- Eye Hospital of Wenzhou Medical University, Hangzhou 310020, China;
Dissociated optic nerve fiber layer (DONFL) appearance is consists of numerous arcuate dark striae within the posterior pole in the direction of the optic nerve fibers. And on the cross-sectional image, DONFL was correspond to inner retinal dimples. It mainly occurs after the internal limiting membrane (ILM) peeling due to the direct damage on the local retina and the broad tractional effect on the posterior retina during membrane peeling. DONFL appearance is considered to be a spontaneous and delayed morphologic change with a subclinical nature, and appears to have little effect on retinal function. In addition to avoiding the removal of ILM and reducing the area of ILM peeling, a novel technique for reposition of the fixed ILM flap with the assistance of perfluoro-n-octane and the temporal inverted ILM flap technique can also be used to prevent and reduce the occurrence of DONFL appearance. Further studies on its development, clinical features and clinical significance are still required.
Citation: Yu Xueting, Tao Jiwei, Shen Lijun. Research status and progress of dissociated optic nerve fiber layer after internal limiting membrane peeling. Chinese Journal of Ocular Fundus Diseases, 2020, 36(4): 327-332. doi: 10.3760/cma.j.cn511434-20190107-00006 Copy
1. | Chatziralli IP, Theodossiadis PG, Steel DHW. Internal limiting membrane peeling in macular hole surgery; why, when, and how?[J]. Retina, 2018, 38(5): 870-882. DOI: 10.1097/IAE.0000000000001959. |
2. | Pichi F, Lembo A, Morara M, et al. Early and late inner retinal changes after inner limiting membrane peeling[J]. Int Ophthalmol, 2014, 34(2): 437-446. DOI: 10.1007/s10792-013-9831-6. |
3. | Tadayoni R, Paques M, Massin P, et al. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal[J]. Ophthalmology, 2001, 108(12): 2279-2283. DOI: 10.1016/s0161-6420(01)00856-9. |
4. | Miura M, Elsner AE, Osako M, et al. Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular hole[J]. Retina, 2003, 23(4): 561-563. DOI: 10.1097/00006982-200308000-00024. |
5. | Machida S, Fujiwara T, Gotoh T, et al. Observation of the ocular fundus by an infrared-sensitive video camera after vitreoretinal surgery assisted by indocyanine green[J]. Retina, 2003, 23(2): 183-191. DOI: 10.1097/00006982-200304000-00008. |
6. | Mitamura Y, Ohtsuka K. Relationship of dissociated optic nerve fiber layer appearance to internal limiting membrane peeling[J]. Ophthalmology, 2005, 112(10): 1766-1770. DOI: 10.1016/j.ophtha.2005.04.026. |
7. | 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[J]. Invest Ophthalmol Vis Sci, 2011, 52(11): 8349-8355. DOI: 10.1167/iovs.11-8043. |
8. | Spaide RF. “Dissociated optic nerve fiber layer appearance” after internal limiting membrane removal is inner retinal dimpling[J]. Retina, 2012, 32(9): 1719-1726. DOI: 10.1097/IAE.0b013e3182671191. |
9. | Kishimoto H, Kusuhara S, Matsumiya W, et al. Retinal surface imaging provided by cirrus high-definition optical coherence tomography prominently visualizes a dissociated optic nerve fiber layer appearance after macular hole surgery[J]. Int Ophthalmol, 2011, 31(5): 385-392. DOI: 10.1007/s10792-011-9474-4. |
10. | Hisatomi T, Tachibana T, Notomi S, et al. Internal limiting membrane peeling-dependent retinal structural changes after vitrectomy in rhegmatogenous retinal detachment[J]. Retina, 2018, 38(3): 471-479. DOI: 10.1097/IAE.0000000000001558. |
11. | Runkle AP, Srivastava SK, Yuan A, et al. Factors associated with development of dissociated optic nerve fiber layer appearance in the pioneer intraoperative optical coherence tomography study[J]. Retina, 2018, 38(Suppl 1): S103-109. DOI: 10.1097/IAE.0000000000002017. |
12. | Kim KY, Yu SY, Kim M, et al. Morphological change of inner retinal layer on spectral-domain optical coherence tomography following macular hole surgery[J]. Ophthalmologica, 2013, 230(1): 18-26. DOI: 10.1159/000350552. |
13. | Sakimoto S, Ikuno Y, Fujimoto S, et al. Characteristics of the retinal surface after internal limiting membrane peeling in highly myopic eyes[J]. Am J Ophthalmol, 2014, 158(4): 762-768. DOI: 10.1016/j.ajo.2014.06.024. |
14. | Ito Y, Terasaki H, Takahashi A, et al. Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular holes[J]. Ophthalmology, 2005, 112(8): 1415-1420. DOI: 10.1016/j.ophtha.2005.02.023. |
15. | Kim YJ, Lee KS, Joe SG, et al. Incidence and quantitative analysis of dissociated optic nerve fiber layer appearance: real loss of retinal nerve fiber layer?[J]. Eur J Ophthalmol, 2018, 28(3): 317-323. DOI: 10.5301/ejo.5001067. |
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17. | Imai H, Ohta K. Microperimetric determination of retinal sensitivity in areas of dissociated optic nerve fiber layer following internal limiting membrane peeling[J]. Jpn J Ophthalmol, 2010, 54(5): 435-440. DOI: 10.1007/s10384-010-0839-4. |
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19. | Kusuhara S, Matsumiya W, Imai H, et al. Evaluating dissociated optic nerve fiber layer appearance using en face layer imaging produced by optical coherence tomography[J]. Ophthalmologica, 2014, 232(3): 170-178. DOI: 10.1159/000364811. |
20. | Park SH, Kim YJ, Lee SJ. Incidence of and risk factors for dissociated optic nerve fiber layer after epiretinal membrane surgery[J]. Retina, 2016, 36(8): 1469-1473. DOI: 10.1097/IAE.0000000000000949. |
21. | Mazit C, Scholtes F, Rabaut C, et al. Assessment of macular profile using optical coherence tomography after epiretinal membrane surgery[J]. J Fr Ophtalmol, 2008, 31(7): 667-672. DOI: 10.1016/s0181-5512(08)74380-8. |
22. | Olenik A, Rios J, Mateo C. Inverted internal limiting membrane flap technique for macular holes in high myopia with axial length ≥30 mm[J]. Retina, 2016, 36(9): 1688-1693. DOI: 10.1097/IAE.0000000000001010. |
23. | Kumar V. Dissociated optic nerve fiber layer in subinternal limiting membrane hemorrhage[J]. Ophthalmology, 2017, 124(6): 872. DOI: 10.1016/j.ophtha.2016.12.014. |
24. | Foos RY. Vitreoretinal juncture; topographical variations[J]. Invest Ophthalmol, 1972, 11(10): 801-808. |
25. | Mester V, Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes[J]. Am J Ophthalmol, 2000, 129(6): 769-777. DOI: 10.1016/s0002-9394(00)00358-5. |
26. | Mittleman D, Green WR, Michels RG, et al. Clinicopathologic correlation of an eye after surgical removal of an epiretinal membrane[J]. Retina, 1989, 9(2): 143-147. DOI: 10.1097/00006982-198909020-00015. |
27. | Henrich PB, Monnier CA, Halfter W, et al. Nanoscale topographic and biomechanical studies of the human internal limiting membrane[J]. Invest Ophthalmol Vis Sci, 2012, 53(6): 2561-2570. DOI: 10.1167/iovs.11-8502. |
28. | Mitamura Y, Suzuki T, Kinoshita T, et al. Optical coherence tomographic findings of dissociated optic nerve fiber layer appearance[J]. Am J Ophthalmol, 2004, 137(6): 1155-1156. DOI: 10.1016/j.ajo.2004.01.052. |
29. | Steel DH, Dinah C, Habib M, et al. ILM peeling technique influences the degree of a dissociated optic nerve fibre layer appearance after macular hole surgery[J]. Graefe's Arch Clin Exp Ophthalmol, 2015, 253(5): 691-698. DOI: 10.1007/s00417-014-2734-z. |
30. | Haritoglou C, Gandorfer A, Kampik A. NFL appearance after peeling[J]. Ophthalmology, 2006, 113(9): 1690-1691. DOI: 10.1016/j.ophtha.2006.01.020. |
31. | Demirel S, Abdullayev A, Yanik O, et al. Evaluation of ganglion cell-inner plexiform layer thickness after vitreoretinal surgery with internal limiting membrane peeling in cases with idiopathic macular hole[J]. Turk J Ophthalmol, 2017, 47(3): 138-143. DOI: 10.4274/tjo.34545. |
32. | Sabry D, El-Kannishy A, Kamel R, et al. Correlation between en face optical coherence tomography defects of the inner retinal layers and ganglion cell inner plexiform layer analysis after internal limiting membrane peeling for idiopathic full-thickness macular hole[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 444-450. DOI: 10.1167/iovs.15-18043. |
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34. | Newman EA. Regional specialization of retinal glial cell membrane[J]. Nature, 1984, 309(5964): 155-157. DOI: 10.1038/309155a0. |
35. | Amouyal F, Shah SU, Pan CK, et al. Morphologic features and evolution of inner retinal dimples on optical coherence tomography after internal limiting membrane peeling[J]. Retina, 2014, 34(10): 2096-2102. DOI: 10.1097/IAE.0000000000000193. |
36. | Holländer H, Makarov F, Dreher Z, et al. Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Muller cells[J]. J Comp Neurol, 1991, 313(4): 587-603. DOI: 10.1002/cne.903130405. |
37. | Sebag J. Age-related differences in the human vitreoretinal interface[J]. Arch Ophthalmol, 1991, 109(7): 966-971. DOI: 10.1001/archopht.1991.01080070078039. |
38. | Wolf S, Schnurbusch U, Wiedemann P, et al. Peeling of the basal membrane in the human retina: ultrastructural effects[J]. Ophthalmology, 2004, 111(2): 238-243. DOI: 10.1016/j.ophtha.2003.05.022. |
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40. | Gandorfer A, Haritoglou C, Kampik A, et al. Ultrastructure of the vitreoretinal interface following removal of the internal limiting membrane using indocyanine green[J]. Curr Eye Res, 2004, 29(4-5): 319-320. DOI: 10.1080/02713680490515964. |
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- 1. Chatziralli IP, Theodossiadis PG, Steel DHW. Internal limiting membrane peeling in macular hole surgery; why, when, and how?[J]. Retina, 2018, 38(5): 870-882. DOI: 10.1097/IAE.0000000000001959.
- 2. Pichi F, Lembo A, Morara M, et al. Early and late inner retinal changes after inner limiting membrane peeling[J]. Int Ophthalmol, 2014, 34(2): 437-446. DOI: 10.1007/s10792-013-9831-6.
- 3. Tadayoni R, Paques M, Massin P, et al. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal[J]. Ophthalmology, 2001, 108(12): 2279-2283. DOI: 10.1016/s0161-6420(01)00856-9.
- 4. Miura M, Elsner AE, Osako M, et al. Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular hole[J]. Retina, 2003, 23(4): 561-563. DOI: 10.1097/00006982-200308000-00024.
- 5. Machida S, Fujiwara T, Gotoh T, et al. Observation of the ocular fundus by an infrared-sensitive video camera after vitreoretinal surgery assisted by indocyanine green[J]. Retina, 2003, 23(2): 183-191. DOI: 10.1097/00006982-200304000-00008.
- 6. Mitamura Y, Ohtsuka K. Relationship of dissociated optic nerve fiber layer appearance to internal limiting membrane peeling[J]. Ophthalmology, 2005, 112(10): 1766-1770. DOI: 10.1016/j.ophtha.2005.04.026.
- 7. 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[J]. Invest Ophthalmol Vis Sci, 2011, 52(11): 8349-8355. DOI: 10.1167/iovs.11-8043.
- 8. Spaide RF. “Dissociated optic nerve fiber layer appearance” after internal limiting membrane removal is inner retinal dimpling[J]. Retina, 2012, 32(9): 1719-1726. DOI: 10.1097/IAE.0b013e3182671191.
- 9. Kishimoto H, Kusuhara S, Matsumiya W, et al. Retinal surface imaging provided by cirrus high-definition optical coherence tomography prominently visualizes a dissociated optic nerve fiber layer appearance after macular hole surgery[J]. Int Ophthalmol, 2011, 31(5): 385-392. DOI: 10.1007/s10792-011-9474-4.
- 10. Hisatomi T, Tachibana T, Notomi S, et al. Internal limiting membrane peeling-dependent retinal structural changes after vitrectomy in rhegmatogenous retinal detachment[J]. Retina, 2018, 38(3): 471-479. DOI: 10.1097/IAE.0000000000001558.
- 11. Runkle AP, Srivastava SK, Yuan A, et al. Factors associated with development of dissociated optic nerve fiber layer appearance in the pioneer intraoperative optical coherence tomography study[J]. Retina, 2018, 38(Suppl 1): S103-109. DOI: 10.1097/IAE.0000000000002017.
- 12. Kim KY, Yu SY, Kim M, et al. Morphological change of inner retinal layer on spectral-domain optical coherence tomography following macular hole surgery[J]. Ophthalmologica, 2013, 230(1): 18-26. DOI: 10.1159/000350552.
- 13. Sakimoto S, Ikuno Y, Fujimoto S, et al. Characteristics of the retinal surface after internal limiting membrane peeling in highly myopic eyes[J]. Am J Ophthalmol, 2014, 158(4): 762-768. DOI: 10.1016/j.ajo.2014.06.024.
- 14. Ito Y, Terasaki H, Takahashi A, et al. Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular holes[J]. Ophthalmology, 2005, 112(8): 1415-1420. DOI: 10.1016/j.ophtha.2005.02.023.
- 15. Kim YJ, Lee KS, Joe SG, et al. Incidence and quantitative analysis of dissociated optic nerve fiber layer appearance: real loss of retinal nerve fiber layer?[J]. Eur J Ophthalmol, 2018, 28(3): 317-323. DOI: 10.5301/ejo.5001067.
- 16. Nukada K, Hangai M, Ooto S, et al. Tomographic features of macula after successful macular hole surgery[J]. Invest Ophthalmol Vis Sci, 2013, 54(4): 2417-2428. DOI: 10.1167/iovs.12-10838.
- 17. Imai H, Ohta K. Microperimetric determination of retinal sensitivity in areas of dissociated optic nerve fiber layer following internal limiting membrane peeling[J]. Jpn J Ophthalmol, 2010, 54(5): 435-440. DOI: 10.1007/s10384-010-0839-4.
- 18. Steel DH, Dinah C, White K, et al. The relationship between a dissociated optic nerve fibre layer appearance after macular hole surgery and Muller cell debris on peeled internal limiting membrane[J]. Acta Ophthalmol, 2017, 95(2): 153-157. DOI: 10.1111/aos.13195.
- 19. Kusuhara S, Matsumiya W, Imai H, et al. Evaluating dissociated optic nerve fiber layer appearance using en face layer imaging produced by optical coherence tomography[J]. Ophthalmologica, 2014, 232(3): 170-178. DOI: 10.1159/000364811.
- 20. Park SH, Kim YJ, Lee SJ. Incidence of and risk factors for dissociated optic nerve fiber layer after epiretinal membrane surgery[J]. Retina, 2016, 36(8): 1469-1473. DOI: 10.1097/IAE.0000000000000949.
- 21. Mazit C, Scholtes F, Rabaut C, et al. Assessment of macular profile using optical coherence tomography after epiretinal membrane surgery[J]. J Fr Ophtalmol, 2008, 31(7): 667-672. DOI: 10.1016/s0181-5512(08)74380-8.
- 22. Olenik A, Rios J, Mateo C. Inverted internal limiting membrane flap technique for macular holes in high myopia with axial length ≥30 mm[J]. Retina, 2016, 36(9): 1688-1693. DOI: 10.1097/IAE.0000000000001010.
- 23. Kumar V. Dissociated optic nerve fiber layer in subinternal limiting membrane hemorrhage[J]. Ophthalmology, 2017, 124(6): 872. DOI: 10.1016/j.ophtha.2016.12.014.
- 24. Foos RY. Vitreoretinal juncture; topographical variations[J]. Invest Ophthalmol, 1972, 11(10): 801-808.
- 25. Mester V, Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes[J]. Am J Ophthalmol, 2000, 129(6): 769-777. DOI: 10.1016/s0002-9394(00)00358-5.
- 26. Mittleman D, Green WR, Michels RG, et al. Clinicopathologic correlation of an eye after surgical removal of an epiretinal membrane[J]. Retina, 1989, 9(2): 143-147. DOI: 10.1097/00006982-198909020-00015.
- 27. Henrich PB, Monnier CA, Halfter W, et al. Nanoscale topographic and biomechanical studies of the human internal limiting membrane[J]. Invest Ophthalmol Vis Sci, 2012, 53(6): 2561-2570. DOI: 10.1167/iovs.11-8502.
- 28. Mitamura Y, Suzuki T, Kinoshita T, et al. Optical coherence tomographic findings of dissociated optic nerve fiber layer appearance[J]. Am J Ophthalmol, 2004, 137(6): 1155-1156. DOI: 10.1016/j.ajo.2004.01.052.
- 29. Steel DH, Dinah C, Habib M, et al. ILM peeling technique influences the degree of a dissociated optic nerve fibre layer appearance after macular hole surgery[J]. Graefe's Arch Clin Exp Ophthalmol, 2015, 253(5): 691-698. DOI: 10.1007/s00417-014-2734-z.
- 30. Haritoglou C, Gandorfer A, Kampik A. NFL appearance after peeling[J]. Ophthalmology, 2006, 113(9): 1690-1691. DOI: 10.1016/j.ophtha.2006.01.020.
- 31. Demirel S, Abdullayev A, Yanik O, et al. Evaluation of ganglion cell-inner plexiform layer thickness after vitreoretinal surgery with internal limiting membrane peeling in cases with idiopathic macular hole[J]. Turk J Ophthalmol, 2017, 47(3): 138-143. DOI: 10.4274/tjo.34545.
- 32. Sabry D, El-Kannishy A, Kamel R, et al. Correlation between en face optical coherence tomography defects of the inner retinal layers and ganglion cell inner plexiform layer analysis after internal limiting membrane peeling for idiopathic full-thickness macular hole[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 444-450. DOI: 10.1167/iovs.15-18043.
- 33. Baba T, Yamamoto S, Kimoto R, et al. Reduction of thickness of ganglion cell complex after internal limiting membrane peeling during vitrectomy for idiopathic macular hole[J]. Eye, 2012, 26(9): 1173-1180. DOI: 10.1038/eye.2012.170.
- 34. Newman EA. Regional specialization of retinal glial cell membrane[J]. Nature, 1984, 309(5964): 155-157. DOI: 10.1038/309155a0.
- 35. Amouyal F, Shah SU, Pan CK, et al. Morphologic features and evolution of inner retinal dimples on optical coherence tomography after internal limiting membrane peeling[J]. Retina, 2014, 34(10): 2096-2102. DOI: 10.1097/IAE.0000000000000193.
- 36. Holländer H, Makarov F, Dreher Z, et al. Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Muller cells[J]. J Comp Neurol, 1991, 313(4): 587-603. DOI: 10.1002/cne.903130405.
- 37. Sebag J. Age-related differences in the human vitreoretinal interface[J]. Arch Ophthalmol, 1991, 109(7): 966-971. DOI: 10.1001/archopht.1991.01080070078039.
- 38. Wolf S, Schnurbusch U, Wiedemann P, et al. Peeling of the basal membrane in the human retina: ultrastructural effects[J]. Ophthalmology, 2004, 111(2): 238-243. DOI: 10.1016/j.ophtha.2003.05.022.
- 39. Brazitikos PD, Katsimpris JM, Tsironi E, et al. Retinal nerve fiber layer thickness evaluation after trypan blue-assisted macular surgery[J]. Retina, 2010, 30(4): 640-647. DOI: 10.1097/IAE.0b013e3181c085ab.
- 40. Gandorfer A, Haritoglou C, Kampik A, et al. Ultrastructure of the vitreoretinal interface following removal of the internal limiting membrane using indocyanine green[J]. Curr Eye Res, 2004, 29(4-5): 319-320. DOI: 10.1080/02713680490515964.
- 41. Nakamura T, Murata T, Hisatomi T, et al. Ultrastructure of the vitreoretinal interface following the removal of the internal limiting membrane using indocyanine green[J]. Curr Eye Res, 2003, 27(6): 395-399. DOI: 10.1076/ceyr.27.6.395.18189.
- 42. Bringmann A, Pannicke T, Grosche J, et al. Muller cells in the healthy and diseased retina[J]. Pro Reti Eye Res, 2006, 25(4): 397-424. DOI: 10.1016/j.preteyeres.2006.05.003.
- 43. Konstantinidis L, Uffer S, Bovey EH. Ultrastructural changes of the internal limiting membrane removed during indocyanine green assisted peeling versus conventional surgery for idiopathic macular epiretinal membrane[J]. Retina, 2009, 29(3): 380-386. DOI: 10.1097/IAE.0b013e31818eccdb.
- 44. Brockmann T, Steger C, Westermann M, et al. Ultrastructure of the membrana limitans interna after dye-assisted membrane peeling[J]. Ophthalmologica, 2011, 226(4): 228-233. DOI: 10.1159/000331218.
- 45. Schumann RG, Gandorfer A, Priglinger SG, et al. Vital dyes for macular surgery: a comparative electron microscopy study of the internal limiting membrane[J]. Retina, 2009, 29(5): 669. DOI: 10.1097/IAE.0b013e318196b1c8.
- 46. Yamashita T, Uemura A, Kita H, et al. Analysis of the retinal nerve fiber layer after indocyanine green-assisted vitrectomy for idiopathic macular holes[J]. Ophthalmology, 2006, 113(2): 280-284. DOI: 10.1016/j.ophtha.2005.10.046.
- 47. Iriyama A, Uchida S, Yanagi Y, et al. Effects of indocyanine green on retinal ganglion cells[J]. Invest Ophthalmol Vis Sci, 2004, 45(3): 943-947. DOI: 10.1167/iovs.03-1026.
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