The visual outcomes of idiopathic epiretinal membrane removal in eyes with ectopic inner foveal layers and preserved macular segmentation

Abstract

Purpose

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.

Methods

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.

Results

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).

Conclusion

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.

Fig. 1
Fig. 2
Fig. 3

Data availability

Data are available upon request to the corresponding authors.

Code availability

Statistical software (R) and statistical packages used for this study are open access and adequate reference is provided.

References

  1. 1.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    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

    Article  PubMed  Google Scholar 

  3. 3.

    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

    Article  PubMed  Google Scholar 

  4. 4.

    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

    Article  PubMed  Google Scholar 

  5. 5.

    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

    Article  Google Scholar 

  6. 6.

    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

    Article  PubMed  Google Scholar 

  7. 7.

    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

    Article  PubMed  Google Scholar 

  8. 8.

    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

    Article  Google Scholar 

  9. 9.

    Team RDC (2010) R: a language and enviroment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  10. 10.

    Tibshirani R (1996) Regression shrinkage and selection via the lasso. J R Stat Soc Ser B Methodol 58(1):267–288

    Google Scholar 

  11. 11.

    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

  12. 12.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    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

    Article  PubMed  Google Scholar 

  14. 14.

    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

    Article  PubMed  Google Scholar 

  15. 15.

    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

    Article  Google Scholar 

  16. 16.

    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

    Article  PubMed  Google Scholar 

  17. 17.

    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

    Article  PubMed  Google Scholar 

  18. 18.

    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

    Article  PubMed  Google Scholar 

  19. 19.

    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

    Article  PubMed  Google Scholar 

  20. 20.

    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

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    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

    Article  PubMed  Google Scholar 

  22. 22.

    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

    Article  Google Scholar 

  23. 23.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    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

    Article  PubMed  Google Scholar 

  25. 25.

    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

    Article  PubMed  Google Scholar 

  26. 26.

    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

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    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

    Article  Google Scholar 

  28. 28.

    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

    Article  PubMed  Google Scholar 

  29. 29.

    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

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

Michele Coppola: conceptualization, writing—original draft

Maria Vittoria Cicinelli, Maria Brambati, Alessandro Marchese: methodology, writing—review and editing

Emma Clara Zanzottera, Antonio Peroglio Deiro, Michal Post: visualization, data curation

Francesco Bandello: project administration, supervision

Corresponding author

Correspondence to Maria Vittoria Cicinelli.

Ethics declarations

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.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Supplementary Fig 1

Percentage of missing data. EIFL: ectopic inner foveal layer; ONL: outer nuclear layer; VA: visual acuity; CMT: central macular thickness (PDF 5 kb).

ESM 1

(PDF 46 kb).

ESM 2

(PDF 30 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Keywords

  • Epiretinal membrane
  • Ectopic inner foveal layer
  • Pars plana vitrectomy
  • Optical coherence tomography
  • Biomarkers