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Офтальмохирургия. 2021; : 83-88

Удаление внутренней пограничной мембраны при патологии витреомакулярного интерфейса: за и против

Колесник С. В., Колесник А. И., Миридонова А. В., Авакян Ф. А., Журавлев А. С.

https://doi.org/10.25276/0235-4160-2021-3-83-88

Аннотация

Цель. Предоставить данные об эффективности и безопасности удаления внутренней пограничной мембраны (ВПМ) при различных патологиях витреомакулярного интерфейса. Материал и методы. Для выполнения обзора был осуществлен поиск источников литературы по реферативным базам PubMed и Scopus за период до 2021 года включительно с использованием ключевых слов «internal limiting membrane peeling», «macular hole», «epiretinal membrane». Всего было отобрано 38 статей, относящихся к теме обзора. Результаты. Многочисленными исследованиями подтверждена эффективность пилинга ВПМ в улучшении анатомо-функциональных исходов лечения различных заболеваний. Однако даже безупречно выполненный пилинг может вызывать как анатомические, так и функциональные последствия для сетчатки. Различными исследованиями продемонстрировано, что анатомические осложнения пилинга ВПМ не коррелировали с функциональными результатами лечения. Заключение. Выполненный анализ литературы позволяет утверждать, что удаление ВПМ обеспечивает улучшение анатомо-функциональных результатов лечения и снижает необходимость повторного хирургического вмешательства. Однако для оценки безопасности данной процедуры необходимы дальнейшие исследования с оценкой зрительных функций в отдаленном периоде.

Список литературы

1. Захаров В.Д., Борзенок С.А., Колесник С.В., Горшков И.М., Колесник А.И., Миридонова А.В. Этиопатогенетические аспекты и роль структур витреоретинального интерфейса в формировании идиопатических эпиретинальных мембран. Практическая медицина. 2018;3: 71–76.

2. Candiello J, Cole G, Halfter W. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biology. 2010;29(5): 402–410. doi: 10.1016/j.matbio.2010.03.004

3. Remington L. Retina. In: Clinical anatomy and physiology of the visual system (3rd ed.). Oxford: Butterworth-Heinemann; 2012. P. 61–92.

4. Abdelkader EA, McBain VA, Anand M, Scott NW, Rehman Siddiqui MA, Lois N. In vivo safety of trypan blue use in vitreoretinal surgery. Retina. 2011;31(6): 1122–1127. doi: 10.1097/IAE.0b013e3182003adb

5. Henrich PB, Haritoglou C, Meyer P, Ferreira PR, Schötzau A, Katamay R, Josifova T, Schneider U, Flammer J, Priglinger S. Anatomical and functional outcome in brilliant blue G assisted chromovitrectomy. Acta Ophthalmol. 2010;88(5): 588–593. doi:10.1111/j.1755-3768.2008.01477.x

6. Gerding H, Timmermann M, Thelen U. Staining of the ILM with brilliant blue G (Brilliant Peel®): safety and efficacy. Invest Ophthalmol Vis Sci. 2010;51(13): 2552– 2552.

7. Chatziralli IP, Theodossiadis PG, Steel DHW. Internal limiting membrane peeling in macular hole surgery; why, when, and how? Retina. 2018;38(5): 870–882. doi:10.1097/IAE.0000000000001959.

8. Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology. 2010;117(10): 2018–2025. doi: 10.1016/j.ophtha.2010.02.011.

9. Morizane Y, Shiraga F, Kimura S, Hosokawa M, Shiode Y, Kawata T, Hosogi M, Shirakata Y, Okanouchi T. Autologous transplantation of the internal limiting membrane for refractory macular holes. Am J Ophthalmol. 2014;157(4):861–869. doi: 10.1016/j.ajo.2013.12.028.

10. Кислицина Н.М., Новиков С.В., Колесник А.И., Колесник С.В., Веселкова М.П. Хирургическое лечение макулярных разрывов большого диаметра с использованием суспензии «Витреоконтраст». Современные технологии в офтальмологии. 2017;(1): 120–123.

11. Белый Ю.А., Терещенко А.В., Шкворченко Д.О., Ерохина Е.В., Шилов Н.М. Новая методика формирования фрагмента внутренней пограничной мембра-ны в хирургическом лечении больших идиопатических макулярных разрывов. Офтальмология. 2015;12(4): 27–33. doi:10.18008/1816-5095-2015-4-27-33

12. Mester V, Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes. Am J Ophthalmol. 2000;129(6): 769–777. doi: 10.1016/s0002-9394(00)00358-5

13. Spiteri Cornish K, Lois N, Scott NW, Burr J, Cook J, Boachie C, Tadayoni R, la Cour M, Christensen U, Kwok AKH. Vitrectomy with internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole. Ophthalmology. 2014;121(3): 649–655. doi: 10.1016/j.ophtha.2013.10.020

14. Velez-Montoya R, Ramirez-Estudillo JA, Sjoholm-Gomez de Liano C, BejarCornejo F, Sanchez-Ramos J, Guerrero-Naranjo JL, Morales-Canton V, Hernandez-Da Mota SE. Inverted ILM flap, free ILM flap and conventional ILM peeling for large macular holes. Int J Retina Vitreous. 2018;4. doi: 10.1186/s40942-018-0111-5

15. Morescalchi F, Costagliola C, Gambicorti E, Duse S, Romano MR, Semeraro F. Controversies over the role of internal limiting membrane peeling during vitrectomy in macular hole surgery. Surv Ophthalmol. 2017;62(1): 58–69. doi: 10.1016/j.survophthal.2016.07.003

16. Pak KY, Park KH, Kim KH, Park SW, Byon IS, Kim HW, Chung IY, Lee JE, Lee SJ, Lee JE. Topographic changes of the macula after closure of idiopathic macular hole. Retina. 2017;37(4): 667–672. doi:10.1097/IAE.0000000000001251

17. Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology. 2010;117(10): 2018–2025. doi: 10.1016/j.ophtha.2010.02.011

18. Morizane Y, Shiraga F, Kimura S, Hosokawa M, Shiode Y, Kawata T, Hosogi M, Shirakata Y, Okanouchi T. Autologous transplantation of the internal limiting membrane for refractory macular holes. Am J Ophthalmol. 2014;157(4): 861–869.e1. doi: 10.1016/j.ajo.2013.12.028

19. Kase S, Saito W, Mori S, Saito M, Ando R, Dong Z, Suzuki T, Noda K, Ishida S. Clinical and histological evaluation of large macular hole surgery using the inverted internal limiting membrane flap technique. Clin Ophthalmol. 2017;11: 9–14. doi: 10.2147/OPTH.S119762

20. Almony A, Nudleman E, Shah GK, Blinder KJ, Eliott DB, Mittra RA, Tewari A. Techniques, rationale, and outcomes of internal limiting membrane peeling. Retina. 2012;32(5): 877–891. doi: 10.1097/IAE.0b013e318227ab39

21. Захаров В.Д., Борзенок С.А., Колесник С.В., Горшков И.М., Колесник А.И., Шестопалов В.И., Миридонова А.В., Островский Д.С. Преимущества и клинико-морфологические результаты раннего хирургического лечения идиопатических эпиретинальных мембран. Аспирантский Вестник Поволжья. 2019;19(1–2): 70–79. doi: 10.17816/2072-2354.2019.19.1.70-79

22. Tranos P, Wickham L, Dervenis N, Vakalis A, Asteriades S, Stavrakas P. The role of membrane-inner retina adherence in predicting simultaneous internal limiting membrane peeling during idiopathic epiretinal membrane surgery. Eye (Lond). 2017;31(4): 636–642. doi:10.1038/eye.2016.285

23. Lee JW, Kim IT. Outcomes of idiopathic macular epiretinal membrane removal with and without internal limiting membrane peeling: a comparative study. Jpn J Ophthalmol. 2010;54(2): 129–134. doi: 10.1007/s10384-009-0778-0

24. Nam KY, Kim JY. Effect of internal limiting membrane peeling on the development of epiretinal membrane after pars plana vitrectomy for primary rhegmatogenous retinal detachment. Retina. 2015;35(5): 880–885. doi: 10.1097/IAE.0000000000000421

25. Fallico M, Russo A, Longo A, Pulvirenti A, Avitabile T, Bonfiglio V, Castellino N, Cennamo G, Reibaldi M. Internal limiting membrane peeling versus no peeling during primary vitrectomy for rhegmatogenous retinal detachment: A systematic review and meta-analysis. PLoS ONE. 2018;13(7): e0201010. doi: 10.1371/journal.pone.0201010

26. Захаров В.Д., Шкворченко Д.О., Какунина С.А., Норман К.С., Фозилова Ф.Ф. Эффективность пилинга внутренней пограничной мембраны на фоне силиконовой тампонады при регматогенной отслойке сетчатки. Таврический Медико-Биологический Вестник. 2018;21(4): 23–27.

27. Gandorfer A, Messmer EM, Ulbig MW, Kampik A. Resolution of diabetic macular edema after surgical removal of the posterior hyaloid and the inner limiting membrane. Retina. 2000;20(2): 126–133.

28. Бикбов М.М., Зайнуллин Р.М., Файзрахманов Р.Р. Эффективность витрэктомии с пилингом внутренней пограничной мембраны при диабетическом макулярном отеке в сочетании с витреомакулярным тракционным синдромом. Современные технологии в офтальмологии. 2017;1: 31–35

29. Панченко Ю.А. Эффективность закрытой субтотальной витрэктомии в сочетании с панретинальной лазеркоагуляцией в лечении диабетической макулопатии у больных сахарным диабетом 2-го типа. Архив офтальмологии Украины. 2019;7(2): 38–44.

30. Stolba U, Binder S, Gruber D, Krebs I, Aggermann T, Neumaier B. Vitrectomy for persistent diffuse diabetic macular edema. Am J Ophthalmol. 2005;140(2): 295– 301. doi: 10.1016/j.ajo.2005.03.045

31. Nakajima T, Roggia MF, Noda Y, Ueta T. Effect of internal limiting membrane peeling during vitrectomy for diabetic macular edema: Systematic Review and Meta-analysis. Retina (Philadelphia, Pa). 2015;35(9):1719-1725. doi: 10.1097/IAE.0000000000000622

32. Rinaldi M, dell’Omo R, Morescalchi F, Semeraro F, Gambicorti E, Cacciatore F, Chiosi F, Costagliola C. ILM peeling in nontractional diabetic macular edema: review and metanalysis. Int Ophthalmol. 2018;38(6): 2709–2714. doi: 10.1007/s10792-017-0761-6

33. Mason JO, Feist RM, Albert MA. Eccentric macular holes after vitrectomy with peeling of epimacular proliferation. Retina. 2007;27(1): 45–48. doi: 10.1097/01.iae.0000256661.56617.69

34. Clark A, Balducci N, Pichi F, Veronese C, Morara M, Torrazza C, Ciardella AP. Swelling of the arcuate nerve fiber layer after internal limiting membrane peeling. Retina. 2012;32(8): 1608–1613. doi:10.1097/IAE.0b013e3182437e86

35. Pichi F, Lembo A, Morara M, Veronese C, Alkabes M, Nucci P, Ciardella AP. Early and late inner retinal changes after inner limiting membrane peeling. Int Ophthalmol. 2014;34(2): 437–446. doi: 10.1007/s10792-013-9831-6 36.

36. Tadayoni R, Paques M, Massin P, Mouki-Benani S, Mikol J, Gaudric A. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology. 2001;108(12): 2279–2283. doi: 10.1016/s01616420(01)00856-9

37. Mitamura Y, Ohtsuka K. Relationship of dissociated optic nerve fiber layer appearance to internal limiting membrane peeling. Ophthalmology. 2005;112(10): 1766–1770. doi: 10.1016/j.ophtha.2005.04.026

38. Treumer F, Wacker N, Junge O, Hedderich J, Roider J, Hillenkamp J. Foveal structure and thickness of retinal layers long-term after surgical peeling of idiopathic epiretinal membrane. Invest Ophthalmol Vis Sci. 2011;52(2): 744–750. doi:10.1167/iovs.10-6310

Fyodorov Journal of Ophthalmic Surgery. 2021; : 83-88

ILM removal in vitreomacular interface disorders: for or against?

Kolesnik S. V., Kolesnik A. I., Miridonova A. V., Avakyan F. A., Zhuravlev A. S.

https://doi.org/10.25276/0235-4160-2021-3-83-88

Abstract

Purpose. To provide data on efficacy and safety of internal limiting membrane (ILM) removal in various pathologies of the vitreomacular interface. Material and methods. To perform the review, literature sources were searched through the PubMed and Scopus databases up to year 2021 using the keywords “internal limiting membrane peeling”, “macular hole”, “epiretinal membrane”. A total of 38 articles relevant to the topic of the review were selected. Results. Numerous studies have confirmed the efficacy of internal limiting peeling in improving anatomical and functional outcomes of treatment of various pathologies. However, even a flawlessly performed peeling can cause both anatomical and functional effects on the retina. Various studies have demonstrated that the anatomical complications of ILM peeling did not correlate with the functional outcomes of surgery. Conclusion. Available evidence supports ILM peeling as an intervention that improves anatomical and functional results of treatment and reduces rate of reoperation. However, in order to evaluate the safety of this procedure, further studies with an assessment of the visual function with a long follow-up period ar e required.

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2. Candiello J, Cole G, Halfter W. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biology. 2010;29(5): 402–410. doi: 10.1016/j.matbio.2010.03.004

3. Remington L. Retina. In: Clinical anatomy and physiology of the visual system (3rd ed.). Oxford: Butterworth-Heinemann; 2012. P. 61–92.

4. Abdelkader EA, McBain VA, Anand M, Scott NW, Rehman Siddiqui MA, Lois N. In vivo safety of trypan blue use in vitreoretinal surgery. Retina. 2011;31(6): 1122–1127. doi: 10.1097/IAE.0b013e3182003adb

5. Henrich PB, Haritoglou C, Meyer P, Ferreira PR, Schötzau A, Katamay R, Josifova T, Schneider U, Flammer J, Priglinger S. Anatomical and functional outcome in brilliant blue G assisted chromovitrectomy. Acta Ophthalmol. 2010;88(5): 588–593. doi:10.1111/j.1755-3768.2008.01477.x

6. Gerding H, Timmermann M, Thelen U. Staining of the ILM with brilliant blue G (Brilliant Peel®): safety and efficacy. Invest Ophthalmol Vis Sci. 2010;51(13): 2552– 2552.

7. Chatziralli IP, Theodossiadis PG, Steel DHW. Internal limiting membrane peeling in macular hole surgery; why, when, and how? Retina. 2018;38(5): 870–882. doi:10.1097/IAE.0000000000001959.

8. Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology. 2010;117(10): 2018–2025. doi: 10.1016/j.ophtha.2010.02.011.

9. Morizane Y, Shiraga F, Kimura S, Hosokawa M, Shiode Y, Kawata T, Hosogi M, Shirakata Y, Okanouchi T. Autologous transplantation of the internal limiting membrane for refractory macular holes. Am J Ophthalmol. 2014;157(4):861–869. doi: 10.1016/j.ajo.2013.12.028.

10. Kislitsina N.M., Novikov S.V., Kolesnik A.I., Kolesnik S.V., Veselkova M.P. Khirurgicheskoe lechenie makulyarnykh razryvov bol'shogo diametra s ispol'zovaniem suspenzii «Vitreokontrast». Sovremennye tekhnologii v oftal'mologii. 2017;(1): 120–123.

11. Belyi Yu.A., Tereshchenko A.V., Shkvorchenko D.O., Erokhina E.V., Shilov N.M. Novaya metodika formirovaniya fragmenta vnutrennei pogranichnoi membra-ny v khirurgicheskom lechenii bol'shikh idiopaticheskikh makulyarnykh razryvov. Oftal'mologiya. 2015;12(4): 27–33. doi:10.18008/1816-5095-2015-4-27-33

12. Mester V, Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes. Am J Ophthalmol. 2000;129(6): 769–777. doi: 10.1016/s0002-9394(00)00358-5

13. Spiteri Cornish K, Lois N, Scott NW, Burr J, Cook J, Boachie C, Tadayoni R, la Cour M, Christensen U, Kwok AKH. Vitrectomy with internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole. Ophthalmology. 2014;121(3): 649–655. doi: 10.1016/j.ophtha.2013.10.020

14. Velez-Montoya R, Ramirez-Estudillo JA, Sjoholm-Gomez de Liano C, BejarCornejo F, Sanchez-Ramos J, Guerrero-Naranjo JL, Morales-Canton V, Hernandez-Da Mota SE. Inverted ILM flap, free ILM flap and conventional ILM peeling for large macular holes. Int J Retina Vitreous. 2018;4. doi: 10.1186/s40942-018-0111-5

15. Morescalchi F, Costagliola C, Gambicorti E, Duse S, Romano MR, Semeraro F. Controversies over the role of internal limiting membrane peeling during vitrectomy in macular hole surgery. Surv Ophthalmol. 2017;62(1): 58–69. doi: 10.1016/j.survophthal.2016.07.003

16. Pak KY, Park KH, Kim KH, Park SW, Byon IS, Kim HW, Chung IY, Lee JE, Lee SJ, Lee JE. Topographic changes of the macula after closure of idiopathic macular hole. Retina. 2017;37(4): 667–672. doi:10.1097/IAE.0000000000001251

17. Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology. 2010;117(10): 2018–2025. doi: 10.1016/j.ophtha.2010.02.011

18. Morizane Y, Shiraga F, Kimura S, Hosokawa M, Shiode Y, Kawata T, Hosogi M, Shirakata Y, Okanouchi T. Autologous transplantation of the internal limiting membrane for refractory macular holes. Am J Ophthalmol. 2014;157(4): 861–869.e1. doi: 10.1016/j.ajo.2013.12.028

19. Kase S, Saito W, Mori S, Saito M, Ando R, Dong Z, Suzuki T, Noda K, Ishida S. Clinical and histological evaluation of large macular hole surgery using the inverted internal limiting membrane flap technique. Clin Ophthalmol. 2017;11: 9–14. doi: 10.2147/OPTH.S119762

20. Almony A, Nudleman E, Shah GK, Blinder KJ, Eliott DB, Mittra RA, Tewari A. Techniques, rationale, and outcomes of internal limiting membrane peeling. Retina. 2012;32(5): 877–891. doi: 10.1097/IAE.0b013e318227ab39

21. Zakharov V.D., Borzenok S.A., Kolesnik S.V., Gorshkov I.M., Kolesnik A.I., Shestopalov V.I., Miridonova A.V., Ostrovskii D.S. Preimushchestva i kliniko-morfologicheskie rezul'taty rannego khirurgicheskogo lecheniya idiopaticheskikh epiretinal'nykh membran. Aspirantskii Vestnik Povolzh'ya. 2019;19(1–2): 70–79. doi: 10.17816/2072-2354.2019.19.1.70-79

22. Tranos P, Wickham L, Dervenis N, Vakalis A, Asteriades S, Stavrakas P. The role of membrane-inner retina adherence in predicting simultaneous internal limiting membrane peeling during idiopathic epiretinal membrane surgery. Eye (Lond). 2017;31(4): 636–642. doi:10.1038/eye.2016.285

23. Lee JW, Kim IT. Outcomes of idiopathic macular epiretinal membrane removal with and without internal limiting membrane peeling: a comparative study. Jpn J Ophthalmol. 2010;54(2): 129–134. doi: 10.1007/s10384-009-0778-0

24. Nam KY, Kim JY. Effect of internal limiting membrane peeling on the development of epiretinal membrane after pars plana vitrectomy for primary rhegmatogenous retinal detachment. Retina. 2015;35(5): 880–885. doi: 10.1097/IAE.0000000000000421

25. Fallico M, Russo A, Longo A, Pulvirenti A, Avitabile T, Bonfiglio V, Castellino N, Cennamo G, Reibaldi M. Internal limiting membrane peeling versus no peeling during primary vitrectomy for rhegmatogenous retinal detachment: A systematic review and meta-analysis. PLoS ONE. 2018;13(7): e0201010. doi: 10.1371/journal.pone.0201010

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27. Gandorfer A, Messmer EM, Ulbig MW, Kampik A. Resolution of diabetic macular edema after surgical removal of the posterior hyaloid and the inner limiting membrane. Retina. 2000;20(2): 126–133.

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30. Stolba U, Binder S, Gruber D, Krebs I, Aggermann T, Neumaier B. Vitrectomy for persistent diffuse diabetic macular edema. Am J Ophthalmol. 2005;140(2): 295– 301. doi: 10.1016/j.ajo.2005.03.045

31. Nakajima T, Roggia MF, Noda Y, Ueta T. Effect of internal limiting membrane peeling during vitrectomy for diabetic macular edema: Systematic Review and Meta-analysis. Retina (Philadelphia, Pa). 2015;35(9):1719-1725. doi: 10.1097/IAE.0000000000000622

32. Rinaldi M, dell’Omo R, Morescalchi F, Semeraro F, Gambicorti E, Cacciatore F, Chiosi F, Costagliola C. ILM peeling in nontractional diabetic macular edema: review and metanalysis. Int Ophthalmol. 2018;38(6): 2709–2714. doi: 10.1007/s10792-017-0761-6

33. Mason JO, Feist RM, Albert MA. Eccentric macular holes after vitrectomy with peeling of epimacular proliferation. Retina. 2007;27(1): 45–48. doi: 10.1097/01.iae.0000256661.56617.69

34. Clark A, Balducci N, Pichi F, Veronese C, Morara M, Torrazza C, Ciardella AP. Swelling of the arcuate nerve fiber layer after internal limiting membrane peeling. Retina. 2012;32(8): 1608–1613. doi:10.1097/IAE.0b013e3182437e86

35. Pichi F, Lembo A, Morara M, Veronese C, Alkabes M, Nucci P, Ciardella AP. Early and late inner retinal changes after inner limiting membrane peeling. Int Ophthalmol. 2014;34(2): 437–446. doi: 10.1007/s10792-013-9831-6 36.

36. Tadayoni R, Paques M, Massin P, Mouki-Benani S, Mikol J, Gaudric A. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology. 2001;108(12): 2279–2283. doi: 10.1016/s01616420(01)00856-9

37. Mitamura Y, Ohtsuka K. Relationship of dissociated optic nerve fiber layer appearance to internal limiting membrane peeling. Ophthalmology. 2005;112(10): 1766–1770. doi: 10.1016/j.ophtha.2005.04.026

38. Treumer F, Wacker N, Junge O, Hedderich J, Roider J, Hillenkamp J. Foveal structure and thickness of retinal layers long-term after surgical peeling of idiopathic epiretinal membrane. Invest Ophthalmol Vis Sci. 2011;52(2): 744–750. doi:10.1167/iovs.10-6310