The role of optical coherence tomography angiography in evaluating recurrent macular edema secondary to central retinal vein occlusion after intravitreal injection of ranibizumab_Chinese Journal of Ocular Fundus Diseases

Authors：

An Weiting , Yu Rongguo , Zhao Qi , Gong Xue , Chen Lu ,  Han Jindong

Tianjin Medical University Eye Hospital, School of Optometry & Eye Institute, Tianjin Branch of National Clinical Research Center for Ocular Disease, Tianjin Key Laboratory of Retinal Functions and Diseases, Tianjin 300384, China;
An Weiting and Yu Rongguo are contributed equally to the article;

Corresponding author：

Han Jindong, Email: djindonghan@126.com

Keywords：

Retinal vein occlusion; Macular edema; Recurrence; Tomography, optical coherence

DOI：

10.3760/cma.j.cn511434-20220407-00202

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Objective To observe the differences of macular microvascular structure between recurrent and non-recurrent macular edema (ME) secondary to central retinal vein occlusion (CRVO) after intravitreal injection of ranibizumab (IVR), and to preliminarily analyze the correlation between recurrence and ME. Methods A prospective clinical observational study. Forty-five patients (45 eyes) diagnosed as CRVO with ME were included in this study in Tianjin Medical University Eye Hospital from January 2020 to December 2021. There were 22 males (22 eyes) and 23 females (23 eyes). All cases were unilateral. The average age was 61.11±10.88 years old. All patients received IVR treatment once a month for 3 consecutive months. ME were regressive after the initial three treatments. The patients were divided into recurrent group (21 cases, 21 eyes) and non-recurrent group (24 cases, 24 eyes) based on ME recurrence at 6 months after ME resolution. All patients underwent best corrected visual acuity (BCVA), intraocular pressure, and optical coherence tomography angiography (OCTA). OCTA was used to scan the macula in the area of 3 mm×3 mm, and the vessel density (VD) of superficial capillary plexus (SCP), deep capillary plexus (DCP), fovea and parafovea before and after treatment was measured. Foveal retinal thickness, foveal avascular zone (FAZ) area, perimeter of FAZ (PERIM), avascular index of FAZ (AI), VD within 300 μm width of FAZ range (FD-300). Foveal VD included superficial and deep retinal VD (SFVD, DFVD); parafoveal VD included superficial and deep retinal VD (SPFVD, DPFVD). Taking the initial three treatments as the observation time point, the changes of the parameters of the two groups were compared. Comparison between the recurrent and non-recurrent group was performed by two independent sample t-tests. Receiver operating characteristic (ROC) curve analysis was used to measure the area under the curve (AUC) of VD for predicting the recurrence of ME. Results There were no significant differences in age (t=1.350), IOP (t=1.929), SFVD (t=－1.716), DFVD (t=－1.143), CRT (t=－1.207) and AI (t=1.387) between the recurrent and non-recurrent group (P＞0.05). There were significant differences in times of anti-VEGF therapy (t=5.912), BCVA (t=5.003), SVD (t=－4.617), SPFVD (t=－4.110), DVD (t=－5.503), DPFVD (t=－4.772), FAZ area (t=2.172), PERIM (t=2.606) and FD-300 (t=－3.501) between the recurrent and non-recurrent group (P＜0.05). ROC curve analysis showed that the AUC of DVD in predicting the recurrence of ME was highest, with 0.921, and the threshold was 37.65%. The sensitivity and specificity were 91.7% and 85.7%, respectively. Conclusions The SVD, SPFVD, DVD, DPFVD and FD-300 in the recurrence group are significantly lower than those in the non-recurrence group, while the FAZ area and PERIM are significantly higher than those in the non-recurrence group. DVD≤37.65% can be used as the best threshold for predicting the recurrence of ME.

Citation： An Weiting, Yu Rongguo, Zhao Qi, Gong Xue, Chen Lu, Han Jindong. The role of optical coherence tomography angiography in evaluating recurrent macular edema secondary to central retinal vein occlusion after intravitreal injection of ranibizumab. Chinese Journal of Ocular Fundus Diseases, 2022, 38(9): 744-749. doi: 10.3760/cma.j.cn511434-20220407-00202 Copy

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2.	Higashiyama T, Sawada O, Kakinoki M, et al. Prospective comparisons of intravitreal injections of triamcinolone acetonide and bevacizumab for macular oedema due to branch retinal vein occlusion[J]. Acta Ophthalmol, 2013, 91(4): 318-324. DOI: 10.1111/j.1755-3768.2011.02298.x.
3.	Yoo JH, Ahn J, Oh J, et al. Risk factors of recurrence of macular oedema associated with branch retinal vein occlusion after intravitreal bevacizumab injection[J]. Br J Ophthalmol, 2017, 101(10): 1334-1339. DOI: 10.1136/bjophthalmol-2016-309749.
4.	Tilgner E, Dalcegio Favretto M, Tuisl M, et al. Macular cystic changes as predictive factor for the recurrence of macular oedema in branch retinal vein occlusion[J/OL]. Acta Ophthalmol, 2017, 95(7): e592-e596[2017-11-01]. https://pubmed.ncbi.nlm.nih.gov/28266152/. DOI: 10.1111/aos.13396.
5.	Suzuki M, Nagai N, Minami S, et al. Predicting recurrences of macular edema due to branch retinal vein occlusion during anti-vascular endothelial growth factor therapy[J]. Graefe's Arch Clin Exp Ophthalmol, 2020, 258(1): 49-56. DOI: 10.1007/s00417-019-04495-9.
6.	Hayreh SS. Occlusion of the central retinal vessels[J]. Br J Ophthalmol, 1965, 49(12): 626-645. DOI:10.1136/bjo.49.12.626.
7.	Rosenfeld PJ, Durbin MK, Roisman L, et al. ZEISS Angioplex™ spectral domain optical coherence tomography angiography: technical aspects[J]. Dev Ophthalmol, 2016, 56: 18-29. DOI: 10.1159/000442773.
8.	Coscas F, Glacet-Bernard A, Miere A, et al. Optical coherence tomography angiography in retinal vein occlusion: evaluation of superficial and deep capillary plexa[J]. Am J Ophthalmol, 2016, 161: 160-171. DOI: 10.1016/j.ajo.2015.10.008.
9.	Kim KM, Lee MW, Lim HB, et al. Repeatability of measuring the vessel density in patients with retinal vein occlusion: an optical coherence tomography angiography study[J/OL]. PLoS One, 2020, 15(6): e0234933[2020-06-25]. https://pubmed.ncbi.nlm.nih.gov/32584907/. DOI: 10.1371/journal.pone.0234933.
10.	Coscas F, Sellam A, Glacet-Bernard A, et al. Normative data for vascular density in superficial and deep capillary plexuses of healthy adults assessed by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 211-223. DOI: 10.1167/iovs.15-18793.
11.	Adhi M, Filho MA, Louzada RN, et al. Retinal capillary network and foveal avascular zone in eyes with vein occlusion and fellow eyes analyzed with optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 486-494. DOI: 10.1167/iovs.15-18907.
12.	邢怡桥, 刘芳, 李拓. 缺血型与非缺血型视网膜分支静脉阻塞患者黄斑区血流对比[J]. 眼科新进展, 2019, 39(11): 1036-1039. DOI: 10.13389/j.cnki.rao.2019.0237.Xing YQ, Lu F, Li T. Observation of the macular vessels in ischemic and non-ischemic branch retinal vein occlusion using optical coherence tomography angiography[J]. Rec Adv Ophthalmol, 2019, 39(11): 1036-1039. DOI: 10.13389/j.cnki.rao.2019.0237.
13.	Seknazi D, Coscas F, Sellam A, et al. Optical coherence tomography angiography in retinal vein occlusion: correlations between macular vascular density, visual acuity, and peripheral nonperfusion area on fluorescein angiography[J]. Retina, 2018, 38(8): 1562-1570. DOI: 10.1097/IAE.0000000000001737.
14.	安伟婷, 赵琦, 于荣国, 等. 光相干断层扫描血管成像鉴别缺血型与非缺血型视网膜分支静脉阻塞[J]. 中华眼底病杂志, 2021, 37(12): 926-931. DOI: 10.3760/cma.j.cn511434-20210510-00241.An WT, Zhao Q, Yu RG, et al. The role of optical coherence tomography angiography to distinguish ischemic and non-ischemic branch retinal vein occlusion[J]. Chin J Ocul Fundus Dis, 2021, 37(12): 926-931. DOI: 10.3760/cma.j.cn511434-20210510-00241.
15.	Moussa M, Leila M, Bessa AS, et al. Grading of macular perfusion in retinal vein occlusion using en-face swept-source optical coherence tomography angiography: a retrospective observational case series[J]. BMC Ophthalmol, 2019, 19(1): 127. DOI: 10.1186/s12886-019-1134-x.

1. Finkelstein D. Ischemic macular edema. Recognition and favorable natural history in branch vein occlusion[J]. Arch Ophthalmol, 1992, 110(10): 1427-1434. DOI: 10.1001/archopht.1992.01080220089028.
2. Higashiyama T, Sawada O, Kakinoki M, et al. Prospective comparisons of intravitreal injections of triamcinolone acetonide and bevacizumab for macular oedema due to branch retinal vein occlusion[J]. Acta Ophthalmol, 2013, 91(4): 318-324. DOI: 10.1111/j.1755-3768.2011.02298.x.
3. Yoo JH, Ahn J, Oh J, et al. Risk factors of recurrence of macular oedema associated with branch retinal vein occlusion after intravitreal bevacizumab injection[J]. Br J Ophthalmol, 2017, 101(10): 1334-1339. DOI: 10.1136/bjophthalmol-2016-309749.
4. Tilgner E, Dalcegio Favretto M, Tuisl M, et al. Macular cystic changes as predictive factor for the recurrence of macular oedema in branch retinal vein occlusion[J/OL]. Acta Ophthalmol, 2017, 95(7): e592-e596[2017-11-01]. https://pubmed.ncbi.nlm.nih.gov/28266152/. DOI: 10.1111/aos.13396.
5. Suzuki M, Nagai N, Minami S, et al. Predicting recurrences of macular edema due to branch retinal vein occlusion during anti-vascular endothelial growth factor therapy[J]. Graefe's Arch Clin Exp Ophthalmol, 2020, 258(1): 49-56. DOI: 10.1007/s00417-019-04495-9.
6. Hayreh SS. Occlusion of the central retinal vessels[J]. Br J Ophthalmol, 1965, 49(12): 626-645. DOI:10.1136/bjo.49.12.626.
7. Rosenfeld PJ, Durbin MK, Roisman L, et al. ZEISS Angioplex™ spectral domain optical coherence tomography angiography: technical aspects[J]. Dev Ophthalmol, 2016, 56: 18-29. DOI: 10.1159/000442773.
8. Coscas F, Glacet-Bernard A, Miere A, et al. Optical coherence tomography angiography in retinal vein occlusion: evaluation of superficial and deep capillary plexa[J]. Am J Ophthalmol, 2016, 161: 160-171. DOI: 10.1016/j.ajo.2015.10.008.
9. Kim KM, Lee MW, Lim HB, et al. Repeatability of measuring the vessel density in patients with retinal vein occlusion: an optical coherence tomography angiography study[J/OL]. PLoS One, 2020, 15(6): e0234933[2020-06-25]. https://pubmed.ncbi.nlm.nih.gov/32584907/. DOI: 10.1371/journal.pone.0234933.
10. Coscas F, Sellam A, Glacet-Bernard A, et al. Normative data for vascular density in superficial and deep capillary plexuses of healthy adults assessed by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 211-223. DOI: 10.1167/iovs.15-18793.
11. Adhi M, Filho MA, Louzada RN, et al. Retinal capillary network and foveal avascular zone in eyes with vein occlusion and fellow eyes analyzed with optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 486-494. DOI: 10.1167/iovs.15-18907.
12. 邢怡桥, 刘芳, 李拓. 缺血型与非缺血型视网膜分支静脉阻塞患者黄斑区血流对比[J]. 眼科新进展, 2019, 39(11): 1036-1039. DOI: 10.13389/j.cnki.rao.2019.0237.Xing YQ, Lu F, Li T. Observation of the macular vessels in ischemic and non-ischemic branch retinal vein occlusion using optical coherence tomography angiography[J]. Rec Adv Ophthalmol, 2019, 39(11): 1036-1039. DOI: 10.13389/j.cnki.rao.2019.0237.
13. Seknazi D, Coscas F, Sellam A, et al. Optical coherence tomography angiography in retinal vein occlusion: correlations between macular vascular density, visual acuity, and peripheral nonperfusion area on fluorescein angiography[J]. Retina, 2018, 38(8): 1562-1570. DOI: 10.1097/IAE.0000000000001737.
14. 安伟婷, 赵琦, 于荣国, 等. 光相干断层扫描血管成像鉴别缺血型与非缺血型视网膜分支静脉阻塞[J]. 中华眼底病杂志, 2021, 37(12): 926-931. DOI: 10.3760/cma.j.cn511434-20210510-00241.An WT, Zhao Q, Yu RG, et al. The role of optical coherence tomography angiography to distinguish ischemic and non-ischemic branch retinal vein occlusion[J]. Chin J Ocul Fundus Dis, 2021, 37(12): 926-931. DOI: 10.3760/cma.j.cn511434-20210510-00241.
15. Moussa M, Leila M, Bessa AS, et al. Grading of macular perfusion in retinal vein occlusion using en-face swept-source optical coherence tomography angiography: a retrospective observational case series[J]. BMC Ophthalmol, 2019, 19(1): 127. DOI: 10.1186/s12886-019-1134-x.

Chinese Journal of Ocular Fundus Diseases

The role of optical coherence tomography angiography in evaluating recurrent macular edema secondary to central retinal vein occlusion after intravitreal injection of ranibizumab

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