TECHNIQUES, RATIONALE, AND OUTCOMES OF INTERNAL LIMITING MEMBRANE PEELING

Background: The internal limiting membrane represents the structural interface between the retina and the vitreous and has been postulated to serve several essential functions. Recently, internal limiting membrane peeling has been used in the treatment of a variety of retinal disorders. We review the history, techniques, rationale, and outcomes of internal limiting membrane peeling. Methods: A review of the literature. Results: Internal limiting membrane peeling has been used to successfully treat a variety of retinal disorders including macular hole, epiretinal membrane, diabetic macular edema, retinal vein occlusion, and others. Conclusion: Internal limiting membrane peeling may serve as an important component in the armamentarium of retinal surgery.

[1]  S. Radloff,et al.  Infracyanine-assisted internal limiting membrane peeling in macular hole repair: Does it make a difference? , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[2]  H. Flynn,et al.  PARS PLANA VITRECTOMY WITH INTERNAL LIMITING MEMBRANE PEELING FOR DIABETIC MACULAR EDEMA , 2008, Retina.

[3]  S. Taylor,et al.  The effect of indocyanine-green on functional outcome of macular pucker surgery. , 2003, American journal of ophthalmology.

[4]  A. Kwok,et al.  Treatment of epiretinal membrane: an update. , 2005, Hong Kong medical journal = Xianggang yi xue za zhi.

[5]  F Becquet,et al.  [Efficiency of surgical treatment for chronic macular edema due to branch retinal vein occlusion]. , 2003, Journal francais d'ophtalmologie.

[6]  F. Kuhn,et al.  Internal limiting membrane removal in the management of full-thickness macular holes. , 2000, American journal of ophthalmology.

[7]  F. Kuhn,et al.  Hemorrhagic macular cysts. , 1994, Ophthalmology.

[8]  Eberhard Spoerl,et al.  Biomechanical characteristics of retina. , 2004, Retina.

[9]  T. Lai,et al.  Indocyanine green-assisted internal limiting membrane removal in epiretinal membrane surgery: a clinical and histologic study. , 2004, American journal of ophthalmology.

[10]  J Castro Navarro,et al.  [Macular hole surgery with and without internal limiting membrane peeling]. , 2003, Archivos de la Sociedad Espanola de Oftalmologia.

[11]  Shuichi Yamamoto,et al.  Efficacy of Vitrectomy and Internal Limiting Membrane Removal for Macular Edema Associated with Branch Retinal Vein Occlusion , 2009, Ophthalmologica.

[12]  H. Brooks,et al.  Macular hole surgery with and without internal limiting membrane peeling. , 2000, Ophthalmology.

[13]  P. Walter,et al.  Visual outcome of patients with macular edema after pars plana vitrectomy and indocyanine green-assisted peeling of the internal limiting membrane , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[14]  A. Kampik,et al.  Macular changes after peeling of the internal limiting membrane in macular hole surgery. , 2001, American journal of ophthalmology.

[15]  F. Shiraga,et al.  MACULAR HOLE SURGERY WITH TRIAMCINOLONE ACETONIDE–ASSISTED INTERNAL LIMITING MEMBRANE PEELING: One-Year Results , 2008, Retina.

[16]  Natural history and clinical management of central retinal vein occlusion. The Central Vein Occlusion Study Group. , 1997, Archives of ophthalmology.

[17]  J. Dušková,et al.  Morphometry of surgically removed internal limiting membrane during vitrectomy in diabetic macular edema , 2009, Graefe's Archive for Clinical and Experimental Ophthalmology.

[18]  M. Kondo,et al.  Selective amplitude reduction of the PhNR after macular hole surgery: ganglion cell damage related to ICG-assisted ILM peeling and gas tamponade. , 2006, Investigative ophthalmology & visual science.

[19]  G. Shah,et al.  MACULAR HOLE CLOSURE WITH TRIAMCINOLONE-ASSISTED INTERNAL LIMITING MEMBRANE PEELING , 2008, Retina.

[20]  D. Lam,et al.  Macular hole surgery with and without indocyanine green assistance , 2005, Eye.

[21]  T. Shiba,et al.  Comparison of surgical procedures for vitreous surgery in diabetic macular edema , 2009, Japanese Journal of Ophthalmology.

[22]  A. Ruby,et al.  Pars plana vitrectomy with removal of the internal limiting membrane in the treatment of persistent diabetic macular edema. , 2005, American journal of ophthalmology.

[23]  T. Lai,et al.  Epiretinal membrane surgery with or without internal limiting membrane peeling , 2005, Clinical & experimental ophthalmology.

[24]  C. Bunce,et al.  A randomised controlled feasibility trial of vitrectomy versus laser for diabetic macular oedema , 2004, British Journal of Ophthalmology.

[25]  M. Sasoh,et al.  Triamcinolone acetonide remaining on the fovea after successful macular hole closure. , 2007, Retina.

[26]  P. Hasler,et al.  Early foveal recovery after macular hole surgery , 2008, British Journal of Ophthalmology.

[27]  F. Bandello,et al.  Idiopathic macular hole surgery with low-concentration infracyanine green-assisted peeling of the internal limiting membrane. , 2006, American journal of ophthalmology.

[28]  J. Sipperley,et al.  Macular hole surgery with internal-limiting membrane peeling and intravitreous air. , 1999, Ophthalmology.

[29]  S. Binder,et al.  Vitrectomy for persistent diffuse diabetic macular edema. , 2005, American journal of ophthalmology.

[30]  Y. Mizutani,et al.  Double staining with brilliant blue G and double peeling for epiretinal membranes. , 2009, Ophthalmology.

[31]  M. Perrier,et al.  Trypan internetadvance publication at ajo.com Dec 11, 2002. Blue–assisted peeling of the internal limiting membrane during macular hole surgery , 2003 .

[32]  W. Green,et al.  CLINICOPATHOLOGIC CORRELATION OF AN EPIRETINAL MEMBRANE ASSOCIATED WITH A RECURRENT MACULAR HOLE , 1995, Retina.

[33]  U. Mester,et al.  Results of surgery for epiretinal membranes and their recurrences. , 1996, The British journal of ophthalmology.

[34]  C. Eckardt,et al.  Entfernung der Membrana limitans interna bei Makulalöchern Klinische und morphologische Befunde * , 1997, Der Ophthalmologe.

[35]  Noemi Lois,et al.  Internal limiting membrane peeling in vitreo-retinal surgery. , 2008, Survey of ophthalmology.

[36]  Y. Tsao,et al.  Surgical removal of the internal limiting membrane for the treatment of a macular hole. , 2002, Chang Gung medical journal.

[37]  George A. Williams,et al.  ANATOMICAL AND VISUAL OUTCOMES OF IDIOPATHIC MACULAR HOLE SURGERY WITH INTERNAL LIMITING MEMBRANE REMOVAL USING LOW-CONCENTRATION INDOCYANINE GREEN , 2007, Retina.

[38]  M. Mandelcorn,et al.  INTERNAL LIMITING MEMBRANE PEELING FOR DECOMPRESSION OF MACULAR EDEMA IN RETINAL VEIN OCCLUSION: A REPORT OF 14 CASES , 2004, Retina.

[39]  G. Peyman,et al.  TRIAMCINOLONE ACETONIDE AS AN AID TO VISUALIZATION OF THE VITREOUS AND THE POSTERIOR HYALOID DURING PARS PLANA VITRECTOMY , 2000, Retina.

[40]  S. Uffer,et al.  SURGERY FOR EPIMACULAR MEMBRANE: Impact of Retinal Internal Limiting Membrane Removal on Functional Outcome , 2004, Retina.

[41]  S. Kachi,et al.  Triamcinolone-Assisted Removal of Internal Limiting Membrane Enhances the Effect of Vitrectomy for Diabetic Macular Edema , 2009, Ophthalmic Research.

[42]  S. Priglinger,et al.  Functional outcome after trypan blue-assisted vitrectomy for macular pucker: a prospective, randomized, comparative trial. , 2004, American journal of ophthalmology.

[43]  M. Kraushar,et al.  Retina and Vitreous , 2008 .

[44]  G. Rebolleda,et al.  Trypan blue staining in vitreoretinal surgery. , 2004, Ophthalmology.

[45]  A. Uemura,et al.  LONG-TERM OUTCOMES OF INTERNAL LIMITING MEMBRANE PEELING WITH AND WITHOUT INDOCYANINE GREEN IN MACULAR HOLE SURGERY , 2006, Retina.

[46]  Sanjay Sharma,et al.  Pars plana vitrectomy with internal limiting membranectomy for refractory diabetic macular edema without a taut posterior hyaloid , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[47]  E. Çelik,et al.  LONG-TERM OUTCOMES OF PARS PLANA VITRECTOMY WITH INTERNAL LIMITING MEMBRANE REMOVAL IN DIABETIC MACULAR EDEMA , 2007, Retina.

[48]  Y. Bardak,et al.  Comparison of ICG-assisted ILM peeling and triamcinolone-assisted posterior vitreous removal in diffuse diabetic macular oedema , 2006, Eye.

[49]  Atul Kumar,et al.  Comparative evaluation of vitrectomy and dye-enhanced ILM peel with grid laser in diffuse diabetic macular edema , 2007, Graefe's Archive for Clinical and Experimental Ophthalmology.

[50]  Chloe Gottlieb,et al.  Phacovitrectomy with internal limiting membrane peeling for idiopathic macular hole. , 2002, Canadian journal of ophthalmology. Journal canadien d'ophtalmologie.

[51]  W. Feuer,et al.  Internal limiting membrane peeling in macular hole surgery. , 2001, Ophthalmology.

[52]  M. Figueroa,et al.  SURGICAL AND ANATOMICAL OUTCOMES OF PARS PLANA VITRECTOMY FOR DIFFUSE NONTRACTIONAL DIABETIC MACULAR EDEMA , 2008, Retina.

[53]  MORTON E. Smith,et al.  Internal limiting membrane peeling using triamcinolone acetonide: histopathologic confirmation. , 2004, American journal of ophthalmology.

[54]  R E Foster,et al.  Indocyanine green-assisted peeling of the retinal internal limiting membrane. , 2000, Ophthalmology.

[55]  G. Ravalico,et al.  Internal limiting membrane removal during macular hole surgery: results of a multicenter retrospective study. , 2006, Ophthalmology.

[56]  Eberhard Spoerl,et al.  BIOMECHANICAL SIGNIFICANCE OF THE HUMAN INTERNAL LIMITING LAMINA , 2006, Retina.

[57]  K. Emi,et al.  [Long-term prognosis of internal limiting membrane peeling for idiopathic epiretinal membrane]. , 2004, Nippon Ganka Gakkai zasshi.

[58]  Jay L. Federman,et al.  RETINA AND VITREOUS , 2018, Constable & Lim Colour Atlas of Ophthalmology.

[59]  Jin Ma,et al.  25-Gauge Vitrectomy and Triamcinolone Acetonide–Assisted Internal Limiting Membrane Peeling for Chronic Cystoid Macular Edema Associated With Branch Retinal Vein Occlusion , 2008, Retina.

[60]  R. H. Rosa,et al.  Indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for macular hole repair. , 2001, Ophthalmology.

[61]  S. Uffer,et al.  TEARING AND FOLDING OF THE RETINAL INTERNAL LIMITING MEMBRANE ASSOCIATED WITH MACULAR EPIRETINAL MEMBRANE , 2008, Retina.

[62]  H. Yamashita,et al.  Vitrectomy for Diabetic Macular Edema with and without Internal Limiting Membrane Removal , 2005, Ophthalmologica.

[63]  P. Dillinger,et al.  Vitrectomy with removal of the internal limiting membrane in chronic diabetic macular oedema , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[64]  F. Kuhn,et al.  Vitrectomy with internal limiting membrane removal for clinically significant macular oedema , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[65]  W. Halfter,et al.  Basement membrane-dependent survival of retinal ganglion cells. , 2005, Investigative ophthalmology & visual science.

[66]  Y. Hata,et al.  EVALUATING ADJUNCTIVE SURGICAL PROCEDURES DURING VITRECTOMY FOR DIABETIC MACULAR EDEMA , 2006, Retina.

[67]  J. Duker,et al.  Late re-opening of macular holes after initially successful treatment with vitreous surgery. , 1994, Ophthalmology.

[68]  M. Blumenkranz,et al.  Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction. , 1992, Ophthalmology.

[69]  A. Kampik,et al.  Indocyanine green selectively stains the internal limiting membrane. , 2001, American journal of ophthalmology.

[70]  H. Flynn,et al.  Vitrectomy for diabetic macular edema associated with a thickened and taut posterior hyaloid membrane. , 1996, American journal of ophthalmology.

[71]  G. Shah,et al.  LONG-TERM FOLLOW-UP RESULTS OF ILM PEELING DURING VITRECTOMY SURGERY FOR PREMACULAR FIBROSIS , 2008, Retina.

[72]  Z. Gregor,et al.  Macular holes: vitreoretinal relationships and surgical approaches , 2008, Eye.

[73]  F. Kuhn,et al.  Terson syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. , 1998, Ophthalmology.

[74]  J. Sipperley,et al.  Macular pucker removal with and without internal limiting membrane peeling: pilot study. , 2003, Ophthalmology.

[75]  T. Lai,et al.  Idiopathic macular hole surgery in Chinese patients: a randomised study to compare indocyanine green-assisted internal limiting membrane peeling with no internal limiting membrane peeling. , 2005, Hong Kong medical journal = Xianggang yi xue za zhi.

[76]  O. Gelisken,et al.  Pars plana vitrectomy and removal of the internal limiting membrane in the treatment of chronic macular oedema , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[77]  W. Green,et al.  CLINICOPATHOLOGIC STUDY OF BILATERAL MACULAR HOLES TREATED WITH PARS PLANA VITRECTOMY AND GAS TAMPONADE , 1992, Retina.

[78]  C. Eckardt,et al.  [Removal of the internal limiting membrane in macular holes. Clinical and morphological findings]. , 1997, Der Ophthalmologe : Zeitschrift der Deutschen Ophthalmologischen Gesellschaft.

[79]  T. Kitaoka,et al.  Visual field defects after macular hole surgery with indocyanine green-assisted internal limiting membrane peeling. , 2007, American journal of ophthalmology.

[80]  Y. Sharma,et al.  Modified grid laser photocoagulation versus pars plana vitrectomy with internal limiting membrane removal in diabetic macular edema. , 2005, American journal of ophthalmology.

[81]  B. S. Fine.  Limiting membranes of the sensory retina and pigment epithelium. An electron microscopic study. , 1961, Archives of ophthalmology.

[82]  T. Hikichi,et al.  Association between the short-term natural history of diabetic macular edema and the vitreomacular relationship in type II diabetes mellitus. , 1997, Ophthalmology.

[83]  M. Sebag,et al.  Trypan blue-assisted peeling of the internal limiting membrane during macular hole surgery. , 2003, American journal of ophthalmology.

[84]  K. Noda,et al.  Surgical effects and complications of indocyanine green-assisted internal limiting membrane peeling for idiopathic macular hole. , 2007, Acta ophthalmologica.

[85]  S. Song,et al.  Arteriovenous Sheathotomy for Persistent Macular Edema in Branch Retinal Vein Occlusion , 2006, Korean Journal of Ophthalmology.

[86]  F. Bandello,et al.  Idiopathic macular hole surgery with low-concentration infracyanine green-assisted peeling of the internal limiting membrane. , 2006, American journal of ophthalmology.

[87]  G. Hutchins,et al.  CENTRAL RETINAL VEIN OCCLUSION: A Prospective Histopathologic Study of 29 Eyes in 28 Cases , 2005, Retina.

[88]  T. Williamson,et al.  Outcomes of macular hole surgery: implications for surgical management and clinical governance , 2005, Eye.

[89]  Stanislao Rizzo,et al.  25-gauge, sutureless vitrectomy and standard 20-gauge pars plana vitrectomy in idiopathic epiretinal membrane surgery: a comparative pilot study , 2005, Graefe's Archive for Clinical and Experimental Ophthalmology.

[90]  F. Kuhn.  Point: to peel or not to peel, that is the question. , 2002, Ophthalmology.

[91]  F. Bandello,et al.  Idiopathic macular hole surgery with low-concentration infracyanine green-assisted peeling of the internal limiting membrane. , 2006 .

[92]  Sanjay Sharma,et al.  Outcome results in macular hole surgery: an evaluation of internal limiting membrane peeling with and without indocyanine green. , 2003, Ophthalmology.

[93]  Wei-Chi Wu,et al.  Blood-assisted internal limiting membrane peeling for macular hole repair. , 2008, Ophthalmology.

[94]  S. Androudi,et al.  RETINAL NERVE FIBER LAYER THICKNESS EVALUATION AFTER TRYPAN BLUE–ASSISTED MACULAR SURGERY , 2010, Retina.

[95]  Y. Goto,et al.  BRILLIANT BLUE G SELECTIVELY STAINS THE INTERNAL LIMITING MEMBRANE/BRILLIANT BLUE G–ASSISTED MEMBRANE PEELING , 2006, Retina.

[96]  F. C. Gundogan.  Assessment of macular function by multifocal electroretinography following epiretinal membrane surgery with indocyanine green-assisted internal limiting membrane peeling , 2007, Graefe's Archive for Clinical and Experimental Ophthalmology.

[97]  E. Çelik,et al.  Pars Plana Vitrectomy and Removal of the Internal Limiting Membrane in Diabetic Macular Edema Unresponsive to Grid Laser Photocoagulation , 2006, European journal of ophthalmology.

[98]  Z. Michalewska,et al.  Pars plana vitrectomy with ILM peeling for macular edema secondary to retinal vein occlusion , 2009, European journal of ophthalmology.

[99]  F. Fitzke,et al.  PARS PLANA VITRECTOMY WITH AND WITHOUT PEELING OF THE INNER LIMITING MEMBRANE FOR DIABETIC MACULAR EDEMA , 2006, Retina.

[100]  M L Wolbarsht,et al.  Increased retinal oxygen supply following pan-retinal photocoagulation and vitrectomy and lensectomy. , 1981, Transactions of the American Ophthalmological Society.

[101]  N. Ogino,et al.  Incidence and factors related to macular hole reopening. , 2010, American journal of ophthalmology.

[102]  S. Dean,et al.  A comparison of outcomes after indocyanine green and trypan blue assisted internal limiting membrane peeling during macular hole surgery , 2005, British Journal of Ophthalmology.

[103]  R. Wendel,et al.  Vitreous surgery for idiopathic macular holes. Results of a pilot study. , 1991, Archives of ophthalmology.

[104]  N. Tachi,et al.  LONG-TERM FOLLOW-UP OF VITRECTOMY FOR DIFFUSE NONTRACTIONAL DIABETIC MACULAR EDEMA , 2009, Retina.

[105]  W. Halfter.  Disruption of the retinal basal lamina during early embryonic development leads to a retraction of vitreal end feet, an increased number of ganglion cells, and aberrant axonal outgrowth , 1998, The Journal of comparative neurology.

[106]  L. Benjamin,et al.  Iatrogenic eccentric full thickness macular holes following vitrectomy with ILM peeling for idiopathic macular holes , 2003, Eye.

[107]  T. Lai,et al.  Internal limiting membrane staining with various concentrations of indocyanine green dye under air in macular surgeries. , 2003, American journal of ophthalmology.

[108]  S. C. Lee,et al.  Pars Plana Vitrectomy with Internal Limiting Membrane Peeling Compared with Intravitreal Triamcinolone Injection in the Treatment of Diabetic Macular Edema , 2008, Ophthalmologica.

[109]  S. Priglinger,et al.  TRYPAN BLUE IN MACULAR PUCKER SURGERY: AN EVALUATION OF HISTOLOGY AND FUNCTIONAL OUTCOME , 2004, Retina.

[110]  T. Lai,et al.  Macular hole surgery with or without indocyanine green stained internal limiting membrane peeling , 2003, Clinical & experimental ophthalmology.

[111]  Y. Ogura,et al.  HISTOPATHOLOGIC EVALUATION OF THE INTERNAL LIMITING MEMBRANE SURGICALLY EXCISED FROM EYES WITH DIABETIC MACULOPATHY , 2005, Retina.

[112]  C. Trempe,et al.  The role of the vitreous in diabetic macular edema. , 1988, Ophthalmology.

[113]  E. Jones,et al.  Outcome of ICG-assisted ILM peel in macular hole surgery , 2004, Eye.

[114]  P. Wiedemann,et al.  Clinical findings in macular hole surgery with indocyanine green-assisted peeling of the internal limiting membrane , 2003, Graefe's Archive for Clinical and Experimental Ophthalmology.

[115]  D. Lam,et al.  Anatomical and visual outcome of macular hole surgery with infracyanine green-assisted peeling of the internal limiting membrane, endodrainage, and silicone oil tamponade. , 2004, American journal of ophthalmology.

[116]  F. Adatia,et al.  Surgical macular decompression for macular edema in retinal vein occlusion. , 2007, Canadian journal of ophthalmology. Journal canadien d'ophtalmologie.

[117]  N. Tachi,et al.  Vitrectomy for macular edema combined with retinal vein occlusion , 2004, Documenta Ophthalmologica.

[118]  A. Kampik,et al.  RESOLUTION OF DIABETIC MACULAR EDEMA AFTER SURGICAL REMOVAL OF THE POSTERIOR HYALOID AND THE INNER LIMITING MEMBRANE , 2000, Retina.

[119]  T. Lai,et al.  Indocyanine green assisted retinal internal limiting membrane removal in stage 3 or 4 macular hole surgery , 2003, The British journal of ophthalmology.

[120]  A. Uemura,et al.  LONG-TERM VISUAL OUTCOMES AFTER VITRECTOMY FOR MACULAR EDEMA WITH FOVEAL HEMORRHAGE IN BRANCH RETINAL VEIN OCCLUSION , 2007, Retina.

[121]  T. Aaberg,et al.  Surgical excision of the attached posterior hyaloid. , 1988, Archives of ophthalmology.

[122]  K. Suzuma,et al.  EFFICACY OF SURGICAL REMOVAL OF THE INTERNAL LIMITING MEMBRANE IN DIABETIC CYSTOID MACULAR EDEMA , 2005, Retina.

[123]  G. Shah,et al.  TRIAMCINOLONE-ASSISTED INTERNAL LIMITING MEMBRANE PEELING , 2005, Retina.

[124]  M. Kondo,et al.  Focal macular ERGs in eyes after removal of macular ILM during macular hole surgery. , 2001, Investigative ophthalmology & visual science.

[125]  Christos Haritoglou,et al.  Long-term follow-up after macular hole surgery with internal limiting membrane peeling. , 2002, American journal of ophthalmology.

[126]  C. Aras,et al.  Peeling of internal limiting membrane during vitrectomy for complicated retinal detachment prevents epimacular membrane formation , 2009, Graefe's Archive for Clinical and Experimental Ophthalmology.

[127]  R. Sorcinelli.  Surgical Management of Epiretinal Membrane with Indocyanine-Green-Assisted Peeling , 2003, Ophthalmologica.

[128]  Michael A. Albert,et al.  ECCENTRIC MACULAR HOLES AFTER VITRECTOMY WITH PEELING OF EPIMACULAR PROLIFERATION , 2007, Retina.

[129]  P. Massin,et al.  Relationship between macular hole size and the potential benefit of internal limiting membrane peeling , 2006, British Journal of Ophthalmology.

[130]  S. E. Burk,et al.  Long-term follow-up of indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for idiopathic macular hole repair. , 2004, Ophthalmology.

[131]  G. Naumann,et al.  Applied pathology for ophthalmic microsurgeons , 2008 .

[132]  S. Fekrat,et al.  Pars plana vitrectomy, internal limiting membrane peeling, and panretinal endophotocoagulation for macular edema secondary to central retinal vein occlusion. , 2009, American journal of ophthalmology.

[133]  P. Steven,et al.  Secondary paracentral retinal holes following internal limiting membrane removal , 2006, British Journal of Ophthalmology.

[134]  W. Halfter,et al.  Temporary disruption of the retinal basal lamina and its effect on retinal histogenesis. , 2001, Developmental biology.