Research progress of pars plana vitrectomy with internal limiting membrane peeling for refractory macular edema_Chinese Journal of Ocular Fundus Diseases

Authors：

Miao Yuyang ,  Yan Hua

Department of Ophthalmology, Tianjin Medical University General Hospital, Tianjin 300052, China;

Corresponding author：

Yan Hua, Email: zyyyanhua@tmu.edu.cn

Keywords：

Macular edema; Vitreoretinal surgery; Internal limiting membrane; Review

DOI：

10.3760/cma.j.cn511434-20201207-00605

Video：

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The main treatment methods of macular edema (ME) are intravitreal injection of anti-vacular endothelial growth factor drugs, corticosteroids, retinal laser photocoagulation and pars plana vitrectomy (PPV). However, recurrent ME, epiretinal membrane formation and drug resistance have occurred to a part of patients, which is called refractory ME (RME). PPV with internal limiting membrane peeling (ILMP) has the potential of treating and relieving RME. PPV combined with ILMP can treat and relieve RME by removing the posterior vitreous cortex, or removing the epiretinal membrane or internal limiting membrane at the same time during surgery to relieve the traction between the vitreous body and the retina. However, due to the complex pathogenesis of ME, the therapeutic effects of PPV combined with ILMP on ME caused by different etiologies still need clinical studies to explore the best surgical methods for ME caused by different etiologies.

Citation： Miao Yuyang, Yan Hua. Research progress of pars plana vitrectomy with internal limiting membrane peeling for refractory macular edema. Chinese Journal of Ocular Fundus Diseases, 2021, 37(4): 315-318. doi: 10.3760/cma.j.cn511434-20201207-00605 Copy

1.	Bandello F, Battaglia Parodi M, Lanzetta P, et al. Diabetic macular edema[J]. Dev Ophthalmol, 2017, 58: 102-138. DOI: 10.1159/000455277.
2.	Fardeau C, Champion E, Massamba N, et al. Uveitic macular edema[J]. Eye (Lond), 2016, 30(10): 1277-1292. DOI: 10.1038/eye.2016.115.
3.	Jackson TL, Nicod E, Angelis A, et al. Pars plana vitrectomy for diabetic macular edema: a systematic review, meta-analysis, and synthesis of safety literature[J]. Retina, 2017, 37(5): 886-895. DOI: 10.1097/iae.0000000000001280.
4.	Peynshaert K, Devoldere J, Minnaert AK, et al. Morphology and composition of the inner limiting membrane: species-specific variations and relevance toward drug delivery research[J]. Curr Eye Res, 2019, 44(5): 465-475. DOI: 10.1080/02713683.2019.1565890.
5.	Semeraro F, Morescalchi F, Duse S, et al. Current trends about inner limiting membrane peeling in surgery for epiretinal membranes[J/OL]. J Ophthalmol, 2015, 2015: 671905[2015-09-03]. https://pubmed.ncbi.nlm.nih.gov/26425352/. DOI: 10.1155/2015/671905.
6.	Bonnin S, Sandali O, Bonnel S, et al. Vitrectomy with internal limiting membrane peeling for tractional and nontractional diabetic macular edema: long-term results of a comparative study[J]. Retina, 2015, 35(5): 921-928. DOI: 10.1097/iae.0000000000000433.
7.	Gandorfer A, Messmer EM, Ulbig MW, et al. Resolution of diabetic macular edema after surgical removal of the posterior hyaloid and the inner limiting membrane[J]. Retina, 2000, 20(2): 126-133. DOI: 10.1097/00006982-200003000-00003.
8.	Yang CM, Yeh PT, Cheng SF, et al. Macular appearance after diabetic vitrectomy for fibrovascular proliferation: an optical coherence tomography study[J]. Acta Ophthalmol, 2010, 88(2): 193-198. DOI: 10.1111/j.1755-3768.2008.01420.x.
9.	Guo J, Bi X, Chen SN, et al. Efficacy of internal limiting membrane peeling for diabetic macular edema after preoperative anti-vascular endothelial growth factor injection[J]. Int J Ophthalmol, 2020, 13(11): 1758-1764. DOI: 10.18240/ijo.2020.11.12.
10.	Someya H, Takayama K, Takeuchi M, et al. Outcomes of 25-gauge vitrectomy for tractional and nontractional diabetic macular edema with proliferative diabetic retinopathy[J/OL]. J Ophthalmol, 2019, 2019: 5304524[2019-12-11]. https://pubmed.ncbi.nlm.nih.gov/31885887/. DOI: 10.1155/2019/5304524.
11.	Hu XY, Liu H, Wang LN, et al. Efficacy and safety of vitrectomy with internal limiting membrane peeling for diabetic macular edema: a meta-analysis[J]. Int J Ophthalmol, 2018, 11(11): 1848-1855. DOI: 10.18240/ijo.2018.11.18.
12.	彭永奎, 刘新玲, 许英杰. 25G玻璃体切除术联合或不联合内界膜剥除术治疗严重增殖型糖尿病视网膜黄斑水肿的对比分析[J]. 临床合理用药杂志, 2018, 11(23): 22-23. DOI: 10.15887/j.cnki.13-1389/r.2018.23.010.Peng YK, Liu XL, Xu YJ. Comparative analysis of 25G vitrectomy combined with or without internal limiting membrane peeling for severe proliferative diabetic macular edema[J]. Chinese Journal of Clinical Rational Drug Use, 2018, 11(23): 22-23. DOI: 10.15887/j.cnki.13-1389/r.2018.23.010.
13.	Ulrich JN. Pars plana vitrectomy with internal limiting membrane peeling for nontractional diabetic macular edema[J]. Open Ophthalmol J, 2017, 11: 5-10. DOI: 10.2174/1874364101711010005.
14.	Kumagai K, Hangai M, Ogino N, et al. Effect of internal limiting membrane peeling on long-term visual outcomes for diabetic macular edema[J]. Retina, 2015, 35(7): 1422-1428. DOI: 10.1097/iae.0000000000000497.
15.	Ghassemi F, Bazvand F, Roohipoor R, et al. Outcomes of vitrectomy, membranectomy and internal limiting membrane peeling in patients with refractory diabetic macular edema and non-tractional epiretinal membrane[J]. J Curr Ophthalmol, 2016, 28(4): 199-205. DOI: 10.1016/j.joco.2016.08.006.
16.	Dehghan MH, Salehipour M, Naghib J, et al. Pars plana vitrectomy with internal limiting membrane peeling for refractory diffuse diabetic macular edema[J]. J Ophthalmic Vis Res, 2010, 5(3): 162-167.
17.	Rinaldi M, dell'Omo R, Morescalchi F, et al. ILM peeling in nontractional diabetic macular edema: review and metanalysis[J]. Int Ophthalmol, 2018, 38(6): 2709-2714. DOI: 10.1007/s10792-017-0761-6.
18.	Bracha P, Ciulla TA, Baumal CR. Vital dyes in vitreomacular surgery[J]. Ophthalmic Surg Lasers Imaging Retina, 2018, 49(10): 788-798. DOI: 10.3928/23258160-20181002-07.
19.	Ando F, Yasui O, Hirose H, et al. Optic nerve atrophy after vitrectomy with indocyanine green-assisted internal limiting membrane peeling in diffuse diabetic macular edema. Adverse effect of ICG-assisted ILM peeling[J]. Graefe's Arch Clin Exp Ophthalmol, 2004, 242(12): 995-999. DOI: 10.1007/s00417-004-0864-4.
20.	Hirata A, Yonemura N, Hasumura T, et al. New infusion cannula for prevention of retinal damage by infusion air during vitrectomy[J]. Retina, 2003, 23(5): 682-685. DOI: 10.1097/00006982-200310000-00013.
21.	Georgalas I, Rouvas A, Kotsolis A, et al. Full thickness macular hole formation in a patient with cystoid macular edema caused by CRVO treated with intravitreal bevacizicumab[J]. Ophthalmic Surg Lasers Imaging, 2010, 9: 1-4. DOI: 10.3928/15428877-20100215-31.
22.	Shirakata Y, Fukuda K, Fujita T, et al. Pars plana vitrectomy combined with internal limiting membrane peeling for recurrent macular edema due to branch retinal vein occlusion after antivascular endothelial growth factor treatments[J]. Clin Ophthalmol, 2016, 10: 277-283. DOI: 10.2147/opth.S85751.
23.	Shirakata Y, Fujita T, Nakano Y, et al. Pars plana vitrectomy combined with internal limiting membrane peeling to treat persistent macular edema after anti-vascular endothelial growth factor treatment in cases of ischemic central retinal vein occlusion[J]. Case Rep Ophthalmol, 2016, 7(1): 1-8. DOI: 10.1159/000443322.
24.	Baharivand N, Hariri A, Javadzadeh A, et al. Pars plana vitrectomy and internal limiting membrane peeling for macular edema secondary to retinal vein occlusion[J]. Clin Ophthalmol, 2011, 5: 1089-1093. DOI: 10.2147/opth.S23164.
25.	Adelman RA, Parnes AJ, Bopp S, et al. Strategy for the management of macular edema in retinal vein occlusion: the European vitreoretinal society macular edema study[J/OL]. Biomed Res Int, 2015, 2015: 870987[2015-01-29]. https://pubmed.ncbi.nlm.nih.gov/25705695/. DOI: 10.1155/2015/870987.
26.	Sato S, Inoue M, Yamane S, et al. Outcomes of microincision vitrectomy surgery with internal limiting membrane peeling for macular edema secondary to branch retinal vein occlusion[J]. Clin Ophthalmol, 2015, 9: 439-444. DOI: 10.2147/opth.S75659.
27.	Park DH, Kim IT. Long-term effects of vitrectomy and internal limiting membrane peeling for macular edema secondary to central retinal vein occlusion and hemiretinal vein occlusion[J]. Retina, 2010, 30(1): 117-124. DOI: 10.1097/IAE.0b013e3181bced68.
28.	Kumagai K, Ogino N, Fukami M, et al. Vitrectomy for macular edema due to retinal vein occlusion[J]. Clin Ophthalmol, 2019, 13: 969-984. DOI: 10.2147/opth.S203212.
29.	Iwase T, Oveson BC. Long-term outcome after vitrectomy for macular edema with retinal vein occlusion dividing into the occlusion site[J/OL]. J Ophthalmol, 2014, 2014: 198782[2014-10-13]. https://pubmed.ncbi.nlm.nih.gov/25371814/. DOI: 10.1155/2014/198782.
30.	Mandelcorn MS, Mandelcorn E, Guan K, et al. Surgical macular decompression for macular edema in retinal vein occlusion[J]. Can J Ophthalmol, 2007, 42(1): 116-122. DOI: 10.3129/can.j.ophthalmol.06-091.
31.	Arai M, Yamamoto S, Mitamura Y, et al. Efficacy of vitrectomy and internal limiting membrane removal for macular edema associated with branch retinal vein occlusion[J]. Ophthalmologica, 2009, 223(3): 172-176. DOI: 10.1159/000197113.
32.	Henry CR, Becker MD, Yang Y, et al. Pars plana vitrectomy for the treatment of uveitis[J]. Am J Ophthalmol, 2018, 190: 142-149. DOI: 10.1016/j.ajo.2018.03.031.
33.	Wiechens B, Nölle B, Reichelt JA. Pars-plana vitrectomy in cystoid macular edema associated with intermediate uveitis[J]. Graefe's Arch Clin Exp Ophthalmol, 2001, 239(7): 474-481. DOI: 10.1007/s004170100254.
34.	Kiryu J, Kita M, Tanabe T, et al. Pars plana vitrectomy for cystoid macular edema secondary to sarcoid uveitis[J]. Ophthalmology, 2001, 108(6): 1140-1144. DOI: 10.1016/s0161-6420(01)00558-9.
35.	Pang JP, Son G, Yoon YH, et al. Combined vitrectomy with intravitreal dexamethasone implant for refractory macular edema secondary to diabetic retinopathy, retinal vein occlusion, and noninfectious posterior uveitis[J]. Retina, 2020, 40(1): 56-65. DOI: 10.1097/iae.0000000000002358.
36.	Radetzky S, Walter P, Fauser S, et al. Visual outcome of patients with macular edema after pars plana vitrectomy and indocyanine green-assisted peeling of the internal limiting membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2004, 242(4): 273-278. DOI: 10.1007/s00417-003-0731-8.
37.	Cho M, D'Amico DJ. Transconjunctival 25-gauge pars plana vitrectomy and internal limiting membrane peeling for chronic macular edema[J]. Clin Ophthalmol, 2012, 6: 981-989. DOI: 10.2147/opth.S33391.
38.	Rosenblatt BJ, Shah GK, Sharma S, et al. Pars plana vitrectomy with internal limiting membranectomy for refractory diabetic macular edema without a taut posterior hyaloid[J]. Graefe's Arch Clin Exp Ophthalmol, 2005, 243(1): 20-25. DOI: 10.1007/s00417-004-0958-z.

1. Bandello F, Battaglia Parodi M, Lanzetta P, et al. Diabetic macular edema[J]. Dev Ophthalmol, 2017, 58: 102-138. DOI: 10.1159/000455277.
2. Fardeau C, Champion E, Massamba N, et al. Uveitic macular edema[J]. Eye (Lond), 2016, 30(10): 1277-1292. DOI: 10.1038/eye.2016.115.
3. Jackson TL, Nicod E, Angelis A, et al. Pars plana vitrectomy for diabetic macular edema: a systematic review, meta-analysis, and synthesis of safety literature[J]. Retina, 2017, 37(5): 886-895. DOI: 10.1097/iae.0000000000001280.
4. Peynshaert K, Devoldere J, Minnaert AK, et al. Morphology and composition of the inner limiting membrane: species-specific variations and relevance toward drug delivery research[J]. Curr Eye Res, 2019, 44(5): 465-475. DOI: 10.1080/02713683.2019.1565890.
5. Semeraro F, Morescalchi F, Duse S, et al. Current trends about inner limiting membrane peeling in surgery for epiretinal membranes[J/OL]. J Ophthalmol, 2015, 2015: 671905[2015-09-03]. https://pubmed.ncbi.nlm.nih.gov/26425352/. DOI: 10.1155/2015/671905.
6. Bonnin S, Sandali O, Bonnel S, et al. Vitrectomy with internal limiting membrane peeling for tractional and nontractional diabetic macular edema: long-term results of a comparative study[J]. Retina, 2015, 35(5): 921-928. DOI: 10.1097/iae.0000000000000433.
7. Gandorfer A, Messmer EM, Ulbig MW, et al. Resolution of diabetic macular edema after surgical removal of the posterior hyaloid and the inner limiting membrane[J]. Retina, 2000, 20(2): 126-133. DOI: 10.1097/00006982-200003000-00003.
8. Yang CM, Yeh PT, Cheng SF, et al. Macular appearance after diabetic vitrectomy for fibrovascular proliferation: an optical coherence tomography study[J]. Acta Ophthalmol, 2010, 88(2): 193-198. DOI: 10.1111/j.1755-3768.2008.01420.x.
9. Guo J, Bi X, Chen SN, et al. Efficacy of internal limiting membrane peeling for diabetic macular edema after preoperative anti-vascular endothelial growth factor injection[J]. Int J Ophthalmol, 2020, 13(11): 1758-1764. DOI: 10.18240/ijo.2020.11.12.
10. Someya H, Takayama K, Takeuchi M, et al. Outcomes of 25-gauge vitrectomy for tractional and nontractional diabetic macular edema with proliferative diabetic retinopathy[J/OL]. J Ophthalmol, 2019, 2019: 5304524[2019-12-11]. https://pubmed.ncbi.nlm.nih.gov/31885887/. DOI: 10.1155/2019/5304524.
11. Hu XY, Liu H, Wang LN, et al. Efficacy and safety of vitrectomy with internal limiting membrane peeling for diabetic macular edema: a meta-analysis[J]. Int J Ophthalmol, 2018, 11(11): 1848-1855. DOI: 10.18240/ijo.2018.11.18.
12. 彭永奎, 刘新玲, 许英杰. 25G玻璃体切除术联合或不联合内界膜剥除术治疗严重增殖型糖尿病视网膜黄斑水肿的对比分析[J]. 临床合理用药杂志, 2018, 11(23): 22-23. DOI: 10.15887/j.cnki.13-1389/r.2018.23.010.Peng YK, Liu XL, Xu YJ. Comparative analysis of 25G vitrectomy combined with or without internal limiting membrane peeling for severe proliferative diabetic macular edema[J]. Chinese Journal of Clinical Rational Drug Use, 2018, 11(23): 22-23. DOI: 10.15887/j.cnki.13-1389/r.2018.23.010.
13. Ulrich JN. Pars plana vitrectomy with internal limiting membrane peeling for nontractional diabetic macular edema[J]. Open Ophthalmol J, 2017, 11: 5-10. DOI: 10.2174/1874364101711010005.
14. Kumagai K, Hangai M, Ogino N, et al. Effect of internal limiting membrane peeling on long-term visual outcomes for diabetic macular edema[J]. Retina, 2015, 35(7): 1422-1428. DOI: 10.1097/iae.0000000000000497.
15. Ghassemi F, Bazvand F, Roohipoor R, et al. Outcomes of vitrectomy, membranectomy and internal limiting membrane peeling in patients with refractory diabetic macular edema and non-tractional epiretinal membrane[J]. J Curr Ophthalmol, 2016, 28(4): 199-205. DOI: 10.1016/j.joco.2016.08.006.
16. Dehghan MH, Salehipour M, Naghib J, et al. Pars plana vitrectomy with internal limiting membrane peeling for refractory diffuse diabetic macular edema[J]. J Ophthalmic Vis Res, 2010, 5(3): 162-167.
17. Rinaldi M, dell'Omo R, Morescalchi F, et al. ILM peeling in nontractional diabetic macular edema: review and metanalysis[J]. Int Ophthalmol, 2018, 38(6): 2709-2714. DOI: 10.1007/s10792-017-0761-6.
18. Bracha P, Ciulla TA, Baumal CR. Vital dyes in vitreomacular surgery[J]. Ophthalmic Surg Lasers Imaging Retina, 2018, 49(10): 788-798. DOI: 10.3928/23258160-20181002-07.
19. Ando F, Yasui O, Hirose H, et al. Optic nerve atrophy after vitrectomy with indocyanine green-assisted internal limiting membrane peeling in diffuse diabetic macular edema. Adverse effect of ICG-assisted ILM peeling[J]. Graefe's Arch Clin Exp Ophthalmol, 2004, 242(12): 995-999. DOI: 10.1007/s00417-004-0864-4.
20. Hirata A, Yonemura N, Hasumura T, et al. New infusion cannula for prevention of retinal damage by infusion air during vitrectomy[J]. Retina, 2003, 23(5): 682-685. DOI: 10.1097/00006982-200310000-00013.
21. Georgalas I, Rouvas A, Kotsolis A, et al. Full thickness macular hole formation in a patient with cystoid macular edema caused by CRVO treated with intravitreal bevacizicumab[J]. Ophthalmic Surg Lasers Imaging, 2010, 9: 1-4. DOI: 10.3928/15428877-20100215-31.
22. Shirakata Y, Fukuda K, Fujita T, et al. Pars plana vitrectomy combined with internal limiting membrane peeling for recurrent macular edema due to branch retinal vein occlusion after antivascular endothelial growth factor treatments[J]. Clin Ophthalmol, 2016, 10: 277-283. DOI: 10.2147/opth.S85751.
23. Shirakata Y, Fujita T, Nakano Y, et al. Pars plana vitrectomy combined with internal limiting membrane peeling to treat persistent macular edema after anti-vascular endothelial growth factor treatment in cases of ischemic central retinal vein occlusion[J]. Case Rep Ophthalmol, 2016, 7(1): 1-8. DOI: 10.1159/000443322.
24. Baharivand N, Hariri A, Javadzadeh A, et al. Pars plana vitrectomy and internal limiting membrane peeling for macular edema secondary to retinal vein occlusion[J]. Clin Ophthalmol, 2011, 5: 1089-1093. DOI: 10.2147/opth.S23164.
25. Adelman RA, Parnes AJ, Bopp S, et al. Strategy for the management of macular edema in retinal vein occlusion: the European vitreoretinal society macular edema study[J/OL]. Biomed Res Int, 2015, 2015: 870987[2015-01-29]. https://pubmed.ncbi.nlm.nih.gov/25705695/. DOI: 10.1155/2015/870987.
26. Sato S, Inoue M, Yamane S, et al. Outcomes of microincision vitrectomy surgery with internal limiting membrane peeling for macular edema secondary to branch retinal vein occlusion[J]. Clin Ophthalmol, 2015, 9: 439-444. DOI: 10.2147/opth.S75659.
27. Park DH, Kim IT. Long-term effects of vitrectomy and internal limiting membrane peeling for macular edema secondary to central retinal vein occlusion and hemiretinal vein occlusion[J]. Retina, 2010, 30(1): 117-124. DOI: 10.1097/IAE.0b013e3181bced68.
28. Kumagai K, Ogino N, Fukami M, et al. Vitrectomy for macular edema due to retinal vein occlusion[J]. Clin Ophthalmol, 2019, 13: 969-984. DOI: 10.2147/opth.S203212.
29. Iwase T, Oveson BC. Long-term outcome after vitrectomy for macular edema with retinal vein occlusion dividing into the occlusion site[J/OL]. J Ophthalmol, 2014, 2014: 198782[2014-10-13]. https://pubmed.ncbi.nlm.nih.gov/25371814/. DOI: 10.1155/2014/198782.
30. Mandelcorn MS, Mandelcorn E, Guan K, et al. Surgical macular decompression for macular edema in retinal vein occlusion[J]. Can J Ophthalmol, 2007, 42(1): 116-122. DOI: 10.3129/can.j.ophthalmol.06-091.
31. Arai M, Yamamoto S, Mitamura Y, et al. Efficacy of vitrectomy and internal limiting membrane removal for macular edema associated with branch retinal vein occlusion[J]. Ophthalmologica, 2009, 223(3): 172-176. DOI: 10.1159/000197113.
32. Henry CR, Becker MD, Yang Y, et al. Pars plana vitrectomy for the treatment of uveitis[J]. Am J Ophthalmol, 2018, 190: 142-149. DOI: 10.1016/j.ajo.2018.03.031.
33. Wiechens B, Nölle B, Reichelt JA. Pars-plana vitrectomy in cystoid macular edema associated with intermediate uveitis[J]. Graefe's Arch Clin Exp Ophthalmol, 2001, 239(7): 474-481. DOI: 10.1007/s004170100254.
34. Kiryu J, Kita M, Tanabe T, et al. Pars plana vitrectomy for cystoid macular edema secondary to sarcoid uveitis[J]. Ophthalmology, 2001, 108(6): 1140-1144. DOI: 10.1016/s0161-6420(01)00558-9.
35. Pang JP, Son G, Yoon YH, et al. Combined vitrectomy with intravitreal dexamethasone implant for refractory macular edema secondary to diabetic retinopathy, retinal vein occlusion, and noninfectious posterior uveitis[J]. Retina, 2020, 40(1): 56-65. DOI: 10.1097/iae.0000000000002358.
36. Radetzky S, Walter P, Fauser S, et al. Visual outcome of patients with macular edema after pars plana vitrectomy and indocyanine green-assisted peeling of the internal limiting membrane[J]. Graefe's Arch Clin Exp Ophthalmol, 2004, 242(4): 273-278. DOI: 10.1007/s00417-003-0731-8.
37. Cho M, D'Amico DJ. Transconjunctival 25-gauge pars plana vitrectomy and internal limiting membrane peeling for chronic macular edema[J]. Clin Ophthalmol, 2012, 6: 981-989. DOI: 10.2147/opth.S33391.
38. Rosenblatt BJ, Shah GK, Sharma S, et al. Pars plana vitrectomy with internal limiting membranectomy for refractory diabetic macular edema without a taut posterior hyaloid[J]. Graefe's Arch Clin Exp Ophthalmol, 2005, 243(1): 20-25. DOI: 10.1007/s00417-004-0958-z.

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