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Graefe's Archive for Clinical and Experimental Ophthalmology

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16.07.2020 | Retinal Disorders

The prognostic value of peripheral retinal nonperfusion in diabetic retinopathy using ultra-widefield fluorescein angiography

verfasst von: Fares Antaki, Razek Georges Coussa, Mikel Mikhail, Cyril Archambault, David E. Lederer

Erschienen in: Graefe's Archive for Clinical and Experimental Ophthalmology | Ausgabe 12/2020

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Abstract

Purpose

To investigate the prognostic value of peripheral retinal nonperfusion in patients with diabetic retinopathy using ultra-widefield fluorescein angiography (UWFA).

Methods

A cross-sectional study included 78 treatment-naïve eyes with nonproliferative and proliferative diabetic retinopathy (NPDR and PDR). Eyes were divided into three groups: mild/moderate NPDR (n = 31), severe NPDR (n = 31), and PDR (n = 16). Three nonperfusion variables were calculated reflecting the proportion of nonperfused to visible retina based on initial UWFA: central nonperfusion (CNP) index, peripheral nonperfusion (PNP) index, and PNP ratio. The relationships between these indices and central subfield thickness (CST) and spectacle-corrected visual acuity (SCVA) were evaluated.

Results

CNP and PNP indices were significantly higher in the PDR group vs. mild/moderate NPDR group (p = 0.007 and 0.008, respectively) but not in the PDR group vs. severe NPDR group (p = 0.149 and p = 0.535, respectively). A significant linear correlation was found between the CNP and PNP indices in both severe NPDR and PDR groups (R² = 0.141, p = 0.041, and R² = 0.311, p = 0.025, respectively). Nonperfusion predominance was not statistically correlated with the presence of macular edema (p = 0.058) or disorganization of retinal inner layers (p = 1). In the severe NPDR group, there was a moderately positive correlation between CNP index and CST (r_s = 0.496, p = 0.019) and no correlation between CNP index and SCVA when controlling for CST (p = 0.160). In the PDR group, a strong negative correlation between PNP ratio and CST was found (r_s = −0.659, p = 0.014), but no correlation was observed between CNP index, CST, and SCVA. In the PDR group, a positive correlation was found between PNP index, PNP ratio, and SCVA (r_s = 0.549, p = 0.027, and r_s = 0.626, p = 0.010, respectively), even after controlling for CST (r_s = 0.599, p = 0.040).

Conclusions

Higher amounts of retinal nonperfusion are seen in patients with more severe retinopathy. Increased CNP is associated with macular thickening and subsequent vision loss. Having predominantly PNP was independently associated with worse VA, regardless of macular thickness. Further studies are needed to investigate the role of PNP in vision loss in diabetic retinopathy.

Antonetti DA, Klein R, Gardner TW (2012) Diabetic retinopathy. N Engl J Med 366(13):1227–1239. https://doi.org/10.1056/NEJMra1005073CrossRefPubMed

Duh EJ, Sun JK, Stitt AW (2017) Diabetic retinopathy: current understanding, mechanisms, and treatment strategies. JCI Insight 2(14). https://doi.org/10.1172/jci.insight.93751

Diabetes C, Complications Trial Research G, Nathan DM, Genuth S, Lachin J, Cleary P, Crofford O, Davis M, Rand L, Siebert C (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329(14):977–986. https://doi.org/10.1056/NEJM199309303291401CrossRef

Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group (1998). Lancet 352 (9131):854–865

Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen SJ, Dekker JM, Fletcher A, Grauslund J, Haffner S, Hamman RF, Ikram MK, Kayama T, Klein BE, Klein R, Krishnaiah S, Mayurasakorn K, O'Hare JP, Orchard TJ, Porta M, Rema M, Roy MS, Sharma T, Shaw J, Taylor H, Tielsch JM, Varma R, Wang JJ, Wang N, West S, Xu L, Yasuda M, Zhang X, Mitchell P, Wong TY, Meta-Analysis for Eye Disease Study G (2012) Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35 (3):556–564. doi:https://doi.org/10.2337/dc11-1909

Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group (1991). Ophthalmology 98 (5 Suppl):786–806

Kaines A, Oliver S, Reddy S, Schwartz SD (2009) Ultrawide angle angiography for the detection and management of diabetic retinopathy. Int Ophthalmol Clin 49(2):53–59. https://doi.org/10.1097/IIO.0b013e31819fd471CrossRefPubMed

Silva PS, Cavallerano JD, Sun JK, Soliman AZ, Aiello LM, Aiello LP (2013) Peripheral lesions identified by mydriatic ultrawide field imaging: distribution and potential impact on diabetic retinopathy severity. Ophthalmology 120(12):2587–2595. https://doi.org/10.1016/j.ophtha.2013.05.004CrossRefPubMed

Baxter SL, Ashir A, Nguyen BJ, Nudleman E (2019) Quantification of retinal nonperfusion associated with posterior segment neovascularization in diabetic retinopathy using ultra-Widefield fluorescein angiography. Ophthalmic Surg Lasers Imaging Retina 50(2):86–92. https://doi.org/10.3928/23258160-20190129-04CrossRefPubMedPubMedCentral

10.

Sim DA, Keane PA, Rajendram R, Karampelas M, Selvam S, Powner MB, Fruttiger M, Tufail A, Egan CA (2014) Patterns of peripheral retinal and central macula ischemia in diabetic retinopathy as evaluated by ultra-widefield fluorescein angiography. Am J Ophthalmol 158(1):144–153 e141. https://doi.org/10.1016/j.ajo.2014.03.009CrossRefPubMed

11.

Nicholson L, Ramu J, Chan EW, Bainbridge JW, Hykin PG, Talks SJ, Sivaprasad S (2019) Retinal nonperfusion characteristics on ultra-widefield angiography in eyes with severe nonproliferative diabetic retinopathy and proliferative diabetic retinopathy. JAMA Ophthalmol 137(6):626–631. https://doi.org/10.1001/jamaophthalmol.2019.0440CrossRefPubMedPubMedCentral

12.

Sim DA, Keane PA, Zarranz-Ventura J, Fung S, Powner MB, Platteau E, Bunce CV, Fruttiger M, Patel PJ, Tufail A, Egan CA (2013) The effects of macular ischemia on visual acuity in diabetic retinopathy. Invest Ophthalmol Vis Sci 54(3):2353–2360. https://doi.org/10.1167/iovs.12-11103CrossRefPubMed

13.

Fang M, Fan W, Shi Y, Ip MS, Wykoff CC, Wang K, Falavarjani KG, Brown DM, van Hemert J, Sadda SR (2019) Classification of regions of nonperfusion on ultra-widefield fluorescein angiography in patients with diabetic macular edema. Am J Ophthalmol. https://doi.org/10.1016/j.ajo.2019.03.030

14.

Wessel MM, Nair N, Aaker GD, Ehrlich JR, D'Amico DJ, Kiss S (2012) Peripheral retinal ischaemia, as evaluated by ultra-widefield fluorescein angiography, is associated with diabetic macular oedema. Br J Ophthalmol 96(5):694–698. https://doi.org/10.1136/bjophthalmol-2011-300774CrossRefPubMedPubMedCentral

15.

Holladay JT (2004) Visual acuity measurements. J Cataract Refract Surg 30(2):287–290. https://doi.org/10.1016/j.jcrs.2004.01.014CrossRefPubMed

16.

Sun JK, Lin MM, Lammer J, Prager S, Sarangi R, Silva PS, Aiello LP (2014) Disorganization of the retinal inner layers as a predictor of visual acuity in eyes with center-involved diabetic macular edema. JAMA Ophthalmol 132(11):1309–1316. https://doi.org/10.1001/jamaophthalmol.2014.2350CrossRefPubMed

17.

Quigley M, Cohen S (1999) A new pressure attenuation index to evaluate retinal circulation. A link to protective factors in diabetic retinopathy. Arch Ophthalmol 117(1):84–89. https://doi.org/10.1001/archopht.117.1.84CrossRefPubMed

18.

Wang W, Lo ACY (2018) Diabetic retinopathy: pathophysiology and treatments. Int J Mol Sci 19(6). https://doi.org/10.3390/ijms19061816

19.

Adamis AP, Miller JW, Bernal MT, D'Amico DJ, Folkman J, Yeo TK, Yeo KT (1994) Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol 118(4):445–450. https://doi.org/10.1016/s0002-9394(14)75794-0CrossRefPubMed

20.

Virgili G, Parravano M, Evans JR, Gordon I, Lucenteforte E (2018) Anti-vascular endothelial growth factor for diabetic macular oedema: a network meta-analysis. Cochrane Database Syst Rev 10:CD007419. https://doi.org/10.1002/14651858.CD007419.pub6CrossRefPubMed

21.

Nussenblatt RB, Kaufman SC, Palestine AG, Davis MD, Ferris FL 3rd (1987) Macular thickening and visual acuity. Measurement in patients with cystoid macular edema. Ophthalmology 94(9):1134–1139. https://doi.org/10.1016/s0161-6420(87)33314-7CrossRefPubMed

22.

Rangaraju L, Jiang X, McAnany JJ, Tan MR, Wanek J, Blair NP, Lim JI, Shahidi M (2018) Association between visual acuity and retinal layer metrics in diabetics with and without macular edema. J Ophthalmol 2018:1089043. https://doi.org/10.1155/2018/1089043CrossRefPubMedPubMedCentral

23.

Radwan SH, Soliman AZ, Tokarev J, Zhang L, van Kuijk FJ, Koozekanani DD (2015) Association of disorganization of retinal inner layers with vision after resolution of center-involved diabetic macular edema. JAMA Ophthalmol 133(7):820–825. https://doi.org/10.1001/jamaophthalmol.2015.0972CrossRefPubMed

24.

Balaratnasingam C, Inoue M, Ahn S, McCann J, Dhrami-Gavazi E, Yannuzzi LA, Freund KB (2016) Visual acuity is correlated with the area of the Foveal avascular zone in diabetic retinopathy and retinal vein occlusion. Ophthalmology 123(11):2352–2367. https://doi.org/10.1016/j.ophtha.2016.07.008CrossRefPubMed

25.

Das R, Spence G, Hogg RE, Stevenson M, Chakravarthy U (2018) Disorganization of inner retina and outer retinal morphology in diabetic macular edema. JAMA Ophthalmol 136(2):202–208. https://doi.org/10.1001/jamaophthalmol.2017.6256CrossRefPubMedPubMedCentral

26.

Nicholson L, Ramu J, Triantafyllopoulou I, Patrao NV, Comyn O, Hykin P, Sivaprasad S (2015) Diagnostic accuracy of disorganization of the retinal inner layers in detecting macular capillary non-perfusion in diabetic retinopathy. Clin Exp Ophthalmol 43(8):735–741. https://doi.org/10.1111/ceo.12557CrossRefPubMed

27.

Sawada O, Ichiyama Y, Obata S, Ito Y, Kakinoki M, Sawada T, Saishin Y, Ohji M (2018) 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 256(7):1275–1280. https://doi.org/10.1007/s00417-018-3992-yCrossRefPubMed

28.

Couturier A, Rey PA, Erginay A, Lavia C, Bonnin S, Dupas B, Gaudric A, Tadayoni R (2019) Widefield OCT-angiography and fluorescein angiography assessments of nonperfusion in diabetic retinopathy and edema treated with anti-vascular endothelial growth factor. Ophthalmology 126(12):1685–1694. https://doi.org/10.1016/j.ophtha.2019.06.022CrossRefPubMed

Titel: The prognostic value of peripheral retinal nonperfusion in diabetic retinopathy using ultra-widefield fluorescein angiography
verfasst von: Fares Antaki
Razek Georges Coussa
Mikel Mikhail
Cyril Archambault
David E. Lederer
Publikationsdatum: 16.07.2020
Verlag: Springer Berlin Heidelberg
Erschienen in: Graefe's Archive for Clinical and Experimental Ophthalmology / Ausgabe 12/2020
Print ISSN: 0721-832X
Elektronische ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-020-04847-w

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The prognostic value of peripheral retinal nonperfusion in diabetic retinopathy using ultra-widefield fluorescein angiography

Abstract

Purpose

Methods

Results

Conclusions

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