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Displacement of the retina and changes in the foveal avascular zone area after internal limiting membrane peeling for epiretinal membrane

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Abstract

Purpose

We investigated the differences in displacement of the outer and inner macular retina toward the optic disc after vitrectomy with internal limiting membrane (ILM) peeling for epiretinal membrane (ERM). Foveal avascular zone (FAZ) area changes were also investigated.

Study design

Retrospective observational study

Methods

This retrospective observational case series included 45 eyes of 43 patients that underwent vitrectomy with ERM and ILM peeling for ERM and 38 normal eyes. The locations of the centroid of the FAZ (C-FAZ, center of the foveal inner retina) and foveal bulge (center of the foveal outer retina) were determined using 3×3mm superficial optical coherence tomography angiography. C-FAZ and foveal bulge displacements, and the pre- and postoperative FAZ areas and their associated factors, were investigated.

Results

Postoperative C-FAZ dislocated significantly more toward the optic disc than in pre-operative or normal eyes (P<0.001). C-FAZ and foveal bulge displaced toward the optic disc after surgery; C-FAZ showed significantly greater displacement than foveal bulge (P<0.001). The pre- and postoperative FAZ areas were correlated (P=0.01). Preoperative FAZ areas ≧0.10mm2 were reduced after surgery, and FAZ areas < 0.10mm2 were increased, independent of foveal displacement.

Conclusion

ILM peeling during vitrectomy for ERM caused larger displacement of the inner and smaller displacement of the outer retinas, towards the optic disc. Postoperative changes in the FAZ area were dependent on the baseline FAZ area, but not on the foveal displacement. ILM may physiologically exert centrifugal tractional forces on the fovea.

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Data availability

The datasets analyzed during the current study are not publicly available because of the hospital’s policy to protect personal information of the participants but are available from the corresponding author on reasonable request.

References

  1. Park DW, Sipperley JO, Sneed SR, Dugel PU, Jacobsen J. Macular hole surgery with internal-limiting membrane peeling and intravitreous air. Ophthalmology. 1999;106:1392–8.

    Article  CAS  Google Scholar 

  2. Brooks HL Jr. Macular hole surgery with and without internal limiting membrane peeling. Ophthalmology. 2000;107:1939–48.

    Article  Google Scholar 

  3. Kadonosono K, Itoh N, Uchio E, Nakamura S, Ohno S. Staining of internal limiting membrane in macular hole surgery. Arch Ophthalmol. 2000;118:1116–8.

    Article  CAS  Google Scholar 

  4. Smiddy WE, Feuer W, Cordahi G. Internal limiting membrane peeling in macular hole surgery. Ophthalmology. 2001;108:1471–6.

    Article  CAS  Google Scholar 

  5. Haritoglou C, Gass CA, Schaumberger M, Ehrt O, Gandorfer A, Kampik A. Macular changes after peeling of the internal limiting membrane in macular hole surgery. Am J Ophthalmol. 2001;132:363–8.

    Article  CAS  Google Scholar 

  6. Kumagai K, Furukawa M, Ogino N, Uemura A, Demizu S, Larson E. Vitreous surgery with and without internal limiting membrane peeling for macular hole repair. Retina. 2004;24:721–7.

    Article  Google Scholar 

  7. Enaida H, Hisatomi T, Hata Y, Ueno A, Goto Y, Yamada T, et al. Brilliant blue G selectively stains the internal limiting membrane/brilliant blue G-assisted membrane peeling. Retina. 2006;26:631–6.

    Google Scholar 

  8. Almony A, Nudleman E, Shah GK, Blinder KJ, Eliott DB, Mittra RA, et al. Techniques, rationale, and outcomes of internal limiting membrane peeling. Retina. 2012;32:877–91.

    Article  Google Scholar 

  9. Bovey EH, Uffer S, Achache F. Surgery for epimacular membrane: impact of retinal internal limiting membrane removal on functional outcome. Retina. 2004;24:728–35.

    Article  Google Scholar 

  10. Kwok AKH, Lai TYY, Yuen KSC. Epiretinal membrane surgery with or without internal limiting membrane peeling. Clin Exp Ophthalmol. 2005;33:379–85.

    Article  Google Scholar 

  11. Hattori K, Kataoka K, Takeuchi J, Ito Y, Terasaki H. Predictive Factors of Surgical Outcomes in Vitrectomy for Myopic Traction Maculopathy. Retina. 2018;38(Suppl 1):S23–30.

    Article  Google Scholar 

  12. Taniuchi S, Hirakata A, Itoh Y, Hirota K, Inoue M. Vitrectomy with or without internal limiting membrane peeling for each stage of myopic traction maculopathy. Retina. 2013;33:2018–25.

    Article  Google Scholar 

  13. Shimada N, Sugamoto Y, Ogawa M, Takase H, Ohno-Matsui K. Fovea-sparing internal limiting membrane peeling for myopic traction maculopathy. Am J Ophthalmol. 2012;154:693–701.

    Article  Google Scholar 

  14. Shiraki N, Wakabayashi T, Ikuno Y, Matsumura N, Sato S, Sakaguchi H, et al. Fovea-sparing versus standard internal limiting membrane peeling for myopic traction maculopathy: a study of 102 consecutive cases. Ophthalmol Retina. 2020;4:1170–80.

    Article  Google Scholar 

  15. Iwasaki M, Miyamoto H, Okushiba U, Imaizumi H. Fovea-sparing internal limiting membrane peeling versus complete internal limiting membrane peeling for myopic traction maculopathy. Jpn J Ophthalmol. 2020;64:13–21.

    Article  CAS  Google Scholar 

  16. Ho TC, Yang CM, Huang JS, Yang CH, Yeh PT, Chen TC, et al. Long-term outcome of foveolar internal limiting membrane nonpeeling for myopic traction maculopathy. Retina. 2014;34:1833–40.

    Article  Google Scholar 

  17. Kawano K, Ito Y, Kondo M, Ishikawa K, Kachi S, Ueno S, et al. Displacement of foveal area toward optic disc after macular hole surgery with internal limiting membrane peeling. Eye (Lond). 2013;27:871–7.

    Article  CAS  Google Scholar 

  18. Ishida M, Ichikawa Y, Higashida R, Tsutsumi Y, Ishikawa A, Imamura Y. Retinal displacement toward optic disc after internal limiting membrane peeling for idiopathic macular hole. Am J Ophthalmol. 2014;157:971–7.

    Article  Google Scholar 

  19. Akahori T, Iwase T, Yamamoto K, Ra E, Kawano K, Ito Y, et al. Macular displacement after vitrectomy in eyes with idiopathic macular hole determined by optical coherence tomography angiography. Am J Ophthalmol. 2018;189:111–21.

    Article  Google Scholar 

  20. Yoshikawa M, Murakami T, Nishijima K, Uji A, Ogino K, Horii T, et al. Macular migration toward the optic disc after inner limiting membrane peeling for diabetic macular edema. Invest Ophthalmol Vis Sci. 2013;54:629–35.

    Article  Google Scholar 

  21. Tadayoni R, Paques M, Massin P, Mouki-Benani S, Mikol J, Gaudric A. Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology. 2001;108:2279–83.

    Article  CAS  Google Scholar 

  22. Ito Y, Terasaki H, Takahashi A, Yamakoshi T, Kondo M, Nakamura M. Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular holes. Ophthalmology. 2005;112:1415–20.

    Article  Google Scholar 

  23. Mitamura Y, Ohtsuka K. Relationship of dissociated optic nerve fiber layer appearance to internal limiting membrane peeling. Ophthalmology. 2005;112:1766–70.

    Article  Google Scholar 

  24. Spaide RF. “Dissociated optic nerve fiber layer appearance” after internal limiting membrane removal is inner retinal dimpling. Retina. 2012;32:1719–26.

    Article  Google Scholar 

  25. Sakimoto S, Ikuno Y, Fujimoto S, Sakaguchi H, Nishida K. Characteristics of the retinal surface after internal limiting membrane peeling in highly myopic eyes. Am J Ophthalmol. 2014;158(762–8): e1.

    Google Scholar 

  26. Amouyal F, Shah SU, Pan CK, Schwartz SD, Hubschman JP. Morphologic features and evolution of inner retinal dimples on optical coherence tomography after internal limiting membrane peeling. Retina. 2014;34:2096–102.

    Article  CAS  Google Scholar 

  27. Fukukita H, Ito Y, Iwase T, Kaneko H, Yasuda S, Kataoka K, et al. Inner macular changes after vitrectomy with internal limiting membrane peeling for rhegmatogenous retinal detachment: similarity with alport syndrome. Retina. 2019;39:2332–40.

    Article  Google Scholar 

  28. Tuifua TS, Abraham JR, Srivastava SK, Kaiser PK, Reese J, Ehlers JP. Longitudinal ellipsoid zone and outer retinal integrity dynamics after epiretinal membrane surgery. Retina. 2022;42:265–73.

    Article  Google Scholar 

  29. Kuppuswamy Parthasarathy M, Bhende M. Deviation in the position of foveal bulge from foveal center in normal subjects measured using spectral-domain OCT. Ophthalmol Retina. 2018;2:337–42.

    Article  Google Scholar 

  30. Hasegawa T, Ueda T, Okamoto M, Ogata N. Relationship between presence of foveal bulge in optical coherence tomographic images and visual acuity after rhegmatogenous retinal detachment repair. Retina J Retinal Vitreous Dis. 2014;34:1848–53.

    Google Scholar 

  31. Govetto A, Lalane RA 3rd, Sarraf D, Figueroa MS, Hubschman JP. Insights into epiretinal membranes: presence of ectopic inner foveal layers and a new optical coherence tomography staging scheme. Am J Ophthalmol. 2017;175:99–113.

    Article  Google Scholar 

  32. Kitagawa Y, Shimada H, Shinojima A, Nakashizuka H. Foveal avascular zone area analysis using optical coherence tomography angiography before and after idiopathic epiretinal membrane surgery. Retina. 2019;39:339–46.

    Article  Google Scholar 

  33. Okawa Y, Maruko I, Kawai M, Hasegawa T, Arakawa H, Iida T. Foveal structure and vasculature in eyes with idiopathic epiretinal membrane. PLoS ONE. 2019;14: e0214881.

    Article  CAS  Google Scholar 

  34. Kumagai K, Furukawa M, Suetsugu T, Ogino N. Foveal avascular zone area after internal limiting membrane peeling for epiretinal membrane and macular hole compared with that of fellow eyes and healthy controls. Retina. 2018;38:1786–94.

    Article  Google Scholar 

  35. Momota A, Iwase T, Akahori T, Goto K, Yamamoto K, Ra E, et al. Association between displacement and thickness of macula after vitrectomy in eyes with epiretinal membrane. Sci Rep. 2020;10:13227.

    Article  CAS  Google Scholar 

  36. Kunikata H, Yasuda M, Aizawa N, Osada U, Nishiguchi KM, Abe T, et al. Retinal sensitivity and vessel density after macular hole surgery with the superior inverted internal limiting membrane flap technique. Retina. 2021;41:45–53.

    Article  Google Scholar 

  37. Kaneko H, Hirata N, Shimizu H, Kataoka K, Nonobe N, Mokuno K, et al. Effect of internal limiting membrane peeling on visual field sensitivity in eyes with epiretinal membrane accompanied by glaucoma with hemifield defect and myopia. Jpn J Ophthalmol. 2021;65:380–7.

    Article  Google Scholar 

  38. Tsuchiya S, Higashide T, Sugiyama K. Visual field changes after vitrectomy with internal limiting membrane peeling for epiretinal membrane or macular hole in glaucomatous eyes. PLoS ONE. 2017;12: e0177526.

    Article  Google Scholar 

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Acknowledgements

This work was supported in part by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 19K09989 to HT and 16K11265 to YI.

Funding

Japan Society for the Promotion of Science,16K11265,Yasuki Ito, 19K09989, Hiroko Terasaki.

Author information

Authors and Affiliations

  1. Department of Ophthalmology, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, 466-8550, Japan

    Yosuke Taki, Yasuki Ito, Jun Takeuchi, Hirotaka Ito, Yuyako Nakano, Ai Fujita Sajiki, Etsuyo Horiguchi, Hikaru Ota, Keiko Kataoka & Hiroko Terasaki

  2. Department of Ophthalmology, Fujita Health University School of Medicine, Toyoake, Aichi, Japan

    Yasuki Ito

  3. Kyorin Eye Center, Kyorin University School of Medicine, Tokyo, Japan

    Keiko Kataoka

Authors
  1. Yosuke Taki
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  2. Yasuki Ito
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Corresponding author

Correspondence to Yasuki Ito.

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Conflicts of interest

Y. Taki, None; Y. Ito, Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events (Canon, Kowa, Santen, Bayer, ZEISS, Novartis, Pfizer); J. Takeuchi, None; H. Ito, None; Y. Nakano, None; A. F. Sajiki, None; E. Horiguchi, None; H. Ohta, None; K. Kataoka, Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events (Novartis, Senju, Santen, Boehringer Ingelheim, Bayer); H. Terasaki, Grants or contracts (ZEISS, Kowa, Otsuka, Senju, Santen, Alcon, Sanofi, Novartis, ROHTO, Bayer, Wakamoto, HOYA, Johnson & Johnson), Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events (Otsuka, Kowa, Santen, Senju, Sanofi, Alcon, ROHTO, Novartis, Wakamoto, Bayer), Support for attending meetings and/or travel (Bayer).

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Corresponding Author: Yasuki Ito

Supplementary Information

Below is the link to the electronic supplementary material.

10384_2022_964_MOESM1_ESM.tif

Supplementary Fig. 1 Retinal layer thickness measurement. Foveal thickness and retinal layer thickness of the entire retina, the inner retina (the inner limiting membrane to the outer plexiform layer), and the outer retina (the outer nuclear layer to the retinal pigment epithelium) were measured manually at 1 mm both nasally and temporally to the foveal center (foveal bulge) by using the caliper function of the built-in software of the swept source optical coherence tomography (SS-OCT) device. Supplementary file1 (TIF 20894 KB)

10384_2022_964_MOESM2_ESM.tif

Supplementary Fig. 2 Adjustment of the location of the pre- and postoperative optical coherence tomography (OCT) angiography images. Location of pre- and postoperative en face superficial OCT angiography images were overlaid (a and c), after adjusting the landmarks on choroidal OCT angiography images (b and d, yellow dotted line). Supplementary file2 (TIF 9212 KB)

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Taki, Y., Ito, Y., Takeuchi, J. et al. Displacement of the retina and changes in the foveal avascular zone area after internal limiting membrane peeling for epiretinal membrane. Jpn J Ophthalmol 67, 74–83 (2023). https://doi.org/10.1007/s10384-022-00964-7

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  • DOI: https://doi.org/10.1007/s10384-022-00964-7

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