Volume 25, Issue 1 (Iranian South Medical Journal 2022)                   Iran South Med J 2022, 25(1): 30-41 | Back to browse issues page

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Heidari Z, Sharafi Z. Association of Non-Alcoholic Fatty Liver Dis-ease and Diabetic Retinopathy in Patients with Type 2 Diabetes Mellitus: a Cross-Sectional Study. Iran South Med J 2022; 25 (1) :30-41
URL: http://ismj.bpums.ac.ir/article-1-1545-en.html
1- Department of Internal Medicine, Medical School, Zahedan University of Medical Sciences, Zahedan, Iran , z.heidari10@yahoo.com
2- Department of Epidemiology and Biostatistics, Health School, Zahedan University of Medical Sciences, Zahedan, Iran
Abstract:   (1059 Views)
Background: Diabetic retinopathy is a common chronic complication of diabetes and one of the leading causes of acquired blindness in the world. There is growing evidence that traditional risk factors do not fully justify the onset and progression of diabetic retinopathy. Therefore, some other risk factors such as
non-alcoholic fatty liver disease may be involved in the pathophysiology of diabetic retinopathy.
This study aims to investigate the association of non-alcoholic fatty liver disease with diabetic retinopathy in a group of patients with type 2 diabetes mellitus.

Materials and Methods: This cross-sectional study enrolled 1294 patients with type 2 diabetes mellitus. All participants were evaluated for retinopathy and non-alcoholic fatty liver disease. Systemic examination, eye examination, biochemical tests, and liver ultrasound were performed for all participants. Independent
t-test was used to evaluate the differences between continuous variables and chi-square test was used for qualitative variables.
Multiple logistic regression analysis was used to estimate the odds ratio of different components in the development of diabetic retinopathy. All analyses were performed in STATA software version 22.

Results: Of the participants, 71.87% had non-alcoholic fatty liver disease, and 39.56% had retinopathy. Multivariate logistic regression analysis of risk factors showed that non-alcoholic fatty liver disease and male sex were independently associated with diabetic retinopathy.
Conclusion: This study showed that non-alcoholic fatty liver disease is very common in patients with type 2 diabetes. In these patients, non-alcoholic fatty liver disease is a risk factor for diabetic retinopathy.
Full-Text [PDF 471 kb]   (198 Downloads)    
Type of Study: Original | Subject: Endocrine System
Received: 2021/07/16 | Accepted: 2022/01/11 | Published: 2022/03/13

1. Leoni S, Tovoli F, Napoli L, et al. Current Guidelines For The Management Of Non-Alcoholic Fatty Liver Disease: A Systematic Review With Comparative Analysis. World J Gastroenterol 2018; 24(30): 3361-73.
2. Wong VW, Chan WK, Chitturi S, et al. Asia-Pacific Working Party On Non-Alcoholic Fatty Liver Disease Guidelines 2017-Part 1: Definition, Risk Factors And Assessment. J Gastroenterol Hepatol 2018; 33(1): 70-85.
3. Rinella ME. Nonalcoholic Fatty Liver Disease: A Systematic Review. JAMA 2015; 313(22): 2263-73.
4. Rhee EJ. Nonalcoholic Fatty Liver Disease and Diabetes: An Epidemiological Perspective. Endocrinol Metab 2019; 34(3): 226-33.
5. NCD Risk Factor Collaboration. Trends In Adult Body-Mass Index In 200 Countries From 1975 To 2014: A Pooled Analysis Of 1698 Population-Based Measurement Studies With 19.2 Million Participants. Lancet 2016; 387(10026): 1377-96.
6. Younossi ZM, Koenig AB, Abdelatif D, et al. Global Epidemiology Of Nonalcoholic Fatty Liver Disease-Meta-Analytic Assessment Of Prevalence, Incidence, And Outcomes. Hepatology 2016; 64(1): 73-84.
7. Heidari Z, Gharebaghi A. Prevalence of Non Alcoholic Fatty Liver Disease and its Association with Diabetic Nephropathy in Patients with Type 2 Diabetes Mellitus. J Clin Diagn Res 2017; 11(5): OC04-OC07.
8. Arslan MS, Turhan S, Dincer I, et al. A Potential Link Between Endothelial Function, Cardiovascular Risk, And Metabolic Syndrome In Patients With Non-Alcoholic Fatty Liver Disease. Diabetol Metab Syndr 2014; 6: 109.
9. Song JU, Jang Y, Lim SY, et al. Decreased Lung Function Is Associated With Risk Of Developing Non-Alcoholic Fatty Liver Disease: A Longitudinal Cohort Study. PLoS One 2019; 14(1): e0208736.
10. Hazlehurst JM, Woods C, Marjot T, et al. NonAlcoholic Fatty Liver Disease And Diabetes. Metabolism 2016; 65(8): 1096-108.
11. Perumpail BJ, Khan MA, Yoo ER, et al. Clinical Epidemiology And Disease Burden Of Nonalcoholic Fatty Liver Disease. World J Gastroenterol 2017; 23(47): 8263-76.
12. Alkagiet S, Papagiannis A, Tziomalos K. Associations Between Nonalcoholic Fatty Liver Disease And Ischemic Stroke. World J Hepatol 2018; 10(7): 474-8.
13. Abdeldyem SM, Goda T, Khodeir SA, et al. Nonalcoholic Fatty Liver Disease In Patients With Acute Ischemic Stroke Is Associated With More Severe Stroke And Worse Outcome. J Clin Lipidol 2017; 11(4): 915-9.
14. Mima A. Incretin-Based Therapy for Prevention of Diabetic Vascular Complications. J Diabetes Res 2016; 2016: 1379274.
15. Idilman IS, Akata D, Hazirolan T, et al. Nonalcoholic Fatty Liver Disease Is Associated With Significant Coronary Artery Disease In Type 2 Diabetic Patients: A Computed Tomography Angiography Study 2. J Diabetes 2015; 7(2): 279-86.
16. Yan LH, Mu B, Guan Y, et al. Assessment Of The Relationship Between Non-Alcoholic Fatty Liver Disease And Diabetic Complications. J Diabetes Investig 2016; 7(6): 889-94.
17. Mikolasevic I, Milic S, Wensveen T, et al. Nonalcoholic Fatty Liver Disease - a Multisystem Disease? World J Gastroenterol 2016; 21(43): 9488-505.
18. Chang Y, Ryu S, Sung KC, et al. Alcoholic And Non-Alcoholic Fatty Liver Disease And Associations With Coronary Artery Calcification: Evidence From The Kangbuk Samsung Health Study. Gut 2019; 68(9): 1667-75.
19. Duseja A, Singh SP, Saraswat VA, et al. Non-Alcoholic Fatty Liver Disease And Metabolic Syndrome-Position Paper Of The Indian National Association For The Study Of The Liver, Endocrine Society Of India, Indian College Of Cardiology And Indian Society Of Gastroenterology. J Clin Exp Hepatol 2015; 5(1): 51-68.
20. Zhan YT, Zhang C, Li L, et al. Non-Alcoholic Fatty Liver Disease Is Not Related To The Incidence Of Diabetic Nephropathy In Type 2 Diabetes. Int J Mol Sci 2012; 13(11): 14698-706.
21. Targher G, Byrne CD. Non-Alcoholic Fatty Liver Disease: An Emerging Driving Force In Chronic Kidney Disease. Nat Rev Nephrol 2017; 13(5): 297-310.
22. Campos EJ, Campos A, Martins J, et al. Opening Eyes To Nanomedicine: Where We Are, Challenges And Expectations On Nanotherapy For Diabetic Retinopathy. Nanomedicine 2017; 13(6): 2101-13.
23. Zhang X, Zhao L, Hambly B, et al. Diabetic Retinopathy: Reversibility Of Epigenetic Modifications And New Therapeutic Targets. Cell Biosci 2017; 7: 42.
24. Ashraf H, Afarid M, Shahrzad S. Medical Follow-ups of Patients with Diabetic Retinopathy. Iran South Med J 2010; 13(4): 280-6. (Persian)
25. Afarideh M, Aryan Z, Ghajar A, et al. Association Of Non-Alcoholic Fatty Liver Disease With Microvascular Complications Of Type 2 Diabetes. Prim Care Diabetes 2019; 13(6): 505-14.
26. Zhang M, Li L, Chen J, et al. Presence Of Diabetic Retinopathy Is Lower In Type 2 Diabetic Patients With Non-Alcoholic Fatty Liver Disease. Medicine 2019; 98(18): e15362.
27. Lin TY, Chen YJ, Chen WL, et al. The Relationship between Nonalcoholic Fatty Liver Disease and Retinopathy in NHANES III. PLoS One 2016; 11(11): e0165970.
28. Targher G, Bertolini L, Rodella S, et al. NonAlcoholic Fatty Liver Disease Is Independently Associated With An Increased Prevalence Of Chronic Kidney Disease And Proliferative/ Laser-Treated Retinopathy In Type 2 Diabetic Patients. Diabetologia 2008; 51(3): 444-50.
29. Petersmann A, Muller-Wieland D, Muller UA, et al. Definition, Classification and Diagnosis of Diabetes Mellitus. Exp Clin Endocrinol Diabetes 2019; 127(S 01): S1-S7.
30. Wilkinson CP, Ferris FL 3rd, Klein RE, et al. Proposed International Clinical Diabetic Retinopathy And Diabetic Macular Edema Disease Severity Scales. Ophthalmology 2003; 110(9): 1677-82.
31. Aiello LM. Perspectives On Diabetic Retinopathy. Am J Ophthalmol 2003; 136(1): 122- 35.
32. Tchelepi H, Ralls PW, Radin R, et al. Sonography Of Diffuse Liver Disease. J Ultrasound Med 2002; 21(9): 1023-32.
33. Chalasani N, Younossi Z, Lavine JE, et al. The Diagnosis And Management Of Non-Alcoholic Fatty Liver Disease: Practice Guideline By The American Association For The Study Of Liver Diseases, American College Of Gastroenterology, And The American Gastroenterological Association. Am J Gastroenterol 2012; 107(6): 811-26.
34. Cusi K. Role Of Obesity And Lipotoxicity In The Development Of Nonalcoholic Steatohepatitis: Pathophysiology And Clinical Implications. Gastroenterology 2012; 142(4): 711-25.e6.
35. Dai W, Ye L, Liu A, et al. Prevalence Of Nonalcoholic Fatty Liver Disease In Patients With Type 2 Diabetes Mellitus: A MetaAnalysis. Medicine 2017; 96(39): e8179.
36. 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): 260-77.
37. Dal Canto E, Ceriello A, Ryden L, et al. Diabetes As A Cardiovascular Risk Factor: An Overview Of Global Trends Of Macro And Micro Vascular Complications. Eur J Prev Cardiol 2019; 26(2_suppl): 25-32.
38. Kim BY, Jung CH, Mok JO, et al. Prevalences Of Diabetic Retinopathy And Nephropathy Are Lower In Korean Type 2 Diabetic Patients With Non-Alcoholic Fatty Liver Disease. J Diabetes Investig 2014; 5(2): 170-5.
39. Lv WS, Sun RX, Gao YY, et al. Nonalcoholic Fatty Liver Disease And Microvascular Complications In Type 2 Diabetes. World J Gastroenterol 2013; 19(20): 3134-42.
40. Sasongko MB, Widyaputri F, Agni AN, et al. Prevalence of Diabetic Retinopathy and Blindness in Indonesian Adults With Type 2 Diabetes. Am J Ophthalmol 2017; 181: 79-87.
41. Yun JS, Lim TS, Cha SA, et al. Clinical Course and Risk Factors of Diabetic Retinopathy in Patients with Type 2 Diabetes Mellitus in Korea. Diabetes Metab J 2016; 40(6): 482-93.
42. Yan ZP, Ma JX. Risk Factors For Diabetic Retinopathy In Northern Chinese Patients With Type 2 Diabetes Mellitus. Int J Ophthalmol 2016; 9(8): 1194-9.
43. Abougalambou SS, Abougalambou AS. Risk Factors Associated With Diabetic Retinopathy Among Type 2 Diabetes Patients At Teaching Hospital In Malaysia. Diabetes Metab Syndr 2015; 9(2): 98-103.
44. Targher G, Bertolini L, Scala L, et al. Plasma PAI-1 Levels Are Increased In Patients With Nonalcoholic Steatohepatitis. Diabetes Care 2007; 30(5): e31-2.
45. Abiru S, Migita K, Maeda Y, et al. Serum Cytokine And Soluble Cytokine Receptor Levels In Patients With Non-Alcoholic Steatohepatitis. Liver Int 2006; 26(1): 39-45.
46. Groop PH, Forsblom C, Thomas MC. Mechanisms Of Disease: Pathway-Selective Insulin Resistance And Microvascular Complications Of Diabetes. Nat Clin Pract Endocrinol Metab 2005; 1(2): 100-10.

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