Study on complications of internal limiting membrane peeling_West China Medical Journal

Authors：

QIN Ling ,  ZHANG Ming

Department of Ophthalmology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

ZHANG Ming, Email: zhangmingscu@126.com

Keywords：

Internal limiting membrane peeling; Complication; Controversy; Macular hole; Epiretinal membranes

DOI：

10.7507/1002-0179.201810098

Video：

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Internal limiting membrane peeling is now widely used in the treatment of vitreoretinal diseases, such as idiopathic macular hole, epiretinal membrane, macular edema, traumatic retinopathy, retinoschisis, and optic pit, especially macular diseases. Due to the attention paid to the physiological function of the internal limiting membrane, there is still controversies about whether the internal limiting membrane is removed, and the area and the way of the removal in vitrectomy of the above diseases. Major complications have been reported in literature: effects on internal retinal structure, retinal and choroidal blood flow, retinal electrical activity, potential retinal toxicity of stain, changes in the anatomy of macular area, changes in visual field and potential damage to vision. In this paper, we reviewes the complications of internal limiting membrane peeling in the treatment of macular hole and epiretinal macular membrane.

Citation： QIN Ling, ZHANG Ming. Study on complications of internal limiting membrane peeling. West China Medical Journal, 2018, 33(11): 1428-1432. doi: 10.7507/1002-0179.201810098 Copy

1.	Gass JD. Idiopathic senile macular hole. Its early stages and pathogenesis. Arch Ophthalmol, 1988, 106(5): 629-639.
2.	Morris R, Kuhn F, Witherspoon CD. Hemorrhagic macular cysts. Ophthalmology, 1994, 101(1): 1.
3.	方冬. 内界膜剥除方式进展. 中华实验眼科杂志, 2017, 35(11): 1039-1042.
4.	黄艳, 陈为民, 李平华. 220 例玻璃体切割术治疗黄斑前膜的临床疗效观察. 中华眼科医学杂志: 电子版, 2016, 6(2): 81-86.
5.	张承芬, 董方田, 陈有信, 等. 眼底病学. 2版. 北京: 人民卫生出版社, 2013.
6.	王景昭, 葛坚, 赵家良. 视网膜病//葛坚, 赵家良, 崔浩. 眼科学 (八年制). 北京: 人民卫生出版社, 2010: 295-326.
7.	解传奇, 贾亚丁. 内界膜剥除对特发性黄斑裂孔术后裂孔愈合及视功能影响的 Meta 分析. 山西医科大学学报, 2009, 40(2): 183-185.
8.	Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology, 2000, 107(10): 1939-1948.
9.	Kumagai K, Furukawa M, Ogino N, et al. Vitreous surgery with and without internal limiting membrane peeling for macular hole repair. Retina, 2004, 24(5): 721-727.
10.	Tognetto D, Grandin R, Sanguinetti G, et al. Internal limiting membrane removal during macular hole surgery: results of a multicenter retrospective study. Ophthalmology, 2006, 113(8): 1401-1410.
11.	Lois N, Burr J, Norrie J, et al. Internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole: a pragmatic randomized controlled trial. Invest Ophthalmol Vis Sci, 2011, 52(3): 1586-1592.
12.	Masonis J, Thompson C, Odum S. Safe and accurate: learning the direct anterior total hip arthroplasty. Orthopedics, 2008, 31(12 Suppl 2). https://www.ncbi.nlm.nih.gov/pubmed/19298019.
13.	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. 中华眼视光学与视觉科学杂志, 2016, 18(6): 340-346.
14.	Steven P, Laqua H, Wong D, et al. Secondary paracentral retinal holes following internal limiting membrane removal. Br J Ophthalmol, 2006, 90(3): 293-295.
15.	Alkabes M, Salinas C, Vitale L, et al. En face optical coherence tomography of inner retinal defects after internal limiting membrane peeling for idiopathic macular hole. Invest Ophthalmol Vis Sci, 2011, 52(11): 8349-8355.
16.	Tadayoni R, Paques M, Massin P, et al. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology, 2001, 108(12): 2279-2283.
17.	Balducci N, Morara M, Veronese C, et al. Retinal nerve fiber layer thickness modification after internal limiting membrane peeling. Retina, 2014, 34(4): 655-663.
18.	Ohta K, Sato A, Fukui E. Retinal thickness in eyes with idiopathic macular hole after vitrectomy with internal limiting membrane peeling. Graefes Arch Clin Exp Ophthalmol, 2013, 251(5): 1273-1279.
19.	Liu J, Chen Y, Wang S, et al. Evaluating inner retinal dimples after inner limiting membrane removal using multimodal imaging of optical coherence tomography. BMC Ophthalmol, 2018, 18(1): 155.
20.	Baba T, Kakisu M, Nizawa T, et al. Superficial foveal avascular zone determined by optical coherence tomography angiography before and after macular hole surgery. Retina, 2017, 37(3): 444-450.
21.	Kumagai K, Furukawa M, Suetsugu T, et al. Foveal avascular zone area after internal limiting membrane peeling for epiretinal membrane and macular hole compared with that of fellow eyes and healthy controls. Retina, 2018, 38(9): 1786-1794.
22.	Kumagai K, Hangai M, Furukawa M, et al. Centripetal movement of the capillaries in the central macular region after internal limiting membrane peeling. Retina Cases Brief Rep, 2017. doi: 10.1097/ICB.0000000000000526.
23.	Kumagai K, Uemura A, Furukawa M, et al. Decrease of the foveal avascular zone area after internal limiting membrane peeling: single case study. Int Med Case Rep J, 2017, 10: 81-85.
24.	Cho JH, Yi HC, Bae SH, et al. Foveal microvasculature features of surgically closed macular hole using optical coherence tomography angiography. BMC Ophthalmol, 2017, 17(1): 217.
25.	Shahlaee A, Rahimy E, Hsu J, et al. Preoperative and postoperative features of macular holes on en face imaging and optical coherence tomography angiography. Am J Ophthalmol Case Rep, 2016, 5: 20-25.
26.	Nelis P, Alten F, Clemens CR, et al. Quantification of changes in foveal capillary architecture caused by idiopathic epiretinal membrane using OCT angiography. Graefes Arch Clin Exp Ophthalmol, 2017, 255(7): 1319-1324.
27.	Teng Y, Yu M, Wang Y, et al. OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery. Graefes Arch Clin Exp Ophthalmol, 2017, 255(5): 893-902.
28.	Kim YJ, Kim S, Lee JY, et al. Macular capillary plexuses after epiretinal membrane surgery: an optical coherence tomography angiography study. Br J Ophthalmol, 2018, 102(8): 1086-1091.
29.	Haritoglou C, Gass CA, Schaumberger M, et al. Macular changes after peeling of internal limiting membrame in macular hole surgery. Am J Ophthalmol, 2001, 132(3): 363-368.
30.	Terasaki H, Miyake Y, Nomura R, et al. Focual macular ERGs in eyes after removal of macular ILM during macular hole surgery. Invest Ophthalmol Vis Sci, 2001, 42(1): 229-234.
31.	Burk SE, Da Mata AP, Snyder ME, et al. Indocyanine green-assisted peeling of the retinal internal limiting membrane. Ophthalmology, 2000, 107(11): 2010-2014.
32.	Stanescu-Segall D, Jackson TL. Vital staining with indocyanine green: a review of the clinical and experimental studies relating to safety. Eye (Lond), 2009, 23(3): 504-518.
33.	Farah ME, Maia M, Penha FM, et al. The use of vital dyes during vitreoretinal surgery: chromovitrectomy. Dev Ophthalmol, 2016, 55: 365-375.
34.	de Carlo TE, Romano A, Waheed NK, et al. A review of optical coherence tomography angiography (OCTA). Int J Retina Vitreous, 2015, 1: 5.
35.	Zhang M, Wang J, Pechauer AD, et al. Advanced image processing for optical coherence tomographic angiography of macular diseases. Biomed Opt Express, 2015, 6(12): 4661-4675.
36.	Steel D, Chen Y, Latimer J, et al. Does internal limiting membrane peeling size matter?. J Vitreoretinal Dis, 2017, 1(1): 27-31.
37.	Kumagai K, Ogino N, Furukawa M, et al. Early centripetal displacements of capillaries in macular region caused by internal limiting membrane peeling. Clin Ophthalmol, 2018, 12: 755-763.
38.	Tadayoni R, Creuzot-Carcher C, Korobelnik JF, et al. Internal limiting membrame peeling for large macular holes: a randomizied, multicentric and controled clinical trail. Invest Ophthalmol Vis Sci, 2009, 50(13): 5206.
39.	Spaide RF. " Dissociated optic nerve fiber layer appearance” after internal limiting membrane removal is inner retinal dimpling. Retina, 2012, 32(9): 1719-1726.
40.	Michalewska Z, Nawrocki J. Swept-source optical coherence tomography angiography reveals internal limiting membrane peeling alters deep retinal vasculature. Retina, 2018, 38(Suppl 1): S154-S160.
41.	Cho KH, Park SJ, Cho JH, et al. Inner-retinal irregularity index predicts postoperative visual prognosis in idiopathic epiretinal membrane. Am J Ophthalmol, 2016, 168: 139-149.
42.	俞素勤, 李欣馨, 许迅. OCT 血流成像技术的现在与未来. 中华眼视光学与视觉科学杂志, 2017, 19(10): 577-585.

1. Gass JD. Idiopathic senile macular hole. Its early stages and pathogenesis. Arch Ophthalmol, 1988, 106(5): 629-639.
2. Morris R, Kuhn F, Witherspoon CD. Hemorrhagic macular cysts. Ophthalmology, 1994, 101(1): 1.
3. 方冬. 内界膜剥除方式进展. 中华实验眼科杂志, 2017, 35(11): 1039-1042.
4. 黄艳, 陈为民, 李平华. 220 例玻璃体切割术治疗黄斑前膜的临床疗效观察. 中华眼科医学杂志: 电子版, 2016, 6(2): 81-86.
5. 张承芬, 董方田, 陈有信, 等. 眼底病学. 2版. 北京: 人民卫生出版社, 2013.
6. 王景昭, 葛坚, 赵家良. 视网膜病//葛坚, 赵家良, 崔浩. 眼科学 (八年制). 北京: 人民卫生出版社, 2010: 295-326.
7. 解传奇, 贾亚丁. 内界膜剥除对特发性黄斑裂孔术后裂孔愈合及视功能影响的 Meta 分析. 山西医科大学学报, 2009, 40(2): 183-185.
8. Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology, 2000, 107(10): 1939-1948.
9. Kumagai K, Furukawa M, Ogino N, et al. Vitreous surgery with and without internal limiting membrane peeling for macular hole repair. Retina, 2004, 24(5): 721-727.
10. Tognetto D, Grandin R, Sanguinetti G, et al. Internal limiting membrane removal during macular hole surgery: results of a multicenter retrospective study. Ophthalmology, 2006, 113(8): 1401-1410.
11. Lois N, Burr J, Norrie J, et al. Internal limiting membrane peeling versus no peeling for idiopathic full-thickness macular hole: a pragmatic randomized controlled trial. Invest Ophthalmol Vis Sci, 2011, 52(3): 1586-1592.
12. Masonis J, Thompson C, Odum S. Safe and accurate: learning the direct anterior total hip arthroplasty. Orthopedics, 2008, 31(12 Suppl 2). https://www.ncbi.nlm.nih.gov/pubmed/19298019.
13. 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. 中华眼视光学与视觉科学杂志, 2016, 18(6): 340-346.
14. Steven P, Laqua H, Wong D, et al. Secondary paracentral retinal holes following internal limiting membrane removal. Br J Ophthalmol, 2006, 90(3): 293-295.
15. Alkabes M, Salinas C, Vitale L, et al. En face optical coherence tomography of inner retinal defects after internal limiting membrane peeling for idiopathic macular hole. Invest Ophthalmol Vis Sci, 2011, 52(11): 8349-8355.
16. Tadayoni R, Paques M, Massin P, et al. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology, 2001, 108(12): 2279-2283.
17. Balducci N, Morara M, Veronese C, et al. Retinal nerve fiber layer thickness modification after internal limiting membrane peeling. Retina, 2014, 34(4): 655-663.
18. Ohta K, Sato A, Fukui E. Retinal thickness in eyes with idiopathic macular hole after vitrectomy with internal limiting membrane peeling. Graefes Arch Clin Exp Ophthalmol, 2013, 251(5): 1273-1279.
19. Liu J, Chen Y, Wang S, et al. Evaluating inner retinal dimples after inner limiting membrane removal using multimodal imaging of optical coherence tomography. BMC Ophthalmol, 2018, 18(1): 155.
20. Baba T, Kakisu M, Nizawa T, et al. Superficial foveal avascular zone determined by optical coherence tomography angiography before and after macular hole surgery. Retina, 2017, 37(3): 444-450.
21. Kumagai K, Furukawa M, Suetsugu T, et al. Foveal avascular zone area after internal limiting membrane peeling for epiretinal membrane and macular hole compared with that of fellow eyes and healthy controls. Retina, 2018, 38(9): 1786-1794.
22. Kumagai K, Hangai M, Furukawa M, et al. Centripetal movement of the capillaries in the central macular region after internal limiting membrane peeling. Retina Cases Brief Rep, 2017. doi: 10.1097/ICB.0000000000000526.
23. Kumagai K, Uemura A, Furukawa M, et al. Decrease of the foveal avascular zone area after internal limiting membrane peeling: single case study. Int Med Case Rep J, 2017, 10: 81-85.
24. Cho JH, Yi HC, Bae SH, et al. Foveal microvasculature features of surgically closed macular hole using optical coherence tomography angiography. BMC Ophthalmol, 2017, 17(1): 217.
25. Shahlaee A, Rahimy E, Hsu J, et al. Preoperative and postoperative features of macular holes on en face imaging and optical coherence tomography angiography. Am J Ophthalmol Case Rep, 2016, 5: 20-25.
26. Nelis P, Alten F, Clemens CR, et al. Quantification of changes in foveal capillary architecture caused by idiopathic epiretinal membrane using OCT angiography. Graefes Arch Clin Exp Ophthalmol, 2017, 255(7): 1319-1324.
27. Teng Y, Yu M, Wang Y, et al. OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery. Graefes Arch Clin Exp Ophthalmol, 2017, 255(5): 893-902.
28. Kim YJ, Kim S, Lee JY, et al. Macular capillary plexuses after epiretinal membrane surgery: an optical coherence tomography angiography study. Br J Ophthalmol, 2018, 102(8): 1086-1091.
29. Haritoglou C, Gass CA, Schaumberger M, et al. Macular changes after peeling of internal limiting membrame in macular hole surgery. Am J Ophthalmol, 2001, 132(3): 363-368.
30. Terasaki H, Miyake Y, Nomura R, et al. Focual macular ERGs in eyes after removal of macular ILM during macular hole surgery. Invest Ophthalmol Vis Sci, 2001, 42(1): 229-234.
31. Burk SE, Da Mata AP, Snyder ME, et al. Indocyanine green-assisted peeling of the retinal internal limiting membrane. Ophthalmology, 2000, 107(11): 2010-2014.
32. Stanescu-Segall D, Jackson TL. Vital staining with indocyanine green: a review of the clinical and experimental studies relating to safety. Eye (Lond), 2009, 23(3): 504-518.
33. Farah ME, Maia M, Penha FM, et al. The use of vital dyes during vitreoretinal surgery: chromovitrectomy. Dev Ophthalmol, 2016, 55: 365-375.
34. de Carlo TE, Romano A, Waheed NK, et al. A review of optical coherence tomography angiography (OCTA). Int J Retina Vitreous, 2015, 1: 5.
35. Zhang M, Wang J, Pechauer AD, et al. Advanced image processing for optical coherence tomographic angiography of macular diseases. Biomed Opt Express, 2015, 6(12): 4661-4675.
36. Steel D, Chen Y, Latimer J, et al. Does internal limiting membrane peeling size matter?. J Vitreoretinal Dis, 2017, 1(1): 27-31.
37. Kumagai K, Ogino N, Furukawa M, et al. Early centripetal displacements of capillaries in macular region caused by internal limiting membrane peeling. Clin Ophthalmol, 2018, 12: 755-763.
38. Tadayoni R, Creuzot-Carcher C, Korobelnik JF, et al. Internal limiting membrame peeling for large macular holes: a randomizied, multicentric and controled clinical trail. Invest Ophthalmol Vis Sci, 2009, 50(13): 5206.
39. Spaide RF. " Dissociated optic nerve fiber layer appearance” after internal limiting membrane removal is inner retinal dimpling. Retina, 2012, 32(9): 1719-1726.
40. Michalewska Z, Nawrocki J. Swept-source optical coherence tomography angiography reveals internal limiting membrane peeling alters deep retinal vasculature. Retina, 2018, 38(Suppl 1): S154-S160.
41. Cho KH, Park SJ, Cho JH, et al. Inner-retinal irregularity index predicts postoperative visual prognosis in idiopathic epiretinal membrane. Am J Ophthalmol, 2016, 168: 139-149.
42. 俞素勤, 李欣馨, 许迅. OCT 血流成像技术的现在与未来. 中华眼视光学与视觉科学杂志, 2017, 19(10): 577-585.

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