vision function in DR was associated with an increase in patients' age.²³ This study revealed that the unaided VA and BCVA were strongly inversely correlated with age. Furthermore, the study showed that increased retinopathy was associated with an increase in patients' age. Our finding is consistent with a previous study,²⁴ which reported that DR showed a strong correlation with factors such as older age, elevated blood glucose levels and increased HbA1c levels. This study showed that considerable numbers of patients with DM remain without any method of control, and with a long duration of diabetes, some extending to 20 years. This study found that the duration of DM was a significant influential risk factor for the development of retinopathy. This finding is consistent with previous studies,^25,26 suggesting that the duration of DM is likely the most powerful predictor for the development and progression of DR. These agreed with the Handan Eye Study conducted in rural areas of China, which revealed that DR was linked to a longer duration of DM, high blood sugar levels and hypertension.²⁷ These findings hold significant importance for public health planning in Sudan, highlighting the need for urgent strategies to monitor and manage systematic disorders as well as optimise diabetes control among individuals living with diabetes in rural regions. There is a lack of healthcare facilities in these regions. This study found that myopia was more common in uncontrolled DM compared with controlled groups. This finding highlighted the need for eye care professionals to ensure that DM is controlled or at a normal level when prescribing the correction of uncorrected refractive for patients with DM.

In this study, only 11.1% had PDR, all of them from uncontrolled DM groups. This agreed with the existing literature, which showed that NPDR was more prevalent than proliferative one.^28,29 Various metabolic factors and diseases were identified as risk factors for DR. In several African countries, a notable connection was observed between PDR and complications of diabetes, including diabetic foot, amputation and maculopathy.^29,30,31 This highlights the need for early screening, which would lead to early diagnosis and management.³² It has been observed that early assessment and management would reduce the risk of complications that lead to visual impairment.^19,20,21 Nevertheless, because of scarcity of ophthalmologists in Africa,³² inefficient referrals may hinder the efforts of early detection through screening. It has been suggested that remote screening and tele-diagnosis can alleviate the pressure on the healthcare system and fill the gap.³³ This study did not investigate the role of early detection through screenings or the role of tele-diagnosis. However, it would be of interest to identify these factors in the future as the opportunity for tele-diagnosis in DR is promising for developing countries.³⁴

This study has some limitations. As a result of the cross-sectional study design, the temporal relationship between potential risk factors and outcomes could not be considered. In addition, the study had a short duration, which did not allow for further patient recruitment. Furthermore, the study included a small number of patients with DM all of them were type 2 DM. Despite these factors, we believe that this study provides useful information about the clinical characteristics and associated factors of DR among Sudanese patients with type 2 DM who seek eye care.

 

Conclusion

The study found considerable numbers of patients with DM remain without any method of control and with a long duration of diabetes, some extending to 20 years, which reveals the importance of awareness of diabetic control and regular screening of diabetic patients to prevent visual loss and reduce the rate of DR progression. Maculopathy grade M1 and myopia was more common in uncontrolled DM compared with controlled groups. Decreased vision and increased retinopathy were associated with an increase in patients' age. These facts highlight the need for urgent public health strategies in Sudan to monitor and manage systematic disorders as well as optimise diabetes control.

 

Acknowledgements

Competing interests

The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.

Authors' contributions

N.M.M. and S.H.A was the project leader who was responsible for the experimental and project design, Y.G., A.M.E. made conceptual contributions and provided guidance for the study. N.M.M. and S.H.A. were responsible for the writing of this article with input and edits from Y.G. and A.M.E.

Funding information

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Data availability

Data supporting the findings of this study are available from the corresponding author, N.M.M., on request.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of any affiliated agency of the authors and the publisher.

 

References

1. American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of medical care in diabetes-2021. Diabetes Care. 2021;44(1):5-33. https://doi.org/10.2337/dc21-S002        [ Links ]

2. Petersmann A, Müller-Wieland D, Müller UA, et al. Definition, classification, and diagnosis of diabetes mellitus. Exp Clin Endocrinol Diabetes. 2019;127(1):1-7. https://doi.org/10.1055/a-1018-9078        [ Links ]

3. Kerner W, Brückel J. Definition, classification, and diagnosis of diabetes mellitus. Exp Clin Endocrinol Diabetes. 2014;122(7):384-386. https://doi.org/10.1055/s-0034-1366278        [ Links ]

4. Lovic D, Piperidou A, Zografou I, Grassos H, Pittaras A, Manolis A. The growing epidemic of diabetes mellitus. Curr Vasc Pharmacol. 2020;18(2):104-109. https://doi.org/10.2174/1570161117666190405165911        [ Links ]

5. Zheng Y, Ley S, Hu F. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol. 2018;14(1):88-98. https://doi.org/10.1038/nrendo.2017.151        [ Links ]

6. Khan MAB, Hashim MJ, King JK, Govender RD, Mustafa H, Al Kaabi J. Epidemiology of type 2 diabetes - Global burden of disease and forecasted trends. J Epidemiol Glob Health. 2020;10(1):107-111. https://doi.org/10.2991/jegh.k.191028.001        [ Links ]

7. Wong TY, Sabanayagam C. Strategies to tackle the global burden of diabetic retinopathy: From epidemiology to artificial intelligence. Ophthalmologica. 2020;243(1):9-20. https://doi.org/10.1159/000502387        [ Links ]

8. Burgess PI, Msukwa G, Beare NA. Diabetic retinopathy in sub-Saharan Africa: Meeting the challenges of an emerging epidemic. BMC Med. 2013 Dec;11:1-7. https://doi.org/10.1186/1741-7015-11-157        [ Links ]

9. Vujosevic S, Aldington SJ, Silva P, et al. Screening for diabetic retinopathy: New perspectives and challenges. Lancet Diabetes Endocrinol. 2020;8(4):337-347. https://doi.org/10.1016/S2213-8587(19)30411-5        [ Links ]

10. Glovaci D, Fan W, Wong D. Epidemiology of diabetes mellitus and cardiovascular disease. Curr Cardiol Rep. 2019; 21(1):21. https://doi.org/10.1007/s11886-019-1107-y        [ Links ]

11. Bhatia K, Arora S, Tomar R. Diagnosis of diabetic retinopathy using machine learning classification algorithm. 2016 2nd International Conference on Next Generation Computing Technologies (NGCT); 2016 Oct 14; IEEE; 2016. p. 347-351.         [ Links ]

12. Leasher JL, Bourne RR, Flaxman SR, et al. Global estimates on the number of people blind or visually impaired by diabetic retinopathy: A meta-analysis from 1990 to 2010. Diabetes Care. 2016;39(9):1643-1649. https://doi.org/10.2337/dc15-2171        [ Links ]

13. Mekala KC, Bertoni AG. Epidemiology of diabetes mellitus. In: Orlando G, Piemonti L, Ricordi C, Stratta RJ, Gruessner RWG, editors. Transplantation, bioengineering, and regeneration of the endocrine pancreas. Oxford: Academic Press, 2020; p. 49-58.         [ Links ]

14. Teo ZL, Tham YC, Yu M, et al. Global prevalence of diabetic retinopathy and projection of burden through 2045: systematic review and meta-analysis. Ophthalmology. 2021;128(11):1580-1591. https://doi.org/10.1016/j.ophtha.2021.04.027        [ Links ]

15. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence, and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35(3):556-564. https://doi.org/10.2337/dc11-1909        [ Links ]

16. Burgess PI, MacCormick IJ, Harding SP, Bastawrous A, Beare NA, Garner P. Epidemiology of diabetic retinopathy and maculopathy in Africa: A systematic review. Diabet Med. 2013 Apr;30(4):399-412. https://doi.org/10.1111/j.1464-5491.2012.03756.x        [ Links ]

17. Sivaprasad S, Raman R, Conroy D, et al. The ORNATE India Project: United Kingdom-India Research Collaboration to tackle visual impairment due to diabetic retinopathy. Eye. 2020;34(7):1279-1286. https://doi.org/10.1038/s41433-020-0854-8        [ Links ]

18. Flaxel CJ, Adelman RA, Bailey ST, et al. Diabetic retinopathy preferred practice pattern^®. Ophthalmology. 2020;127(1):66-145. https://doi.org/10.1016/j.ophtha.2019.09.025        [ Links ]

19. Zachariah S, Wykes W, Yorston D. Grading diabetic retinopathy (DR) using the Scottish grading protocol. Community Eye Health. 2015;28(92):72.         [ Links ]

20. Thomas K, Albutt N, Hamid A, Wharton H, Jacob S. Five-year outcomes of digital diabetic eye screening in individuals aged 80 and 85 years. Eye. 2023;20(1):1-5. https://doi.org/10.1038/s41433-023-02577-x        [ Links ]

21. Meredith S, Mourtzoukos S, Rennie C, et al. First year of implementing OCT into a diabetic eye screening service - Quantification of the reduction in hospital eye service referrals. Eye. 2022;36(9):1840-1841. https://doi.org/10.1038/s41433-022-01930-w        [ Links ]

22. Diabetic Retinopathy Clinical Research Network. Aflibercept, bevacizumab, or ranibizumab for diabetic macular edema. N Engl J Med. 2015;372(13):1193-1203. https://doi.org/10.1056/NEJMoa1414264        [ Links ]

23. 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. https://doi.org/10.1371/journal.pone.0032182        [ Links ]

24. Jonas JB, Nangia V, Khare A, et al. Prevalence, and associated factors of diabetic retinopathy in rural central India. Diabetes Care. 2013;36(5):e69. https://doi.org/10.2337/dc12-2377        [ Links ]

25. Manaviat MR, Afkhami M, Shoja MR. Retinopathy, and microalbuminuria in type II diabetic patients. BMC Ophthalmol. 2004;4:9. https://doi.org/10.1186/1471-2415-4-9        [ Links ]

26. Wong TY, Klein R, Islam FM, et al. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006;141(3):446-455. https://doi.org/10.1016/j.ajo.2005.08.063        [ Links ]

27. Wang FH, Liang YB, Peng XY, et al. Risk factors for diabetic retinopathy in a rural Chinese population with type 2 diabetes: The Handan Eye Study. Acta Ophthalmol. 2011;89(4):e336-e343. https://doi.org/10.1111/j.1755-3768.2010.02062.x        [ Links ]

28. Ting DS, Cheung GC, Wong TY. Diabetic retinopathy: Global prevalence, major risk factors, screening practices and public health challenges: A review. Clin Exp Ophthalmol. 2016;44(4):260-277. https://doi.org/10.1111/ceo.12696        [ Links ]

29. Elwali ES, Almobarak AO, Hassan MA, Mahmooud AA, Awadalla H, Ahmed MH. Frequency of diabetic retinopathy and associated risk factors in Khartoum, Sudan: Population-based study. Int J Ophthalmol. 2017;10(6):948-954. https://doi.org/10.18240/ijo.2017.06.18        [ Links ]

30. Jingi AM, Noubiap JJ, Essouma M, et al. Association of insulin treatment versus oral hypoglycaemic agents with diabetic retinopathy and its severity in type 2 diabetes patients in Cameroon, sub-Saharan Africa. Ann Transl Med. 2016;4(20):395. https://doi.org/10.21037/atm.2016.08.42        [ Links ]

31. Mathenge W, Bastawrous A, Peto T, et al. Prevalence, and correlates of diabetic retinopathy in a population-based survey of older people in Nakuru, Kenya. Ophthalmic Epidemiol. 2014;21(3):169-177. https://doi.org/10.3109/09286586.2014.903982        [ Links ]

32. Guigui S, Lifshitz T, Levy J. Diabetic retinopathy in Africa: Advantages of screening. Postgrad Med. 2011;123(4):119-125. https://doi.org/10.3810/pgm.2011.07.2311        [ Links ]

33. Rigato M, Nollino L, Tiago A, et al. Effectiveness of remote screening for diabetic retinopathy among patients referred to Mozambican Diabetes Association (AMODIA): A retrospective observational study. Acta Diabetol. 2022;59(4):563-569. https://doi.org/10.1007/s00592-021-01834-3        [ Links ]

34. Ramasamy K, Mishra C, Kannan NB, Namperumalsamy P, Sen S. Telemedicine in diabetic retinopathy screening in India. Indian J Ophthalmol. 2021 Nov;69(11):2977-2986. https://doi.org/10.4103/ijo.IJO_1442_21        [ Links ]

 

 

Correspondence:
Nuha Mohamed Muhjoub
n.mahjoub@ammanu.edu.jo

Received: 20 Dec. 2023
Accepted: 29 Mar. 2024
Published: 23 May 2024