Clinical observation of microcystic macular edema before and after surgery for idiopathic epiretinal membrane_Chinese Journal of Ocular Fundus Diseases

Authors：

Lyu Zhe , Cen Jiner , Lu Yang , Chen Yiqi , Mao Jianbo , Tao Jiwei , Zhang Yun ,  Shen Lijun

Eye Hospital of Wenzhou Medical University at Hangzhou, Hangzhou 310020, China;

Corresponding author：

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

Keywords：

Epiretinal Membrane; Vitrectomy; Macular edema; Tomography, optical coherence

DOI：

10.3760/cma.j.cn511434-20220425-00251

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Objective To observe the incidence and risk factors of microcystic macular edema (MME) in patients with idiopathic macular epiretinal membrane (IMEM) preoperatively and postoperatively. Methods A retrospective case series study. From January 2017 to May 2021, 72 eyes of 72 patients with IMEM in Eye Hospital of Wenzhou Medical University at Hangzhou were included. There were 18 male and 54 female. Average age was 64.8±7.8 years. Eyes were all monocular. All patients received the examination of best corrected visual acuity (BCVA) by standard logarithmic visual acuity chart, which was represented logarithmic of minimum angle of resolution (logMAR). Optical coherence tomography was used to measure central macular thickness (CMT). MME was defined as small, vertically bounded cystic space located outside the fovea in the inner layer of the retina. According to the presence or absence of MME before surgery, the affected eyes were divided into two groups: non-MME group (35 eyes) and MME group (37 eyes). The difference of logMAR BCVA and CMT was statistically significant between Group A and B (t=3.117, 2.589; P=0.003, 0.012). All patients with IMEM were treated with 23G three-channels pars plana vitrectomy (PPV) with epiretinal membrane and inner limiting membrane (ILM) peeling. The two groups were further divided into four groups according to whether there was MME in the postoperative follow-up time. The group A1 was without MME before and after surgery, group A2 was without MME before surgery and with MME after surgery. The MME group was subdivided into the group with MME before surgery and without MME after surgery (group B1) and the group with MME before and after surgery (group B2). The mean follow-up time was 8.8±7.7 months. The same equipment and methods were used to exam the patients during the follow-up. Paired t test was used to compare the changes of MME, BCVA and CMT before and after surgery. The differences of CMT and BCVA among groups before and after surgery were compared by independent sample t test and one-way ANOVA. Logistic regression was used to analyze the influencing factors of MME before and after surgery, and multiple linear regression was used to analyze the influencing factors of postoperative BCVA. Results There were 35 eyes in the non-MME group, 18 eyes (51.43%, 18/35) in the A1 group and 17 eyes (48.57%, 17/35) in the A2 group, respectively. There were 37 eyes in MME group, 6 eyes (16.22%, 6/37) in group B1 and 31 eyes (83.78%, 31/37) in group B2, respectively. At last follow-up, the logMAR BCVA was 0.10±0.12, 0.25±0.17, 0.09±0.11, 0.30±0.26 in group A1, A2, B1, and B2, respectively. Compared with the logMAR BCVA before surgery, the differences were statistically significant (t=3.779, 4.253, 7.869, 6.668; P＜0.01). There was significant difference in logMAR BCVA among the four groups (F=4.460, P＜0.01). There was a significant difference in logMAR BCVA between group A1 and group A2 (t=－2.930, P=0.006). There was no significant difference between group B1 and group B2 (t=－1.921, P=0.063). The CMT of group A1, A2, B1 and B2 were 371.83±73.24, 431.24±83.13, 407.00±28.07 and 425.19±70.97 μm, respectively. Compared with those before operation, the differences were statistically significant (t=5.197, 2.465, 3.055, 6.078; P＜0.05). There was no significant difference in CMT among the four groups (F=2.597, P=0.059). Logistic regression analysis showed that pre-operation MME was correlated with pre-operation IMEM stage (β=1.494, P=0.004). New MME after surgery was correlated with age (β=0.153, P=0.013). Multiple linear regression analysis showed that postoperative visual acuity was significantly correlated with CMT before surgery and MME after surgery (β=0.001, 0.134; P=0.015, 0.019). Conclusions PPV combined with epiretinal membrane and ILM peeling surgery for IMEM can improve visual acuity and decrease CMT. MME regress or regenerate after surgery. Age is an independent predictor of the risk of newly formed MME after surgery.

Citation： Lyu Zhe, Cen Jiner, Lu Yang, Chen Yiqi, Mao Jianbo, Tao Jiwei, Zhang Yun, Shen Lijun. Clinical observation of microcystic macular edema before and after surgery for idiopathic epiretinal membrane. Chinese Journal of Ocular Fundus Diseases, 2022, 38(10): 805-810. doi: 10.3760/cma.j.cn511434-20220425-00251 Copy

1.	Burggraaff MC, Trieu J, de Vries-Knoppert WA, et al. The clinical spectrum of microcystic macular edema[J]. Invest Ophthalmol Vis Sci, 2014, 55(2): 952-961. DOI: 10.1167/iovs.13-12912.
2.	Balk LJ, Killestein J, Polman CH, et al. Microcystic macular oedema confirmed, but not specific for multiple sclerosis[J/OL]. Brain, 2012, 135(Pt 12): e226[2012-12-01]. https://pubmed.ncbi.nlm.nih.gov/23078994/. DOI: 10.1093/brain/aws216.
3.	Querques G, Coscas F, Forte R, et al. Cystoid macular degeneration in exudative age-related macular degeneration[J]. Am J Ophthalmol, 2011, 152(1): 100-107. DOI: 10.1016/j.ajo.2011.01.027.
4.	Saidha S, Sotirchos ES, Ibrahim MA, et al. Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study[J]. Lancet Neurol, 2012, 11(11): 963-972. DOI: 10.1016/S1474-4422(12)70213-2.
5.	Dolz-Marco R, Hoang QV, Gallego-Pinazo R, et al. Assessment of the significance of cystic changes after epiretinal membrane surgery with internal limiting membrane removal[J]. Retina, 2016, 36(4): 727-732. DOI: 10.1097/IAE.0000000000000780.
6.	Sigler EJ, Randolph JC, Charles S. Delayed onset inner nuclear layer cystic changes following internal limiting membrane removal for epimacular membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2013, 251(7): 1679-1685. DOI: 10.1007/s00417-012-2253-8.
7.	Hsieh MH, Chou YB, Huang YM, et al. Inner nuclear layer microcyst configuration, distribution, and visual prognosis in patients with epiretinal membrane after vitrectomy and membrane peeling[J/OL]. Sci Rep, 2019, 9(1): 11570[2019-08-09]. https://pubmed.ncbi.nlm.nih.gov/31399631/. DOI: 10.1038/s41598-019-48097-1.
8.	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.
9.	Gelfand JM, Nolan R, Schwartz DM, et al. Microcystic macular oedema in multiple sclerosis is associated with disease severity[J]. Brain, 2012, 135(Pt 6): 1786-1793. DOI: 10.1093/brain/aws098.
10.	Gelfand JM, Cree BA, Nolan R, et al. Microcystic inner nuclear layer abnormalities and neuromyelitis optica[J]. JAMA Neurol, 2013, 70(5): 629-633. DOI: 10.1001/jamaneurol.2013.1832.
11.	Sotirchos ES, Saidha S, Byraiah G, et al. In vivo identification of morphologic retinal abnormalities in neuromyelitis optica[J]. Neurology, 2013, 80(15): 1406-1414. DOI: 10.1212/WNL.0b013e31828c2f7a.
12.	Wolff B, Basdekidou C, Vasseur V, et al. Retinal inner nuclear layer microcystic changes in optic nerve atrophy: a novel spectral-domain OCT finding[J]. Retina, 2013, 33(10): 2133-2138. DOI: 10.1097/IAE.0b013e31828e68d0.
13.	Dysli M, Ebneter A, Menke MN, et al. Patients with epiretinal membranes display retrograde maculopathy after surgical peeling of the internal limiting membrane[J]. Retina, 2019, 39(11): 2132-2140. DOI: 10.1097/IAE.0000000000002266.
14.	Abegg M, Dysli M, Wolf S, et al. Microcystic macular edema: retrograde maculopathy caused by optic neuropathy[J]. Ophthalmology, 2014, 121(1): 142-149. DOI: 10.1016/j.ophtha.2013.08.045.
15.	Brazerol J, Iliev ME, Höhn R, et al. Retrograde maculopathy in patients with glaucoma[J]. J Glaucoma, 2017, 26(5): 423-429. DOI: 10.1097/IJG.0000000000000633.
16.	吕喆, 陶继伟, 王奇骅, 等. 内界膜剥除术对比不剥除术治疗特发性黄斑前膜的疗效的meta分析[J]. 中华眼视光学与视觉科学杂志, 2016, 18(6): 340-346. DOI: 10.3760/cma.j.issn.1674-845X.2016.06.005.Lyu Z, Tao JW, Wang QH, et al. A meta-analysis of the clinical effectiveness of idiopathic macular epiretinal membrane surgery with or without internal limiting membrane peeling[J]. Chin J Ophthalmol Vis Sci, 2016, 18(6): 340-346. DOI: 10.3760/cma.j.issn.1674-845X.2016.06.005.
17.	Chen SJ, Tsai FY, Liu HC, et al. Postoperative inner nuclear layer microcysts affecting long-term visual outcomes after epiretinal membrane surgery[J]. Retina, 2016, 36(12): 2377-2383. DOI: 10.1097/IAE.0000000000001100.
18.	余秋蓉, 朱思泉. 白内障术后黄斑囊样水肿的研究进展[J]. 国际眼科杂志, 2005, 5(5): 160-163. DOI: 10.3969/j.issn.1672-5123.2005.05.039.Yu QR, Zhu SQ. Advances of cystoid macular edema after cataract surgery[J]. Int Eye Sci, 2005, 5(5): 160-163. DOI: 10.3969/j.issn.1672-5123.2005.05.039.
19.	Dysli M, Rückert R, Munk MR. Differentiation of underlying pathologies of macular edema using spectral domain optical coherence tomography (SD-OCT)[J]. Ocul Immunol Inflamm, 2019, 27(3): 474-483. DOI: 10.1080/09273948.2019.1603313.
20.	Liu J, Qian Y, Yang S, et al. Pathophysiological correlations between fundus fluorescein angiography and optical coherence tomography results in patients with idiopathic epiretinal membranes[J]. Exp Ther Med, 2017, 14(6): 5785-5792. DOI: 10.3892/etm.2017.5330.

1. Burggraaff MC, Trieu J, de Vries-Knoppert WA, et al. The clinical spectrum of microcystic macular edema[J]. Invest Ophthalmol Vis Sci, 2014, 55(2): 952-961. DOI: 10.1167/iovs.13-12912.
2. Balk LJ, Killestein J, Polman CH, et al. Microcystic macular oedema confirmed, but not specific for multiple sclerosis[J/OL]. Brain, 2012, 135(Pt 12): e226[2012-12-01]. https://pubmed.ncbi.nlm.nih.gov/23078994/. DOI: 10.1093/brain/aws216.
3. Querques G, Coscas F, Forte R, et al. Cystoid macular degeneration in exudative age-related macular degeneration[J]. Am J Ophthalmol, 2011, 152(1): 100-107. DOI: 10.1016/j.ajo.2011.01.027.
4. Saidha S, Sotirchos ES, Ibrahim MA, et al. Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study[J]. Lancet Neurol, 2012, 11(11): 963-972. DOI: 10.1016/S1474-4422(12)70213-2.
5. Dolz-Marco R, Hoang QV, Gallego-Pinazo R, et al. Assessment of the significance of cystic changes after epiretinal membrane surgery with internal limiting membrane removal[J]. Retina, 2016, 36(4): 727-732. DOI: 10.1097/IAE.0000000000000780.
6. Sigler EJ, Randolph JC, Charles S. Delayed onset inner nuclear layer cystic changes following internal limiting membrane removal for epimacular membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2013, 251(7): 1679-1685. DOI: 10.1007/s00417-012-2253-8.
7. Hsieh MH, Chou YB, Huang YM, et al. Inner nuclear layer microcyst configuration, distribution, and visual prognosis in patients with epiretinal membrane after vitrectomy and membrane peeling[J/OL]. Sci Rep, 2019, 9(1): 11570[2019-08-09]. https://pubmed.ncbi.nlm.nih.gov/31399631/. DOI: 10.1038/s41598-019-48097-1.
8. 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.
9. Gelfand JM, Nolan R, Schwartz DM, et al. Microcystic macular oedema in multiple sclerosis is associated with disease severity[J]. Brain, 2012, 135(Pt 6): 1786-1793. DOI: 10.1093/brain/aws098.
10. Gelfand JM, Cree BA, Nolan R, et al. Microcystic inner nuclear layer abnormalities and neuromyelitis optica[J]. JAMA Neurol, 2013, 70(5): 629-633. DOI: 10.1001/jamaneurol.2013.1832.
11. Sotirchos ES, Saidha S, Byraiah G, et al. In vivo identification of morphologic retinal abnormalities in neuromyelitis optica[J]. Neurology, 2013, 80(15): 1406-1414. DOI: 10.1212/WNL.0b013e31828c2f7a.
12. Wolff B, Basdekidou C, Vasseur V, et al. Retinal inner nuclear layer microcystic changes in optic nerve atrophy: a novel spectral-domain OCT finding[J]. Retina, 2013, 33(10): 2133-2138. DOI: 10.1097/IAE.0b013e31828e68d0.
13. Dysli M, Ebneter A, Menke MN, et al. Patients with epiretinal membranes display retrograde maculopathy after surgical peeling of the internal limiting membrane[J]. Retina, 2019, 39(11): 2132-2140. DOI: 10.1097/IAE.0000000000002266.
14. Abegg M, Dysli M, Wolf S, et al. Microcystic macular edema: retrograde maculopathy caused by optic neuropathy[J]. Ophthalmology, 2014, 121(1): 142-149. DOI: 10.1016/j.ophtha.2013.08.045.
15. Brazerol J, Iliev ME, Höhn R, et al. Retrograde maculopathy in patients with glaucoma[J]. J Glaucoma, 2017, 26(5): 423-429. DOI: 10.1097/IJG.0000000000000633.
16. 吕喆, 陶继伟, 王奇骅, 等. 内界膜剥除术对比不剥除术治疗特发性黄斑前膜的疗效的meta分析[J]. 中华眼视光学与视觉科学杂志, 2016, 18(6): 340-346. DOI: 10.3760/cma.j.issn.1674-845X.2016.06.005.Lyu Z, Tao JW, Wang QH, et al. A meta-analysis of the clinical effectiveness of idiopathic macular epiretinal membrane surgery with or without internal limiting membrane peeling[J]. Chin J Ophthalmol Vis Sci, 2016, 18(6): 340-346. DOI: 10.3760/cma.j.issn.1674-845X.2016.06.005.
17. Chen SJ, Tsai FY, Liu HC, et al. Postoperative inner nuclear layer microcysts affecting long-term visual outcomes after epiretinal membrane surgery[J]. Retina, 2016, 36(12): 2377-2383. DOI: 10.1097/IAE.0000000000001100.
18. 余秋蓉, 朱思泉. 白内障术后黄斑囊样水肿的研究进展[J]. 国际眼科杂志, 2005, 5(5): 160-163. DOI: 10.3969/j.issn.1672-5123.2005.05.039.Yu QR, Zhu SQ. Advances of cystoid macular edema after cataract surgery[J]. Int Eye Sci, 2005, 5(5): 160-163. DOI: 10.3969/j.issn.1672-5123.2005.05.039.
19. Dysli M, Rückert R, Munk MR. Differentiation of underlying pathologies of macular edema using spectral domain optical coherence tomography (SD-OCT)[J]. Ocul Immunol Inflamm, 2019, 27(3): 474-483. DOI: 10.1080/09273948.2019.1603313.
20. Liu J, Qian Y, Yang S, et al. Pathophysiological correlations between fundus fluorescein angiography and optical coherence tomography results in patients with idiopathic epiretinal membranes[J]. Exp Ther Med, 2017, 14(6): 5785-5792. DOI: 10.3892/etm.2017.5330.

Chinese Journal of Ocular Fundus Diseases

Clinical observation of microcystic macular edema before and after surgery for idiopathic epiretinal membrane

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