To analyze the functional impact of ectopic inner foveal layers (EIFL), along with other clinical and optical coherence tomography biomarkers, on patients with epiretinal membrane (ERM) and preserved foveal layers’ segmentation undergoing ERM removal.
Retrospective review of consecutive patients with ERM who underwent pars plana vitrectomy with ERM peeling from December 2018 to December 2019. Baseline factors including age, gender, lens status, phacoemulsification at the time of surgery, tamponade agent, dye used for ERM and internal limiting membrane (ILM) enhancement, ILM peeling, best-corrected visual acuity (BCVA) and central macular thickness (CMT), presence and thickness of EIFL, thickness of outer nuclear layer (ONL), presence of a cotton ball, subfoveal state of photoreceptors, and presence of cystoid macular edema were included in a multivariable model having the BCVA at 12 months as the main outcome. The changes in EIFL and ONL thickness over time were also analyzed.
Fifty-one patients (58 eyes, 23 eyes in the no EIFL group, and 35 eyes in the EIFL group) were enrolled. The BCVA significantly improved over 12 months after surgery, regardless of the presence of EIFL (p < 0.001). Eyes with no EIFL had better BCVA at month 3 (p = 0.04), but this difference was no longer detectable at 6 and 12 months. The presence of EIFL was not associated with the final BCVA (p = 0.9), while the CMT at 12 months correlated with EIFL thickness (r = 0.8, p = 0.008).
Patients with EIFL could reach optimal visual acuity in the absence of disorganization of the inner retinal layers but should be warned of potentially longer healing times. None of the morphologic signs included in this study precluded good visual recovery on long-term follow-up.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Data are available upon request to the corresponding authors.
Statistical software (R) and statistical packages used for this study are open access and adequate reference is provided.
Iuliano L, Fogliato G, Gorgoni F, Corbelli E, Bandello F, Codenotti M (2019) Idiopathic epiretinal membrane surgery: safety, efficacy and patient related outcomes. Clin Ophthalmol 13:1253–1265. https://doi.org/10.2147/OPTH.S176120
Hosoda Y, Ooto S, Hangai M, Oishi A, Yoshimura N (2015) Foveal photoreceptor deformation as a significant predictor of postoperative visual outcome in idiopathic epiretinal membrane surgery. Invest Ophthalmol Vis Sci 56(11):6387–6393. https://doi.org/10.1167/iovs.15-16679
Tsunoda K, Watanabe K, Akiyama K, Usui T, Noda T (2012) Highly reflective foveal region in optical coherence tomography in eyes with vitreomacular traction or epiretinal membrane. Ophthalmology 119(3):581–587. https://doi.org/10.1016/j.ophtha.2011.08.026
Scheerlinck LM, van der Valk R, van Leeuwen R (2015) Predictive factors for postoperative visual acuity in idiopathic epiretinal membrane: a systematic review. Acta Ophthalmol 93(3):203–212. https://doi.org/10.1111/aos.12537
Govetto A, Lalane RA 3rd, Sarraf D, Figueroa MS, Hubschman JP (2017) Insights into epiretinal membranes: presence of ectopic inner foveal layers and a new optical coherence tomography staging scheme. Am J Ophthalmol 175:99–113. https://doi.org/10.1016/j.ajo.2016.12.006
Gonzalez-Saldivar G, Berger A, Wong D, Juncal V, Chow DR (2020) Ectopic inner foveal layer classification scheme predicts visual outcomes after epiretinal membrane surgery. Retina 40(4):710–717. https://doi.org/10.1097/IAE.0000000000002486
Govetto A, Virgili G, Rodriguez FJ, Figueroa MS, Sarraf D, Hubschman JP (2019) Functional and anatomical significance of the ectopic inner foveal layers in eyes with idiopathic epiretinal membranes: surgical results at 12 months. Retina 39(2):347–357. https://doi.org/10.1097/IAE.0000000000001940
Govetto A, Bhavsar KV, Virgili G, Gerber MJ, Freund KB, Curcio CA, Burgoyne CF, Hubschman JP, Sarraf D (2017) Tractional abnormalities of the central foveal bouquet in epiretinal membranes: clinical spectrum and pathophysiological perspectives. Am J Ophthalmol 184:167–180. https://doi.org/10.1016/j.ajo.2017.10.011
Team RDC (2010) R: a language and enviroment for statistical computing. R Foundation for Statistical Computing, Vienna
Tibshirani R (1996) Regression shrinkage and selection via the lasso. J R Stat Soc Ser B Methodol 58(1):267–288
van Buuren S, Groothuis-Oudshoorn K (2011) Mice: multivariate imputation by chained equations in R. 45(3):67. https://doi.org/10.18637/jss.v045.i03
Cicinelli MV, Marchese A, Bandello F, Coppola M (2019) Inner retinal layer and outer retinal layer findings after macular hole surgery assessed by means of optical coherence tomography. J Ophthalmol 2019:3821479. https://doi.org/10.1155/2019/3821479
Coppola M, Marchese A, Cicinelli MV, Rabiolo A, Giuffre C, Gomarasca S, Querques G, Bandello F (2020) Macular optical coherence tomography findings after vitreoretinal surgery for rhegmatogenous retinal detachment. Eur J Ophthalmol 30(4):805–816. https://doi.org/10.1177/1120672120911334
Cicinelli MV, Carnevali A, Rabiolo A, Querques L, Zucchiatti I, Scorcia V, Bandello F, Querques G (2017) Clinical spectrum of macular-foveal capillaries evaluated with optical coherence tomography angiography. Retina 37(3):436–443. https://doi.org/10.1097/IAE.0000000000001199
Doguizi S, Sekeroglu MA, Ozkoyuncu D, Omay AE, Yilmazbas P (2018) Clinical significance of ectopic inner foveal layers in patients with idiopathic epiretinal membranes. Eye (Lond) 32:1652–1660. https://doi.org/10.1038/s41433-018-0153-9
Ooto S, Hangai M, Yoshimura N (2015) Effects of sex and age on the normal retinal and choroidal structures on optical coherence tomography. Curr Eye Res 40(2):213–225. https://doi.org/10.3109/02713683.2014.952828
Ooto S, Hangai M, Sakamoto A, Tomidokoro A, Araie M, Otani T, Kishi S, Matsushita K, Maeda N, Shirakashi M, Abe H, Takeda H, Sugiyama K, Saito H, Iwase A, Yoshimura N (2010) Three-dimensional profile of macular retinal thickness in normal Japanese eyes. Invest Ophthalmol Vis Sci 51(1):465–473. https://doi.org/10.1167/iovs.09-4047
Song WK, Lee SC, Lee ES, Kim CY, Kim SS (2010) Macular thickness variations with sex, age, and axial length in healthy subjects: a spectral domain-optical coherence tomography study. Invest Ophthalmol Vis Sci 51(8):3913–3918. https://doi.org/10.1167/iovs.09-4189
Ooto S, Hangai M, Tomidokoro A, Saito H, Araie M, Otani T, Kishi S, Matsushita K, Maeda N, Shirakashi M, Abe H, Ohkubo S, Sugiyama K, Iwase A, Yoshimura N (2011) Effects of age, sex, and axial length on the three-dimensional profile of normal macular layer structures. Invest Ophthalmol Vis Sci 52(12):8769–8779. https://doi.org/10.1167/iovs.11-8388
Kawasaki R, Wang JJ, Mitchell P, Aung T, Saw SM, Wong TY, Singapore Malay Eye Study G (2008) Racial difference in the prevalence of epiretinal membrane between Caucasians and Asians. Br J Ophthalmol 92(10):1320–1324. https://doi.org/10.1136/bjo.2008.144626
Clayton JA, Davis AF (2015) Sex/gender disparities and women's eye health. Curr Eye Res 40(2):102–109. https://doi.org/10.3109/02713683.2014.986333
Kofod M, la Cour M (2012) Quantification of retinal tangential movement in epiretinal membranes. Ophthalmology 119(9):1886–1891. https://doi.org/10.1016/j.ophtha.2012.03.022
Takagi S, Kudo S, Yokota H, Akiba M, Mandai M, Hirami Y, Takahashi M, Kurimoto Y, Ishida M (2019) Assessment of the deformation of the outer nuclear layer in the Epiretinal membrane using spectral-domain optical coherence tomography. BMC Ophthalmol 19(1):113. https://doi.org/10.1186/s12886-019-1124-z
Port AD, Nolan JG, Siegel NH, Chen X, Ness SD, Subramanian ML (2021) Combined phaco-vitrectomy provides lower costs and greater area under the curve vision gains than sequential vitrectomy and phacoemulsification. Graefes Arch Clin Exp Ophthalmol 259(1):45–52. https://doi.org/10.1007/s00417-020-04877-4
Hamoudi H, Correll Christensen U, La Cour M (2018) Epiretinal membrane surgery: an analysis of 2-step sequential- or combined phacovitrectomy surgery on refraction and macular anatomy in a prospective trial. Acta Ophthalmol 96(3):243–250. https://doi.org/10.1111/aos.13572
Shi L, Chang JS, Suh LH, Chang S (2019) Differences in refractive outcomes between phacoemulsification for cataract alone and combined phacoemulsification and vitrectomy for epiretinal membrane. Retina 39(7):1410–1415. https://doi.org/10.1097/IAE.0000000000002153
Guber J, Pereni I, Scholl HPN, Guber I, Haynes RJ (2019) Outcomes after epiretinal membrane surgery with or without internal limiting membrane peeling. Ophthalmol Therapy 8(2):297–303. https://doi.org/10.1007/s40123-019-0185-7
Chabot G, Bourgault S, Cinq-Mars B, Tourville E, Caissie M (2017) Effect of air and sulfur hexafluoride (SF6) tamponade on visual acuity after epiretinal membrane surgery: a pilot study. Can J Ophthalmol 52(3):269–272. https://doi.org/10.1016/j.jcjo.2016.11.004
Cismondi F, Fialho AS, Vieira SM, Reti SR, Sousa JM, Finkelstein SN (2013) Missing data in medical databases: impute, delete or classify? Artif Intell Med 58(1):63–72. https://doi.org/10.1016/j.artmed.2013.01.003
Ethics approval and consent to participate
The study received the approval of the San Gerardo ASST Monza IRB. Patients signed written consent at the time of enrollment to be included in observational clinical research studies.
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Coppola, M., Brambati, M., Cicinelli, M.V. et al. The visual outcomes of idiopathic epiretinal membrane removal in eyes with ectopic inner foveal layers and preserved macular segmentation. Graefes Arch Clin Exp Ophthalmol (2021). https://doi.org/10.1007/s00417-021-05102-6
- Epiretinal membrane
- Ectopic inner foveal layer
- Pars plana vitrectomy
- Optical coherence tomography