Point: to peel or not to peel, that is the question
2002; Elsevier BV; Volume: 109; Issue: 1 Linguagem: Inglês
10.1016/s0161-6420(01)00992-7
ISSN1549-4713
Autores Tópico(s)Glaucoma and retinal disorders
ResumoThe innermost layer of the retina, the internal limiting membrane (lamina; ILM), is composed in part of type IV collagen. This 6 μ-thick, transparent structure rests on a bed of Müller cell footplates that in turn form a contiguous montage, separating the ILM from the nerve fiber layer.The ILM received virtually no clinical attention until vitrectomy removal of epimacular proliferations (EMP) became routine in the 1980s and ILM fragments were often identified in surgical specimens. The controversial issue of intentional ILM peeling first emerged in the early 1990s, following Gass’ theory of macular hole pathogenesis1Gass J.D.M. Idiopathic senile macular hole. Its early stages and pathogenesis.Arch Ophthalmol. 1988; 106: 629-639Crossref PubMed Scopus (911) Google Scholar and coinciding with the advent of macular hole surgery.2Kelly N.E. Wendel R.T. Vitreous surgery for idiopathic macular holes. Results of a pilot study.Arch Ophthalmol. 1991; 109: 654-659Crossref PubMed Scopus (1154) Google ScholarInitial reports of ILM removal3Brooks H.J. ILM peeling in full thickness macular hole surgery.Vitreoretin Surg Technol. 1995; 7: 1-8Google Scholar, 4Eckardt C. Eckardt U. Groos S. et al.Entfernung der Membrana limitans interna bei Makulalöchem. Klinische und morphologische Befunde.Ophthalmologe. 1997; 94: 545-551Crossref PubMed Scopus (228) Google Scholar, 5Morris R. Witherspoon C.D. Kuhn F. Priester B. Internal limiting membrane maculorrhexis for traction maculopathy.Vitreoretin Surg Technol. 1997; 8: 1-5Google Scholar, 6Rice T. Internal limiting membrane removal in surgery for full-thickness macular holes.in: Madreperla S. McCuen B.I. Macular Hole Pathogenesis, Diagnosis, and Treatment. Butterworth-Heinemann, Boston1999: 125-146Google Scholar were greeted with skepticism, questioning whether the removed specimen was indeed ILM, not EMP or the posterior vitreous cortex. Growing clinical experience and ample proof from light and electron microscopic as well as immunofluorescence studies,7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar, 8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 9Yooh H.S. Brooks Jr, H.L. Capone Jr, A. et al.Ultrastructural features of tissue removed during idiopathic macular hole surgery.Am J Ophthalmol. 1996; 122: 67-75PubMed Google Scholar have effectively silenced this skepticism. As the initial enthusiasm for adjuvant therapy subsided,10Thompson J.T. Smiddy W.E. Williams G.A. et al.Comparison of recombinant transforming growth factor-beta-2 and placebo as an adjunctive agent for macular hole surgery.Ophthalmology. 1998; 105: 700-706Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar the popularity of ILM peeling for tangential traction relief increased.11Olsen T.W. Sternberg Jr, P. Capone Jr, A. et al.Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane.Retina. 1998; 18: 322-329Crossref PubMed Scopus (131) Google Scholar Vitreous Society surveys (Pollack JS and Packo K: Vitreous Society Annual Meeting, Cancun, Mexico, January 2001) found that from 1999 to 2000 the rate of proponents of ILM removal in macular hole surgery increased from 23% to 34%, while the proportion of surgeons rarely peeling decreased from 38% to 20%.It is now clear that ILM removal is possible; but should we remove ILM? Is the procedure safe; does it improve the outcome when compared with existing techniques; and is it indicated beyond macular hole surgery?In 1990, Morris et al (Ophthalmology 1990;97 (suppl):130) reported the first cases of intentional ILM removal. In patients with Terson’s syndrome and sub-ILM macular hemorrhage, they removed both the blood and the detached ILM. The authors subsequently described follow-ups as long as 8 years in these patients12Morris R. Kuhn F. Witherspoon C.D. et al.Hemorrhagic macular cysts in Terson’s syndrome and its implications for macular surgery.Dev ophthalmol. 1997; 29: 44-54Crossref PubMed Scopus (29) Google Scholar; 83% of adult eyes reached ≥20/25 vision without clinically visible surface re/proliferation. Based on this experience, they suggested in 199413Morris R. Kuhn F. Witherspoon C.D. R Hemorrhagic macular cysts.Ophthalmology. 1994; 101 ([letter]): 1Abstract Full Text PDF PubMed Scopus (43) Google Scholar that ILM removal be considered for all forms of “traction maculopathy.” Although intentional ILM manipulations had been discouraged prior to 1990, no permanent damage specific to, or caused by, ILM removal was found,14Gaudric A. Fardeau C. Goberville M. et al.[Ablation of the internal limiting membrane, macular unfolding and visual outcome in surgery of idiopathic epimacular membranes].J Fr Ophthalmol. 1993; 16: 571-576PubMed Google Scholar, 15Trese M. Chandler D.B. Machemer R. Macular pucker II. Ultrastructure.Graefes Arch Clin Exp Ophthalmol. 1983; 221: 16-26Crossref PubMed Scopus (54) Google Scholar and only a single report16Sivalingam A. Eagle Jr, R.C. Duker J.S. et al.Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery.Ophthalmology. 1990; 97: 1549-1552Abstract Full Text PDF PubMed Scopus (101) Google Scholar suggested worse outcomes if the specimen also contained “long ILM segments.”Internal limiting membrane removal did raise concerns. Müller cell damage was contradicted by both experimental data (following ILM peeling in the freshly removed porcine eye, the Müller cells remained anatomically intact and showed excellent growth in culture17Guidry C. Isolation and characterization of porcine Müller cells Myofibroblastic dedifferentiation in culture.Invest Ophthalmol Vis Sci. 1996; 37: 740-752PubMed Google Scholar; normal multifocal macular ERG was reported 1 year after ILM removal18Morris R, Witherspoon CD, Kuhn F, et al. Traction maculopathy. In: Kriegelstein G, ed., Retinology Today, Munich: Verlag für Medizin und Naturwissenschafter 2000;83–8.Google Scholar) and clinical observations (excellent long-term visual outcome12Morris R. Kuhn F. Witherspoon C.D. et al.Hemorrhagic macular cysts in Terson’s syndrome and its implications for macular surgery.Dev ophthalmol. 1997; 29: 44-54Crossref PubMed Scopus (29) Google Scholar). Visual field defects, described in up to 17% of eyes undergoing macular hole surgery19Pendergast S.D. McCuen II, B.W. Visual field loss after macular hole surgery.Ophthalmology. 1996; 103: 1069-1077Abstract Full Text PDF PubMed Scopus (96) Google Scholar are now attributed to dehumidified air infused at higher pressures.20Welch J.C. Dehydration injury as a possible cause of visual defect after pars plana vitrectomy for macular hole.Am J Ophthalmol. 1997; 124: 698-699Abstract Full Text PDF PubMed Scopus (95) Google Scholar No visual field defect has been found in a large series of eyes with ILM removal for macular hole.6Rice T. Internal limiting membrane removal in surgery for full-thickness macular holes.in: Madreperla S. McCuen B.I. Macular Hole Pathogenesis, Diagnosis, and Treatment. Butterworth-Heinemann, Boston1999: 125-146Google Scholar Phototoxicity occasionally occurs,21Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397–8.Google Scholar but this preventable complication is nonspecific to ILM peeling.22Kuhn F. Morris R. Massey M. Photic retinal injury from endoillumination during vitrectomy.Am J Ophthalmol. 1991; 111: 42-46Abstract Full Text PDF PubMed Scopus (48) Google Scholar Retinal edema and small capillary hemorrhages are commonly seen but have not been reported to cause permanent consequences.The introduction of ILM staining with indocyanine green (ICG; Kim VY, Clark JD: Ophthalmology 1999;106 (suppl):201) and the FILMS (Fluidic Internal Limiting Membrane Separation) technique by Morris et al23Morris R. Kuhn F. Surgical treatment of macular surface disorders.in: Boyd B. World Atlas Series of Ophthalmic Surgery. Vol IV. Highlights of Ophthalmology, Panama City1998: 58-64Google Scholar further enhance ease and safety. Recently, questions were raised regarding the potential toxicity of ICG; however, the majority of authors have found no adverse effects.In summary, intentional ILM removal, although a technically challenging procedure that requires caution and experience, is a safe maneuver.Ideally, a randomized, prospective, double-masked, multicenter study should determine whether ILM removal improves the functional outcome. In the absence of such a study, one must carefully analyze existing reports, and realizing their obvious limitations, review the largest possible cohorts.Many authors found high anatomical and functional success rates with ILM removal in macular hole surgery,4Eckardt C. Eckardt U. Groos S. et al.Entfernung der Membrana limitans interna bei Makulalöchem. Klinische und morphologische Befunde.Ophthalmologe. 1997; 94: 545-551Crossref PubMed Scopus (228) Google Scholar, 7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar, 8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 9Yooh H.S. Brooks Jr, H.L. Capone Jr, A. et al.Ultrastructural features of tissue removed during idiopathic macular hole surgery.Am J Ophthalmol. 1996; 122: 67-75PubMed Google Scholar, 11Olsen T.W. Sternberg Jr, P. Capone Jr, A. et al.Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane.Retina. 1998; 18: 322-329Crossref PubMed Scopus (131) Google Scholar, 14Gaudric A. Fardeau C. Goberville M. et al.[Ablation of the internal limiting membrane, macular unfolding and visual outcome in surgery of idiopathic epimacular membranes].J Fr Ophthalmol. 1993; 16: 571-576PubMed Google Scholar, 15Trese M. Chandler D.B. Machemer R. Macular pucker II. Ultrastructure.Graefes Arch Clin Exp Ophthalmol. 1983; 221: 16-26Crossref PubMed Scopus (54) Google Scholar, 21Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397–8.Google Scholar, 24Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology 2000;107:1939–48; discussion 1948–9.Google Scholar, 25Gribomont A.C. [“Rupture” of the internal limiting membrane in surgery of the macular hole preliminary results].Bull Soc Belg Ophtalmol. 1999; 272: 9-11PubMed Google Scholar, 26Kapetanios A.D. Donati G. Pournaras C.J. [Results and complications of surgery for idiopathic macular holes].Klin Montsbl Augenheill. 1999; 214: 282-284Crossref PubMed Scopus (4) Google Scholar, 27Livingstone B.I. Bourke R.D. Retrospective study of macular holes treated with pars plana vitrectomy.Aust N Z J Ophthalmol. 1999; 27: 331-341Crossref PubMed Scopus (18) Google Scholar, 28Schrader W.F. Schrenker M. Can the functional outcome in macular hole surgery be improved by internal limiting membrane maculorhexis?.Klin Oczna. 1999; 101: 169-173PubMed Google Scholar and comparing series with and without ILM peeling, all but one study29Margherio R.R. Margherio A.R. Williams G.A. et al.Effect of perifoveal tissue dissection in the management of acute idiopathic full-thickness macular holes.Arch Ophthalmol. 2000; 118: 495-498Crossref PubMed Scopus (92) Google Scholar reported statistically significantly improved outcomes if the ILM was peeled. Internal limiting membrane removal appears to be especially beneficial in eyes with primary surgical failure or reopened/large/chronic holes.24Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology 2000;107:1939–48; discussion 1948–9.Google Scholar A literature meta-analysis, reviewing 31 studies involving 1,654 eyes undergoing macular hole surgery, compared three different surgical techniques: no adjuvant, no ILM peeling; adjuvant, no ILM peeling; and no adjuvant, ILM peeling. There was no statistically significant difference between the first two methods, but ILM removal resulted in statistically significantly (P < 0.0001) better anatomical and functional outcomes over both other techniques.7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar Although these reports reflect years of advancing surgical techniques, ILM peeling was the primary change; removal of the cortical vitreous and gas tamponade have remained largely static. In summary, it appears that the chances of macular hole closure and visual recovery significantly increase if the tangential traction is released by removal of the perifoveal ILM in a sufficiently large area around the hole. This effect is most obvious in eyes after primary surgical failure and for holes of longer duration or larger size.It is now widely accepted that tangential traction is involved in the formation of idiopathic macular holes, cellophane maculopathy, and macular pucker23Morris R. Kuhn F. Surgical treatment of macular surface disorders.in: Boyd B. World Atlas Series of Ophthalmic Surgery. Vol IV. Highlights of Ophthalmology, Panama City1998: 58-64Google Scholar; even specimens from vitreomacular traction syndrome commonly contain ILM.8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 30Smiddy W.E. Green W.R. Michels R.G. de la Cruz Z. Ultrastructural studies of vitreomacular traction syndrome.Am J Ophthalmol. 1989; 107: 177-185Abstract Full Text PDF PubMed Scopus (82) Google Scholar The concept of ILM peeling in eyes with traction maculopathy18Morris R, Witherspoon CD, Kuhn F, et al. Traction maculopathy. In: Kriegelstein G, ed., Retinology Today, Munich: Verlag für Medizin und Naturwissenschafter 2000;83–8.Google Scholar is supported by logic (complete traction relief is more likely with removal of the very surface on which these forces accumulate rather than with tissue removal in front of this plane) and by the fact that EMP recurrence or macular hole reopening after sufficient ILM removal has not been reported; conversely, up to 5% of holes without ILM peeling reopen.31Christmas N.J. Smiddy W.E. Flynn Jr, H.W. Reopening of macular holes after initially successful repair.Ophthalmology. 1998; 105: 1835-1838Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar, 32Duker J.S. Wendel R. Patel A.C. Puliafito C.A. Late re-opening of macular holes after initially successfully treatment with vitreous surgery.Ophthalmology. 1994; 101: 1373-1378Abstract Full Text PDF PubMed Scopus (105) Google Scholar Since it is not possible to preoperatively identify the eyes in which tangential traction has played a crucial role in macular hole development, ILM removal may be considered as a prophylactic measure against macular hole reopening. Peeling of the inelastic ILM has proven effective and appears indicated for traumatic macular holes33Kuhn F. Morris R. Mester V. Witherspoon C.D. Internal limiting membrane removal for traumatic macular holes.Ophthalmic Surg Lasers. 2001; 32: 308-315PubMed Google Scholar and may play a role in the management of eyes with clinically significant (diabetic) macular edema refractory to other treatments. In summary, ILM peeling is indicated for eyes in which traction exerted upon the macula has generated functional complications.When Machemer introduced vitrectomy, it sounded shocking to ophthalmologists who were taught not to violate the vitreous. Similarly dramatic was Zivojnovic’s initial advocacy of retinotomy. Now surgeons intentionally remove the innermost layer of the retina. The first two of these revolutionary steps allowed treatment of conditions otherwise untreatable. Internal limiting membrane peeling is not claimed to cure pathologies for which no other treatment exists, but it has been reasonably proven to significantly increase the success rate in macular hole surgery and may be expected to do so for other forms of traction maculopathy. The innermost layer of the retina, the internal limiting membrane (lamina; ILM), is composed in part of type IV collagen. This 6 μ-thick, transparent structure rests on a bed of Müller cell footplates that in turn form a contiguous montage, separating the ILM from the nerve fiber layer. The ILM received virtually no clinical attention until vitrectomy removal of epimacular proliferations (EMP) became routine in the 1980s and ILM fragments were often identified in surgical specimens. The controversial issue of intentional ILM peeling first emerged in the early 1990s, following Gass’ theory of macular hole pathogenesis1Gass J.D.M. Idiopathic senile macular hole. Its early stages and pathogenesis.Arch Ophthalmol. 1988; 106: 629-639Crossref PubMed Scopus (911) Google Scholar and coinciding with the advent of macular hole surgery.2Kelly N.E. Wendel R.T. Vitreous surgery for idiopathic macular holes. Results of a pilot study.Arch Ophthalmol. 1991; 109: 654-659Crossref PubMed Scopus (1154) Google Scholar Initial reports of ILM removal3Brooks H.J. ILM peeling in full thickness macular hole surgery.Vitreoretin Surg Technol. 1995; 7: 1-8Google Scholar, 4Eckardt C. Eckardt U. Groos S. et al.Entfernung der Membrana limitans interna bei Makulalöchem. Klinische und morphologische Befunde.Ophthalmologe. 1997; 94: 545-551Crossref PubMed Scopus (228) Google Scholar, 5Morris R. Witherspoon C.D. Kuhn F. Priester B. Internal limiting membrane maculorrhexis for traction maculopathy.Vitreoretin Surg Technol. 1997; 8: 1-5Google Scholar, 6Rice T. Internal limiting membrane removal in surgery for full-thickness macular holes.in: Madreperla S. McCuen B.I. Macular Hole Pathogenesis, Diagnosis, and Treatment. Butterworth-Heinemann, Boston1999: 125-146Google Scholar were greeted with skepticism, questioning whether the removed specimen was indeed ILM, not EMP or the posterior vitreous cortex. Growing clinical experience and ample proof from light and electron microscopic as well as immunofluorescence studies,7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar, 8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 9Yooh H.S. Brooks Jr, H.L. Capone Jr, A. et al.Ultrastructural features of tissue removed during idiopathic macular hole surgery.Am J Ophthalmol. 1996; 122: 67-75PubMed Google Scholar have effectively silenced this skepticism. As the initial enthusiasm for adjuvant therapy subsided,10Thompson J.T. Smiddy W.E. Williams G.A. et al.Comparison of recombinant transforming growth factor-beta-2 and placebo as an adjunctive agent for macular hole surgery.Ophthalmology. 1998; 105: 700-706Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar the popularity of ILM peeling for tangential traction relief increased.11Olsen T.W. Sternberg Jr, P. Capone Jr, A. et al.Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane.Retina. 1998; 18: 322-329Crossref PubMed Scopus (131) Google Scholar Vitreous Society surveys (Pollack JS and Packo K: Vitreous Society Annual Meeting, Cancun, Mexico, January 2001) found that from 1999 to 2000 the rate of proponents of ILM removal in macular hole surgery increased from 23% to 34%, while the proportion of surgeons rarely peeling decreased from 38% to 20%. It is now clear that ILM removal is possible; but should we remove ILM? Is the procedure safe; does it improve the outcome when compared with existing techniques; and is it indicated beyond macular hole surgery? In 1990, Morris et al (Ophthalmology 1990;97 (suppl):130) reported the first cases of intentional ILM removal. In patients with Terson’s syndrome and sub-ILM macular hemorrhage, they removed both the blood and the detached ILM. The authors subsequently described follow-ups as long as 8 years in these patients12Morris R. Kuhn F. Witherspoon C.D. et al.Hemorrhagic macular cysts in Terson’s syndrome and its implications for macular surgery.Dev ophthalmol. 1997; 29: 44-54Crossref PubMed Scopus (29) Google Scholar; 83% of adult eyes reached ≥20/25 vision without clinically visible surface re/proliferation. Based on this experience, they suggested in 199413Morris R. Kuhn F. Witherspoon C.D. R Hemorrhagic macular cysts.Ophthalmology. 1994; 101 ([letter]): 1Abstract Full Text PDF PubMed Scopus (43) Google Scholar that ILM removal be considered for all forms of “traction maculopathy.” Although intentional ILM manipulations had been discouraged prior to 1990, no permanent damage specific to, or caused by, ILM removal was found,14Gaudric A. Fardeau C. Goberville M. et al.[Ablation of the internal limiting membrane, macular unfolding and visual outcome in surgery of idiopathic epimacular membranes].J Fr Ophthalmol. 1993; 16: 571-576PubMed Google Scholar, 15Trese M. Chandler D.B. Machemer R. Macular pucker II. Ultrastructure.Graefes Arch Clin Exp Ophthalmol. 1983; 221: 16-26Crossref PubMed Scopus (54) Google Scholar and only a single report16Sivalingam A. Eagle Jr, R.C. Duker J.S. et al.Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery.Ophthalmology. 1990; 97: 1549-1552Abstract Full Text PDF PubMed Scopus (101) Google Scholar suggested worse outcomes if the specimen also contained “long ILM segments.” Internal limiting membrane removal did raise concerns. Müller cell damage was contradicted by both experimental data (following ILM peeling in the freshly removed porcine eye, the Müller cells remained anatomically intact and showed excellent growth in culture17Guidry C. Isolation and characterization of porcine Müller cells Myofibroblastic dedifferentiation in culture.Invest Ophthalmol Vis Sci. 1996; 37: 740-752PubMed Google Scholar; normal multifocal macular ERG was reported 1 year after ILM removal18Morris R, Witherspoon CD, Kuhn F, et al. Traction maculopathy. In: Kriegelstein G, ed., Retinology Today, Munich: Verlag für Medizin und Naturwissenschafter 2000;83–8.Google Scholar) and clinical observations (excellent long-term visual outcome12Morris R. Kuhn F. Witherspoon C.D. et al.Hemorrhagic macular cysts in Terson’s syndrome and its implications for macular surgery.Dev ophthalmol. 1997; 29: 44-54Crossref PubMed Scopus (29) Google Scholar). Visual field defects, described in up to 17% of eyes undergoing macular hole surgery19Pendergast S.D. McCuen II, B.W. Visual field loss after macular hole surgery.Ophthalmology. 1996; 103: 1069-1077Abstract Full Text PDF PubMed Scopus (96) Google Scholar are now attributed to dehumidified air infused at higher pressures.20Welch J.C. Dehydration injury as a possible cause of visual defect after pars plana vitrectomy for macular hole.Am J Ophthalmol. 1997; 124: 698-699Abstract Full Text PDF PubMed Scopus (95) Google Scholar No visual field defect has been found in a large series of eyes with ILM removal for macular hole.6Rice T. Internal limiting membrane removal in surgery for full-thickness macular holes.in: Madreperla S. McCuen B.I. Macular Hole Pathogenesis, Diagnosis, and Treatment. Butterworth-Heinemann, Boston1999: 125-146Google Scholar Phototoxicity occasionally occurs,21Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397–8.Google Scholar but this preventable complication is nonspecific to ILM peeling.22Kuhn F. Morris R. Massey M. Photic retinal injury from endoillumination during vitrectomy.Am J Ophthalmol. 1991; 111: 42-46Abstract Full Text PDF PubMed Scopus (48) Google Scholar Retinal edema and small capillary hemorrhages are commonly seen but have not been reported to cause permanent consequences. The introduction of ILM staining with indocyanine green (ICG; Kim VY, Clark JD: Ophthalmology 1999;106 (suppl):201) and the FILMS (Fluidic Internal Limiting Membrane Separation) technique by Morris et al23Morris R. Kuhn F. Surgical treatment of macular surface disorders.in: Boyd B. World Atlas Series of Ophthalmic Surgery. Vol IV. Highlights of Ophthalmology, Panama City1998: 58-64Google Scholar further enhance ease and safety. Recently, questions were raised regarding the potential toxicity of ICG; however, the majority of authors have found no adverse effects. In summary, intentional ILM removal, although a technically challenging procedure that requires caution and experience, is a safe maneuver. Ideally, a randomized, prospective, double-masked, multicenter study should determine whether ILM removal improves the functional outcome. In the absence of such a study, one must carefully analyze existing reports, and realizing their obvious limitations, review the largest possible cohorts. Many authors found high anatomical and functional success rates with ILM removal in macular hole surgery,4Eckardt C. Eckardt U. Groos S. et al.Entfernung der Membrana limitans interna bei Makulalöchem. Klinische und morphologische Befunde.Ophthalmologe. 1997; 94: 545-551Crossref PubMed Scopus (228) Google Scholar, 7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar, 8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 9Yooh H.S. Brooks Jr, H.L. Capone Jr, A. et al.Ultrastructural features of tissue removed during idiopathic macular hole surgery.Am J Ophthalmol. 1996; 122: 67-75PubMed Google Scholar, 11Olsen T.W. Sternberg Jr, P. Capone Jr, A. et al.Macular hole surgery using thrombin-activated fibrinogen and selective removal of the internal limiting membrane.Retina. 1998; 18: 322-329Crossref PubMed Scopus (131) Google Scholar, 14Gaudric A. Fardeau C. Goberville M. et al.[Ablation of the internal limiting membrane, macular unfolding and visual outcome in surgery of idiopathic epimacular membranes].J Fr Ophthalmol. 1993; 16: 571-576PubMed Google Scholar, 15Trese M. Chandler D.B. Machemer R. Macular pucker II. Ultrastructure.Graefes Arch Clin Exp Ophthalmol. 1983; 221: 16-26Crossref PubMed Scopus (54) Google Scholar, 21Park DW, Sipperley JO, Sneed SR, et al. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology 1999;106:1392–7; discussion 1397–8.Google Scholar, 24Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology 2000;107:1939–48; discussion 1948–9.Google Scholar, 25Gribomont A.C. [“Rupture” of the internal limiting membrane in surgery of the macular hole preliminary results].Bull Soc Belg Ophtalmol. 1999; 272: 9-11PubMed Google Scholar, 26Kapetanios A.D. Donati G. Pournaras C.J. [Results and complications of surgery for idiopathic macular holes].Klin Montsbl Augenheill. 1999; 214: 282-284Crossref PubMed Scopus (4) Google Scholar, 27Livingstone B.I. Bourke R.D. Retrospective study of macular holes treated with pars plana vitrectomy.Aust N Z J Ophthalmol. 1999; 27: 331-341Crossref PubMed Scopus (18) Google Scholar, 28Schrader W.F. Schrenker M. Can the functional outcome in macular hole surgery be improved by internal limiting membrane maculorhexis?.Klin Oczna. 1999; 101: 169-173PubMed Google Scholar and comparing series with and without ILM peeling, all but one study29Margherio R.R. Margherio A.R. Williams G.A. et al.Effect of perifoveal tissue dissection in the management of acute idiopathic full-thickness macular holes.Arch Ophthalmol. 2000; 118: 495-498Crossref PubMed Scopus (92) Google Scholar reported statistically significantly improved outcomes if the ILM was peeled. Internal limiting membrane removal appears to be especially beneficial in eyes with primary surgical failure or reopened/large/chronic holes.24Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology 2000;107:1939–48; discussion 1948–9.Google Scholar A literature meta-analysis, reviewing 31 studies involving 1,654 eyes undergoing macular hole surgery, compared three different surgical techniques: no adjuvant, no ILM peeling; adjuvant, no ILM peeling; and no adjuvant, ILM peeling. There was no statistically significant difference between the first two methods, but ILM removal resulted in statistically significantly (P < 0.0001) better anatomical and functional outcomes over both other techniques.7Mester V. Kuhn F. Internal limiting membrane removal in the management of full-thickness macular holes.Am J Ophthalmol. 2000; 129: 769-777Abstract Full Text Full Text PDF PubMed Scopus (288) Google Scholar Although these reports reflect years of advancing surgical techniques, ILM peeling was the primary change; removal of the cortical vitreous and gas tamponade have remained largely static. In summary, it appears that the chances of macular hole closure and visual recovery significantly increase if the tangential traction is released by removal of the perifoveal ILM in a sufficiently large area around the hole. This effect is most obvious in eyes after primary surgical failure and for holes of longer duration or larger size. It is now widely accepted that tangential traction is involved in the formation of idiopathic macular holes, cellophane maculopathy, and macular pucker23Morris R. Kuhn F. Surgical treatment of macular surface disorders.in: Boyd B. World Atlas Series of Ophthalmic Surgery. Vol IV. Highlights of Ophthalmology, Panama City1998: 58-64Google Scholar; even specimens from vitreomacular traction syndrome commonly contain ILM.8Shinoda K. Hirakata T. Hida T. et al.Ultrastructural and immunohistochemical findings in five patients with vitreomacular traction syndrome.Retina. 2000; 20: 289-293Crossref PubMed Scopus (33) Google Scholar, 30Smiddy W.E. Green W.R. Michels R.G. de la Cruz Z. Ultrastructural studies of vitreomacular traction syndrome.Am J Ophthalmol. 1989; 107: 177-185Abstract Full Text PDF PubMed Scopus (82) Google Scholar The concept of ILM peeling in eyes with traction maculopathy18Morris R, Witherspoon CD, Kuhn F, et al. Traction maculopathy. In: Kriegelstein G, ed., Retinology Today, Munich: Verlag für Medizin und Naturwissenschafter 2000;83–8.Google Scholar is supported by logic (complete traction relief is more likely with removal of the very surface on which these forces accumulate rather than with tissue removal in front of this plane) and by the fact that EMP recurrence or macular hole reopening after sufficient ILM removal has not been reported; conversely, up to 5% of holes without ILM peeling reopen.31Christmas N.J. Smiddy W.E. Flynn Jr, H.W. Reopening of macular holes after initially successful repair.Ophthalmology. 1998; 105: 1835-1838Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar, 32Duker J.S. Wendel R. Patel A.C. Puliafito C.A. Late re-opening of macular holes after initially successfully treatment with vitreous surgery.Ophthalmology. 1994; 101: 1373-1378Abstract Full Text PDF PubMed Scopus (105) Google Scholar Since it is not possible to preoperatively identify the eyes in which tangential traction has played a crucial role in macular hole development, ILM removal may be considered as a prophylactic measure against macular hole reopening. Peeling of the inelastic ILM has proven effective and appears indicated for traumatic macular holes33Kuhn F. Morris R. Mester V. Witherspoon C.D. Internal limiting membrane removal for traumatic macular holes.Ophthalmic Surg Lasers. 2001; 32: 308-315PubMed Google Scholar and may play a role in the management of eyes with clinically significant (diabetic) macular edema refractory to other treatments. In summary, ILM peeling is indicated for eyes in which traction exerted upon the macula has generated functional complications. When Machemer introduced vitrectomy, it sounded shocking to ophthalmologists who were taught not to violate the vitreous. Similarly dramatic was Zivojnovic’s initial advocacy of retinotomy. Now surgeons intentionally remove the innermost layer of the retina. The first two of these revolutionary steps allowed treatment of conditions otherwise untreatable. Internal limiting membrane peeling is not claimed to cure pathologies for which no other treatment exists, but it has been reasonably proven to significantly increase the success rate in macular hole surgery and may be expected to do so for other forms of traction maculopathy.
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