Contribution of ultra-wide field fluorescein angiography in diabetic retinopathy in a Tunisian population
##plugins.themes.academic_pro.article.main##
Abstract
Aim: To assess the contribution of ultra-wide field (UWF) fluorescein angiography (FA) in clinically non proliferative diabetic retinopathy (DR) and to study the relationship between peripheral vascular lesions and the presence of diabetic macular edema (DME).
Methods: Retrospective study of consecutive UWF-FA obtained using a wide-field contact lens system. DME was detected on both FA and spectral-domain optical coherence tomography (SD-OCT).
Results: A total of 71 eyes of 39 diabetic patients with clinically non proliferative DR (NPDR) was included. DR was clinically graded as severe NPDR in 52 eyes (73%), moderate NPDR in 15 eyes (21%) and mild NPDR in 4 eyes (6%).
On UWF-FA, DR was predominantly anterior in 14% of cases (10/71), predominantly posterior in 48% of cases (34/71) and diffuse in 38% of cases (27/71). Retinal non perfusion was present in 87% of eyes (62/71), predominating in superior-temporal areas. Peripheral vessel leakage was present in 85% of cases (60/71) and retinal neovascularization was noted in 14% of cases (10/71), unpgrading DR severity from NPDR to proliferative DR in 10 eyes.
DME was present on SD-OCT in 53% of cases. Central macular thickness was significantly higher in eyes with retinal non-perfusion (353 μm vs. 254 μm, p=0,006) and retinal non-perfusion was associated with macular edema (97% vs. 76%, p=0,01) and poor visual acuity (p<0.001). Peripheral vessel leakage was associated with retinal non-perfusion (p<0.001) and retinal neovascularization (53% vs. 35%, p=0.01), but it was not associated with the presence of DME (p=0.449).
Conclusion: UWF-FA was of great help assessing DR and evaluating peripheral retinal lesions in order to refine DR staging and to guide laser treatment. Besides, it allows better understanding of DME pathophysiology.
Keywords:
Diabetic retinopathy; ultra-wide field fluorescein angiography; anterior diabetic retinopathy; retinal non perfusion; peripheral vascular leakage; retinal neovascularization; diabetic macular edema##plugins.themes.academic_pro.article.details##
References
- 1. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010; 376: 124-36. 2. Khandekar R. Screening and public health strategies for diabetic retinopathy in the Eastern Mediterranean region. Middle East Afr J Ophthalmol. 2012; 19: 178-84. 3. Bouguerra R, Alberti H, Salem LB, et al. The global diabetes pandemic: the Tunisian experience. Eur J Clin Nutr. 2007; 61. 4. Saidi O, O'Flaherty M, Mansour N Ben, et al. Forecasting Tunisian type 2 diabetes prevalence to 2027: validation of a simple model. BMC Public Health. 2015; 15: 104. 5. Rivero ME, Bartsch DU, Otto T, Freeman WR. Automated scanning laser ophthalmoscope image montages of retinal diseases. Ophthalmology. 1999; 106: 2296-300. 6. Early Treatment Diabetic Retinopathy Study Research Group. Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Ophthalmology. 1991; 98: 823-33. 7. Fischer J, Otto T, Delori F, Pace L, Staurenghi G. Scanning Laser Ophthalmoscopy (SLO). In: High Resolution Imaging in Microscopy and Ophthalmology. Cham: Springer International Publishing; 2019. p. 35-57. 8. Hassenstein A, Meyer CH. Clinical use and research applications of Heidelberg retinal angiography and spectral-domain optical coherence tomography - a review. Clin Experiment Ophthalmol. 2009; 37: 130-43. 9. Staurenghi G, Viola F, Mainster MA, Graham RD, Harrington PG. Scanning laser ophthalmoscopy and angiography with a wide-field contact lens system. Arch Ophthalmol. 2005; 123: 244-52. 10. Witmer MT, Parlitsis G, Patel S, Kiss S. Comparison of ultra-widefield fluorescein angiography with the Heidelberg Spectralis(®) noncontact ultra-widefield module versus the Optos(®) Optomap(®). Clin Ophthalmol. 2013; 7: 389-94. 11. Friberg TR, Gupta A, Yu J, et al. Ultrawide angle fluorescein angiographic imaging: a comparison to conventional digital acquisition systems. Ophthalmic Surg Lasers Imaging Retina. 2008; 39: 304-11. 12. Csutak A, Lengyel I, Jonasson F, et al. Agreement between image grading of conventional (45°) and ultra wide-angle (200°) digital images in the macula in the Reykjavik eye study. Eye. 2010; 24: 1568-75. 13. Mackenzie PJ, Russell M, Ma PE, Isbister CM, Maberley DAL. Sensitivity and specificity of the optos optomap for detecting peripheral retinal lesions. Retina. 2007; 27: 1119-24. 14. Wessel MM, Aaker GD, Parlitsis G, Cho M, D'Amico DJ, Kiss S. Ultra-wide-field angiography improves the detection and classification of diabetic retinopathy. Retina. 2012; 32: 785-91. 15. Silva PS, Dela Cruz AJ, Ledesma MG, et al. Diabetic Retinopathy Severity and Peripheral Lesions Are Associated with Nonperfusion on Ultrawide Field Angiography. Ophthalmology. 2015; 122: 2465-72. 16. Talks SJ, Manjunath V, Steel DHW, Peto T, Taylor R. New vessels detected on wide-field imaging compared to two-field and seven-field imaging: implications for diabetic retinopathy screening image analysis. Br J Ophthalmol. 2015; 99: 1606-9. 17. Oliver SCN, Schwartz SD. Peripheral vessel leakage (PVL): a new angiographic finding in diabetic retinopathy identified with ultra wide-field fluorescein angiography. Semin Ophthalmol. 2010; 25: 27-33. 18. Kong M, Lee MY, Ham D-I. Ultrawide-field fluorescein angiography for evaluation of diabetic retinopathy. Korean J Ophthalmol. 2012; 26: 428-31. 19. Wessel MM, Nair N, Aaker GD, Ehrlich JR, D'Amico DJ, Kiss S. Peripheral retinal ischaemia, as evaluated by ultra-widefield fluorescein angiography, is associated with diabetic macular oedema. Br J Ophthalmol. 2012; 96: 694-8. 20. Patel RD, Messner L V, Teitelbaum B, Michel KA, Hariprasad SM. Characterization of ischemic index using ultra-widefield fluorescein angiography in patients with focal and diffuse recalcitrant diabetic macular edema. Am J Ophthalmol. 2013; 155: 1038-1044.e2. 21. Sim DA, Keane PA, Rajendram R, et al. Patterns of peripheral retinal and central macula ischemia in diabetic retinopathy as evaluated by ultra-widefield fluorescein angiography. Am J Ophthalmol. 2014; 158: 144-153.e1. 22. Silva PS, Cavallerano JD, Sun JK, Soliman AZ, Aiello LM, Aiello LP. Peripheral lesions identified by mydriatic ultrawide field imaging: distribution and potential impact on diabetic retinopathy severity. Ophthalmology. 2013; 120: 2587-95. 23. Jiang AC, Srivastava SK, Hu M, et al. Quantitative Ultra-Widefield Angiographic Features and Associations with Diabetic Macular Edema. Ophthalmol Retin. 2020; 4: 49-56. 24. Bae K, Lee JY, Kim TH, et al. Anterior Diabetic Retinopathy Studied by Ultra-widefield Angiography. Korean J Ophthalmol. 2016; 30: 344-51. 25. Sawada O, Ichiyama Y, Obata S, et al. Comparison between wide-angle OCT angiography and ultra-wide field fluorescein angiography for detecting non-perfusion areas and retinal neovascularization in eyes with diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2018; 256: 1275-80. 26. Couturier A, Rey P-A, Erginay A, et al. Widefield OCT-Angiography and Fluorescein Angiography Assessments of Nonperfusion in Diabetic Retinopathy and Edema Treated with Anti-Vascular Endothelial Growth Factor. Ophthalmology. 2019; 126: 1685-94. 27. Cui Y, Zhu Y, Wang JC, et al. Comparison of widefield swept-source optical coherence tomography angiography with ultra-widefield colour fundus photography and fluorescein angiography for detection of lesions in diabetic retinopathy. Br J Ophthalmol. 2021; 105: 577-81. 28. Tan CS, Chew MC, van Hemert J, Singer MA, Bell D, Sadda SR. Measuring the precise area of peripheral retinal non-perfusion using ultra-widefield imaging and its correlation with the ischaemic index. Br J Ophthalmol. 2016; 100: 235-9. 29. Fan W, Uji A, Borrelli E, et al. Precise Measurement of Retinal Vascular Bed Area and Density on Ultra-wide Fluorescein Angiography in Normal Subjects. Am J Ophthalmol. 2018; 188: 155-63. 30. Fan W, Uji A, Nittala M, et al. Retinal vascular bed area on ultra-wide field fluorescein angiography indicates the severity of diabetic retinopathy. Br J Ophthalmol. 2021;