Correlation study on the changes of retinal artery angle in idiopathic epiretinal membrane and its correlation with visual acuity and optical coherence tomography classification_Chinese Journal of Ocular Fundus Diseases

Authors：

Xiang Ziyi ¹ , Mao Jianbo ¹ , Wang Qinmei ¹ , Zhang Zhengxi ¹ , Chen Yijing ¹ , Zhang Shian ¹ , Zhang Xiaoya ¹ , Zhong Jing ¹ ,  Shen Lijun ²

1. The Affiliated Eye Hospital of Wenzhou Medical University at Hangzhou, Hangzhou 310020, China;
2. Department of Ophthalmology, Zhejiang Provincial People's Hospital, Hangzhou 310020, China;

Corresponding author：

Shen Lijun, Email: slj@mail.eye.ac.cn

Keywords：

Idiopathic epiretinal membrane; Retinal artery angle; Fundus photography; Optical coherence tomography; Ectopic inner foveal layer

DOI：

10.3760/cma.j.cn511434-20231103-00443

Video：

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Objective To observe the change of retinal artery angle in eyes with idiopathic epiretinal membrane (ERM) and to analyze the relationship between retinal artery angle, ERM classification based on optical coherence tomography (OCT), and visual acuity. Methods A retrospective cross-sectional clinical study. A total of 187 eyes in 187 patients diagnosed with monocular idiopathic ERM (IERM group) in Department of Ophthalmology of Zhejiang Provincial People's Hospital and the Affiliated Eye Hospital of Wenzhou Medical University at Hangzhou from November 2018 to January 2023 were included in the study. The contralateral healthy eyes were included as the control group. All patients underwent best corrected visual acuity (BCVA), fundus photography, spectral-domain OCT, OCT angiography (OCTA) and axial length (AL) measurement. BCVA examination was performed using the standard logarithmic visual acuity chart, which was converted to the logarithm of the minimum angle of resolution (logMAR) visual acuity. The foveal avascular zone (FAZ) area was measured by OCTA. The central macular thickness (CMT) was measured by spectral domain OCTaccording to the grading criteria of ectopic inner foveal layer (EIFL) was divided into stages 1 to 4 with 42, 45, 62, and 38 eyes, and the IERM group was subdivided into stage 1, stage 2, stage 3, and stage 4 groups accordingly. Image J was used to measure the retinal artery angle and the 1/2 retinal artery angle on fundus images. Multiple linear regression analysis was used to analyze the correlation between BCVA and artery angle, 1/2 artery Angle, CMT, FAZ area and AL. Results Compared with the control group, eyes in IERM group had worse BCVA (t=9.727), thicker CMT (t=12.452), smaller FAZ area (t=－14.329), smaller artery angle (t=－9.165) and smaller 1/2 artery angle (t=－9.549). The differences were statistically significant (P＜0.001). With the increase of IERM stage, the artery angle and 1/2 artery angle decreased significantly (F=21.763, 12.515; P＜0.001). There was no significant difference in artery angle and 1/2 artery angle between stage 1 group and stage 2 group, and 1/2 arterial angle between stage 2 group and stage 3 group (P＞0.05). There were significant differences in artery angle and 1/2 artery angle between the other groups (P＜0.05). There were significant differences in CMT and logMAR BCVA among different classification subgroups in IERM groups (P＜0.05). There was no significant difference in FAZ area between grade 3 group and grade 4 group (P＞0.05). There were significant differences in FAZ area between the other groups (P＜0.05). Correlation analysis showed that decreased artery angle (P=0.013) and increased CMT (P＜0.001) were associated with decreased BCVA. Conclusions Compared with healthy eyes, the artery angle decreases significantly with the increase of ERM stage. Decreased retinal artery angle is associated with decreased visual acuity in IERM eyes.

Citation： Xiang Ziyi, Mao Jianbo, Wang Qinmei, Zhang Zhengxi, Chen Yijing, Zhang Shian, Zhang Xiaoya, Zhong Jing, Shen Lijun. Correlation study on the changes of retinal artery angle in idiopathic epiretinal membrane and its correlation with visual acuity and optical coherence tomography classification. Chinese Journal of Ocular Fundus Diseases, 2024, 40(3): 190-195. doi: 10.3760/cma.j.cn511434-20231103-00443 Copy

1.	Ng CH, Cheung N, Wang JJ, et al. Prevalence and risk factors for epiretinal membranes in a multi-ethnic United States population[J]. Ophthalmology, 2011, 118(4): 694-699. DOI: 10.1016/j.ophtha.2010.08.009.
2.	Cheung N, Tan SP, Lee SY, et al. Prevalence and risk factors for epiretinal membrane: the Singapore epidemiology of eye disease study[J]. Br J Ophthalmol, 2017, 101(3): 371-376. DOI: 10.1136/bjophthalmol-2016-308563.
3.	You Q, Xu L, Jonas JB. Prevalence and associations of epiretinal membranes in adult Chinese: the Beijing eye study[J]. Eye (Lond), 2008, 22(7): 874-879. DOI: 10.1038/sj.eye.6702786.
4.	Joe SG, Lee KS, Lee JY, et al. Inner retinal layer thickness is the major determinant of visual acuity in patients with idiopathic epiretinal membrane[J/OL]. Acta Ophthalmol, 2013, 91(3): e242-e243[2012-12-31]. https://pubmed.ncbi.nlm.nih.gov/23280145/. DOI: 10.1111/aos.12017.
5.	Govetto A, Virgili G, Rodriguez FJ, et al. Functional and anatomical significance of the ectopic inner foveal layers in eyes with idiopathic epiretinal membranes: surgical results at 12 months[J]. Retina, 2019, 39(2): 347-357. DOI: 10.1097/IAE.0000000000001940.
6.	Sakai D, Takagi S, Hirami Y, et al. Correlation between tangential distortion of the outer retinal layer and metamorphopsia in patients with epiretinal membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(7): 1751-1758. DOI: 10.1007/s00417-021-05077-4.
7.	Yang X, Yu Y, Wu X, et al. Changes in foveal photoreceptor integrity after idiopathic epiretinal membrane surgery and its relationship with visual outcomes[J]. Graefe's Arch Clin Exp Ophthalmol, 2023, 261(4): 925-933. DOI: 10.1007/s00417-022-05886-1.
8.	Govetto A, Lalane RA 3rd, Sarraf D, et al. Insights into epiretinal membranes: presence of ectopic inner foveal layers and a new optical coherence tomography staging scheme[J]. Am J Ophthalmol, 2017, 175: 99-113. DOI: 10.1016/j.ajo.2016.12.006.
9.	Kofod M, la Cour M. Quantification of retinal tangential movement in epiretinal membranes[J]. Ophthalmology, 2012, 119(9): 1886-1891. DOI: 10.1016/j.ophtha.2012.03.022.
10.	Weinberger D, Stiebel-Kalish H, Priel E, et al. Digital red-free photography for the evaluation of retinal blood vessel displacement in epiretinal membrane[J]. Ophthalmology, 1999, 106(7): 1380-1383. DOI: 10.1016/S0161-6420(99)10164-7.
11.	Arimura E, Matsumoto C, Okuyama S, et al. Retinal contraction and metamorphopsia scores in eyes with idiopathic epiretinal membrane[J]. Invest Ophthalmol Vis Sci, 2005, 46(8): 2961-2966. DOI: 10.1167/iovs.04-1104.
12.	Dell'omo R, Cifariello F, Dell'omo E, et al. Influence of retinal vessel printings on metamorphopsia and retinal architectural abnormalities in eyes with idiopathic macular epiretinal membrane[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7803-7811. DOI: 10.1167/iovs.13-12817.
13.	Nagura K, Inoue T, Zhou HP, et al. Association between retinal artery angle and visual function in eyes with idiopathic epiretinal membrane[J]. Transl Vis Sci Technol, 2021, 10(9): 35. DOI: 10.1167/tvst.10.9.35.
14.	Hosoda Y, Ooto S, Hangai M, et al. Foveal photoreceptor deformation as a significant predictor of postoperative visual outcome in idiopathic epiretinal membrane surgery[J]. Invest Ophthalmol Vis Sci, 2015, 56(11): 6387-6393. DOI: 10.1167/iovs.15-16679.
15.	Yang HS, Kim JT, Joe SG, et al. Postoperative restoration of foveal inner retinal configuration in patients with epiretinal membrane and abnormally thick inner retina[J]. Retina, 2015, 35(1): 111-119. DOI: 10.1097/IAE.0000000000000276.
16.	Kim BH, Kim DI, Bae KW, et al. Influence of postoperative ectopic inner foveal layer on visual function after removal of idiopathic epiretinal membrane[J/OL]. PLoS One, 2021, 16(11): e0259388[2021-11-04]. https://pubmed.ncbi.nlm.nih.gov/34735519/. DOI: 10.1371/journal.pone.0259388.
17.	Alkabes M, Fogagnolo P, Vujosevic S, et al. Correlation between new OCT parameters and metamorphopsia in advanced stages of epiretinal membranes[J]. Acta Ophthalmol, 2020, 98(8): 780-786. DOI: 10.1111/aos.14336.
18.	Coppola M, Brambati M, Cicinelli MV, et al. The visual outcomes of idiopathic epiretinal membrane removal in eyes with ectopic inner foveal layers and preserved macular segmentation[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(8): 2193-2201. DOI: 10.1007/s00417-021-05102-6.
19.	González-Saldivar G, Berger A, Wong D, et al. Ectopic inner foveal layer classification scheme predicts visual outcomes after epiretinal membrane surgery[J]. Retina, 2020, 40(4): 710-717. DOI: 10.1097/IAE.0000000000002486.
20.	姚一民, 柴茜楠, 魏玉华, 等. 特发性黄斑前膜异常中心凹内层的临床意义评估[J]. 中华眼底病杂志, 2021, 37(5): 359-364. DOI: 10.3760/cma.j.cn511434-20201222-00628.Yao YM, Chai QN, Wei YH, et al. Evaluation of the clinical significance of the ectopic inner foveal layers of idiopathic epiretinal membranes[J]. Chin J Ocul Fundus Dis, 2021, 37(5): 359-364. DOI: 10.3760/cma.j.cn511434-20201222-00628.
21.	Mastropasqua R, D'Aloisio R, Viggiano P, et al. Early retinal flow changes after vitreoretinal surgery in idiopathic epiretinal membrane using swept source optical coherence tomography angiography[J]. J Clin Med, 2019, 8(12): 2067. DOI: 10.3390/jcm8122067.
22.	Koo HC, Rhim WI, Lee EK. Morphologic and functional association of retinal layers beneath the epiretinal membrane with spectral-domain optical coherence tomography in eyes without photoreceptor abnormality[J]. Graefe's Arch Clin Exp Ophthalmol, 2012, 250(4): 491-498. DOI: 10.1007/s00417-011-1848-9.
23.	Song SJ, Lee MY, Smiddy WE. Ganglion cell layer thickness and visual improvement after epiretinal membrane surgery[J]. Retina, 2016, 36(2): 305-310. DOI: 10.1097/IAE.0000000000000705.

1. Ng CH, Cheung N, Wang JJ, et al. Prevalence and risk factors for epiretinal membranes in a multi-ethnic United States population[J]. Ophthalmology, 2011, 118(4): 694-699. DOI: 10.1016/j.ophtha.2010.08.009.
2. Cheung N, Tan SP, Lee SY, et al. Prevalence and risk factors for epiretinal membrane: the Singapore epidemiology of eye disease study[J]. Br J Ophthalmol, 2017, 101(3): 371-376. DOI: 10.1136/bjophthalmol-2016-308563.
3. You Q, Xu L, Jonas JB. Prevalence and associations of epiretinal membranes in adult Chinese: the Beijing eye study[J]. Eye (Lond), 2008, 22(7): 874-879. DOI: 10.1038/sj.eye.6702786.
4. Joe SG, Lee KS, Lee JY, et al. Inner retinal layer thickness is the major determinant of visual acuity in patients with idiopathic epiretinal membrane[J/OL]. Acta Ophthalmol, 2013, 91(3): e242-e243[2012-12-31]. https://pubmed.ncbi.nlm.nih.gov/23280145/. DOI: 10.1111/aos.12017.
5. Govetto A, Virgili G, Rodriguez FJ, et al. Functional and anatomical significance of the ectopic inner foveal layers in eyes with idiopathic epiretinal membranes: surgical results at 12 months[J]. Retina, 2019, 39(2): 347-357. DOI: 10.1097/IAE.0000000000001940.
6. Sakai D, Takagi S, Hirami Y, et al. Correlation between tangential distortion of the outer retinal layer and metamorphopsia in patients with epiretinal membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(7): 1751-1758. DOI: 10.1007/s00417-021-05077-4.
7. Yang X, Yu Y, Wu X, et al. Changes in foveal photoreceptor integrity after idiopathic epiretinal membrane surgery and its relationship with visual outcomes[J]. Graefe's Arch Clin Exp Ophthalmol, 2023, 261(4): 925-933. DOI: 10.1007/s00417-022-05886-1.
8. Govetto A, Lalane RA 3rd, Sarraf D, et al. Insights into epiretinal membranes: presence of ectopic inner foveal layers and a new optical coherence tomography staging scheme[J]. Am J Ophthalmol, 2017, 175: 99-113. DOI: 10.1016/j.ajo.2016.12.006.
9. Kofod M, la Cour M. Quantification of retinal tangential movement in epiretinal membranes[J]. Ophthalmology, 2012, 119(9): 1886-1891. DOI: 10.1016/j.ophtha.2012.03.022.
10. Weinberger D, Stiebel-Kalish H, Priel E, et al. Digital red-free photography for the evaluation of retinal blood vessel displacement in epiretinal membrane[J]. Ophthalmology, 1999, 106(7): 1380-1383. DOI: 10.1016/S0161-6420(99)10164-7.
11. Arimura E, Matsumoto C, Okuyama S, et al. Retinal contraction and metamorphopsia scores in eyes with idiopathic epiretinal membrane[J]. Invest Ophthalmol Vis Sci, 2005, 46(8): 2961-2966. DOI: 10.1167/iovs.04-1104.
12. Dell'omo R, Cifariello F, Dell'omo E, et al. Influence of retinal vessel printings on metamorphopsia and retinal architectural abnormalities in eyes with idiopathic macular epiretinal membrane[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7803-7811. DOI: 10.1167/iovs.13-12817.
13. Nagura K, Inoue T, Zhou HP, et al. Association between retinal artery angle and visual function in eyes with idiopathic epiretinal membrane[J]. Transl Vis Sci Technol, 2021, 10(9): 35. DOI: 10.1167/tvst.10.9.35.
14. Hosoda Y, Ooto S, Hangai M, et al. Foveal photoreceptor deformation as a significant predictor of postoperative visual outcome in idiopathic epiretinal membrane surgery[J]. Invest Ophthalmol Vis Sci, 2015, 56(11): 6387-6393. DOI: 10.1167/iovs.15-16679.
15. Yang HS, Kim JT, Joe SG, et al. Postoperative restoration of foveal inner retinal configuration in patients with epiretinal membrane and abnormally thick inner retina[J]. Retina, 2015, 35(1): 111-119. DOI: 10.1097/IAE.0000000000000276.
16. Kim BH, Kim DI, Bae KW, et al. Influence of postoperative ectopic inner foveal layer on visual function after removal of idiopathic epiretinal membrane[J/OL]. PLoS One, 2021, 16(11): e0259388[2021-11-04]. https://pubmed.ncbi.nlm.nih.gov/34735519/. DOI: 10.1371/journal.pone.0259388.
17. Alkabes M, Fogagnolo P, Vujosevic S, et al. Correlation between new OCT parameters and metamorphopsia in advanced stages of epiretinal membranes[J]. Acta Ophthalmol, 2020, 98(8): 780-786. DOI: 10.1111/aos.14336.
18. Coppola M, Brambati M, Cicinelli MV, et al. The visual outcomes of idiopathic epiretinal membrane removal in eyes with ectopic inner foveal layers and preserved macular segmentation[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(8): 2193-2201. DOI: 10.1007/s00417-021-05102-6.
19. González-Saldivar G, Berger A, Wong D, et al. Ectopic inner foveal layer classification scheme predicts visual outcomes after epiretinal membrane surgery[J]. Retina, 2020, 40(4): 710-717. DOI: 10.1097/IAE.0000000000002486.
20. 姚一民, 柴茜楠, 魏玉华, 等. 特发性黄斑前膜异常中心凹内层的临床意义评估[J]. 中华眼底病杂志, 2021, 37(5): 359-364. DOI: 10.3760/cma.j.cn511434-20201222-00628.Yao YM, Chai QN, Wei YH, et al. Evaluation of the clinical significance of the ectopic inner foveal layers of idiopathic epiretinal membranes[J]. Chin J Ocul Fundus Dis, 2021, 37(5): 359-364. DOI: 10.3760/cma.j.cn511434-20201222-00628.
21. Mastropasqua R, D'Aloisio R, Viggiano P, et al. Early retinal flow changes after vitreoretinal surgery in idiopathic epiretinal membrane using swept source optical coherence tomography angiography[J]. J Clin Med, 2019, 8(12): 2067. DOI: 10.3390/jcm8122067.
22. Koo HC, Rhim WI, Lee EK. Morphologic and functional association of retinal layers beneath the epiretinal membrane with spectral-domain optical coherence tomography in eyes without photoreceptor abnormality[J]. Graefe's Arch Clin Exp Ophthalmol, 2012, 250(4): 491-498. DOI: 10.1007/s00417-011-1848-9.
23. Song SJ, Lee MY, Smiddy WE. Ganglion cell layer thickness and visual improvement after epiretinal membrane surgery[J]. Retina, 2016, 36(2): 305-310. DOI: 10.1097/IAE.0000000000000705.

Chinese Journal of Ocular Fundus Diseases

Correlation study on the changes of retinal artery angle in idiopathic epiretinal membrane and its correlation with visual acuity and optical coherence tomography classification

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