Inner-limiting-membrane peeling in epiretinal membrane surgery: an evolving surgical trend

An epiretinal membrane (ERM) forms in the posterior pole from cellular proliferation on the inner limiting membrane (also known as the internal limiting membrane, ILM). ERMs are most commonly idiopathic and develop after posterior vitreous detachment but can occur secondary to ocular or systemic diseases or retinal injuries such as tears and detachments. Most patients who develop ERMs remain asymptomatic; however, metamorphopsia and progressive decline in visual acuity can occur over time with epiretinal contraction. Surgery with pars plana vitrectomy is indicated in patients with symptomatic ERMs. In recent years there has been a surgical trend among vitreoretinal surgeons to combine ILM peeling in procedures for ERM removal. The reason for the increasing popularity of these combined surgeries is multifold; though, the role of an ILM peel in these cases is not entirely clear and has been debated. Here, our objective is to provide a brief overview of the literature and opinions on ILM peeling during ERM surgery. As the ILM is relatively transparent, its surgical removal was largely regarded as technically challenging until the advent of retinal staining techniques began to be reported in the early 2000s. Initial reports showed that stripping of all epiretinal tissue, including the ERM and ILM, could be expedited and facilitated using indocyanine green (ICG) dye.1Burke S.E. Da Mata A.P. Snyder M.E. Rosa Jr, R.H. Foster R.E. Indocyanine-green-assisted peeling of the retinal internal limiting membrane.Ophthalmology. 2000; 107: 2010-2014Abstract Full Text Full Text PDF PubMed Scopus (274) Google Scholar The benefit for vitreoretinal surgeons in doing this was that ICG showed a distinct contrast between the ILM and deeper retinal tissue, leading to reduced intraoperative complexity whereby there was no need to start and restart the peeling or worry about peeling tissue from the underlying retina. Shortly thereafter it was noted that retinal toxicity may result from ICG staining, and another vital dye, brilliant blue G, could also be useful in staining the epiretina with potentially low retinal toxicity.2Tadayoni R. Paques M. Girmens J.F. Massin P. Gaudric A. Persistence of fundus florescence after use of indocyanine green for macular surgery.Ophthalmology. 2003; 110: 604-608Abstract Full Text Full Text PDF PubMed Scopus (114) Google Scholar, 3Enaida H. Hisatomi T. Goto Y. Hata Y. Ueno A. Ishibashi T. Preclinical investigation of internal limiting membrane staining and peeling using intravitreal brilliant blue G.Retina. 2006; 26: 623-630Crossref PubMed Scopus (139) Google Scholar Eventually, many well-executed studies provided evidence establishing that both ICG and brilliant blue G were safe for use in vitreoretinal surgeries.4Yuen D. Gonder J. Proulx A. Liu H. Hutnik C. Comparison of the in-vitro safety of intraocular dyes using two retinal cell lines: a focus on brilliant blue G and indocyanine green.Am J Ophthalmol. 2009; 147: 251-259Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar The advent of surgical dyes led to a trend to concomitantly peel the ILM during ERM removal surgery. Subsequently, as reported in the American Society of Retina Specialists “preferences and trends survey,” from 2008 to 2010, the number of vitreoretinal surgeons doing ILM peeling for ERM surgery increased from 25% to 44%.5Chang S. Gregory-Roberts E.M. Park S. Laud K. Smith S.D. Hoang Q.V. Double peeling during vitrectomy for macular pucker: the Charles L. Schepens lecture.JAMA Ophthalmol. 2013; 131: 525-530Crossref PubMed Scopus (35) Google Scholar It has been well established that there is equal improvement in postoperative best corrected visual acuity (BCVA) with or without ILM peeling during ERM surgeries. Many cross-sectional and retrospective studies have provided data to support this concept over the past decade. More recently, several longitudinal studies have investigated the long-term outcomes of ERM surgeries up to 3 years,6Azuma K. Ueta T. Eguchi A. Aihara M. Effects of internal limiting membrane peeling combined with removal of idiopathic epiretinal membrane: a systematic review of literature and meta-analysis.Retina. 2017; 37: 1813-1819Crossref PubMed Scopus (45) Google Scholar, 7Fang X.L. Tong Y. Zhou Y.L. Zhao P.Q. Wang Z.Y. Internal limiting membrane peeling of not: a systematic review and meta-analysis of idiopathic macular pucker surgery.Br J Ophthalmol. 2017; 101: 1535-1541Crossref PubMed Scopus (24) Google Scholar and in the spring of 2018, the first data evaluating 5-year outcomes of ERM surgeries were published.8Sultan H. Wykoff C.C. Shah A.R. Five-year outcomes of surgically treated symptomatic epiretinal membranes with and without internal limiting membrane peeling.Ophthalmic Surg Lasers Imaging Retina. 2018; 49: 296-302Crossref PubMed Scopus (8) Google Scholar The longitudinal data show that, up to 5 years postoperatively, there are no significant differences between the improvement in BCVA in patients who underwent a combined ERM and ILM peeling procedure versus those who only had the ERM removed. These longitudinal studies reinforce the notion that BCVA outcomes are similar whether the ILM is peeled or not. At the same time, these studies have provided valuable insight into other clinically relevant endpoints for ophthalmologists such as ERM recurrence and postoperative anatomical changes in retinal thickness. By peeling the ILM, vitreoretinal surgeons can be assured that an ERM is completely removed. Therefore, in the absence of surgical complications, the possibility of leaving a “persistent” ERM postoperatively from an incomplete peel is extremely low with a combined ILM and ERM peeling procedure. In keeping with this, the cross-sectional and longitudinal literature has established that there is in fact lower ERM recurrence postoperatively in these combined surgeries.6Azuma K. Ueta T. Eguchi A. Aihara M. Effects of internal limiting membrane peeling combined with removal of idiopathic epiretinal membrane: a systematic review of literature and meta-analysis.Retina. 2017; 37: 1813-1819Crossref PubMed Scopus (45) Google Scholar, 7Fang X.L. Tong Y. Zhou Y.L. Zhao P.Q. Wang Z.Y. Internal limiting membrane peeling of not: a systematic review and meta-analysis of idiopathic macular pucker surgery.Br J Ophthalmol. 2017; 101: 1535-1541Crossref PubMed Scopus (24) Google Scholar, 8Sultan H. Wykoff C.C. Shah A.R. Five-year outcomes of surgically treated symptomatic epiretinal membranes with and without internal limiting membrane peeling.Ophthalmic Surg Lasers Imaging Retina. 2018; 49: 296-302Crossref PubMed Scopus (8) Google Scholar, 9Park D.W. Dugel P.U. Garda J. et al.Macular pucker removal with and without internal limiting membrane peeling: pilot study.Ophthalmology. 2003; 110: 62-64Abstract Full Text Full Text PDF PubMed Scopus (208) Google Scholar, 10Kang K.T. Kim K.S. Kim Y.C. Surgical results of idiopathic and secondary epiretinal membrane.Int Ophthalmol. 2014; 34: 1227-1232Crossref PubMed Scopus (23) Google Scholar, 11Ahn S.J. Ahn J. Woo S.J. Park K.H. Photoreceptor change and visual outcome after idiopathic epiretinal membrane removal with or without additional internal limiting membrane peeling.Retina. 2014; 34: 172-181Crossref PubMed Scopus (47) Google Scholar Similarly, postoperative anatomical changes such as central retinal and macular thickness have also been investigated. However, the results from these studies are not as straightforward to interpret.7Fang X.L. Tong Y. Zhou Y.L. Zhao P.Q. Wang Z.Y. Internal limiting membrane peeling of not: a systematic review and meta-analysis of idiopathic macular pucker surgery.Br J Ophthalmol. 2017; 101: 1535-1541Crossref PubMed Scopus (24) Google Scholar A cross-sectional study reported that ILM peeling during ERM surgeries is associated with an increase in macular thickness postoperatively.12Lee J.W. Kim I.T. Outcomes of idiopathic macular epiretinal membrane removal with and without internal limiting membrane peeling: a comparative study.Jpn J Ophthalmol. 2010; 54: 129-134Crossref PubMed Scopus (62) Google Scholar Yet, longitudinal data suggest that there is a progressive decline in retinal thickness postoperatively, and after 5 years there is not a significant difference in retinal thickness for combined ERM and ILM peeling versus non-ILM peeling.8Sultan H. Wykoff C.C. Shah A.R. Five-year outcomes of surgically treated symptomatic epiretinal membranes with and without internal limiting membrane peeling.Ophthalmic Surg Lasers Imaging Retina. 2018; 49: 296-302Crossref PubMed Scopus (8) Google Scholar These findings likely reflect the progressive resolution of cystoid macular edema that occurs postoperatively, but it is important to note that fluctuations in central retinal thickness are common within the first postoperative year. Opponents against a combined procedure for ILM removal during ERM surgery highlight that with no difference in visual outcomes, peeling the ILM subjects patients to unnecessary risks and complications that would otherwise not come into play. Common complications associated with ILM peeling in ERM surgeries related to either surgical technique or intraoperative complications include macular holes, visual field defects, retinal toxicity from surgical dyes, and photoreceptor dysfunction.2Tadayoni R. Paques M. Girmens J.F. Massin P. Gaudric A. Persistence of fundus florescence after use of indocyanine green for macular surgery.Ophthalmology. 2003; 110: 604-608Abstract Full Text Full Text PDF PubMed Scopus (114) Google Scholar, 3Enaida H. Hisatomi T. Goto Y. Hata Y. Ueno A. Ishibashi T. Preclinical investigation of internal limiting membrane staining and peeling using intravitreal brilliant blue G.Retina. 2006; 26: 623-630Crossref PubMed Scopus (139) Google Scholar, 11Ahn S.J. Ahn J. Woo S.J. Park K.H. Photoreceptor change and visual outcome after idiopathic epiretinal membrane removal with or without additional internal limiting membrane peeling.Retina. 2014; 34: 172-181Crossref PubMed Scopus (47) Google Scholar, 13Amouyal F. Shah S.U. Pan C.K. Schwartz S.D. Hubschman J.P. Morphologic features and evolution of inner retinal dimples on optical coherence tomography after internal limiting membrane peeling.Retina. 2014; 34: 2096-2102Crossref PubMed Scopus (23) Google Scholar, 14Uemura A. Kanda S. Sakamoto Y. Kita H. Visual field defects after uneventful vitrectomy for epiretinal membrane with indocyanine green–assisted internal limiting membrane peeling.Am J Ophthalmol. 2003; 136: 252-257Abstract Full Text Full Text PDF PubMed Scopus (163) Google Scholar These adverse events have been well described and must always be considered to have an effect on the overall surgical outcomes. In conclusion, there has been an evolving trend among vitreoretinal surgeons to perform ILM peeling during ERM surgery. However, given current data, the role of ILM peeling in these cases is controversial and the role of a combined surgery remains unclear. With emerging longitudinal postoperative data we are developing a better understanding of visual outcomes, ERM recurrence, and anatomical changes after ERM surgeries. At this point, it appears that ILM peeling during ERM surgery does not result in a significantly greater improvement in BCVA compared with ERM peeling alone. However, combining ILM peeling does appear to be associated with a lower rate of ERM recurrence at least up until 5 years. A larger body of longitudinal evidence is needed to better understand which patients will have the best long-term outcomes from ERM surgery with ILM peeling. For now, vitreoretinal surgeons should continue to take patient-centred approach to planning ERM surgery while considering the operative risks in combination with the growing body of evidence of postoperative outcomes.