Evaluation of primary internal limiting membrane peeling in cases with rhegmatogenous retinal detachment

Mohamed Esmail Abdullah, Hossam Eldeen Mohammad Moharram, Ahmed Shawkat Abdelhalim, Khaled Mohamed Mourad, Mohamed Farouk Abdelkader, Mohamed Esmail Abdullah, Hossam Eldeen Mohammad Moharram, Ahmed Shawkat Abdelhalim, Khaled Mohamed Mourad, Mohamed Farouk Abdelkader

Abstract

Background: Epiretinal membranes (ERMs) have been reported after pars plana vitrectomy (PPV) for rhegmatogenous retinal detachment (RRD). Peeling of the internal limiting membrane (ILM) can prevent post-PPV ERM formation but has a potential negative impact on macular structure and function.

Purpose: To investigate the anatomical and functional outcomes of ILM peeling during PPV for primary RRD.

Methods: This was a prospective nonrandomized study that included 60 eyes of 60 patients with a primary macula-off RRD and less than grade C proliferative vitreoretinopathy (PVR). Eyes were allocated into 2 groups; Group A underwent PPV without ILM peeling and Group B had ILM peeling. At postoperative month 6, all patients underwent retinal imaging using spectral domain optical coherence tomography (OCT) and OCT angiography and macular function was assessed using multifocal electroretinogram (mfERG). Baseline characteristics and postoperative anatomical and visual outcomes were recorded and statistically analyzed.

Results: We enrolled 30 eyes of 30 patients in each group. In Group A, mean age was 44.6 years, while the mean age of Group B patients was 49.9 years. Postoperative LogMAR visual acuity was significantly better in Group A than in Group B (p < 0.001). ERMs were demonstrated on OCT in 13.3% of Group A and none of Group B patients (p = 0.04). Retinal dimples were found in 53.3% of Group B and none of Group A eyes (p < 0.001). OCTA showed a greater vessel density of the superficial capillary plexus (SCP) in Group A compared to Group B eyes (p = 0.046), while no difference was found regarding deep capillary vessel density (p = 0.7). Mean amplitude of mfERG P1 wave was significantly higher in Group A eyes than in Group B (p = 0.002). Both the SCP vessel density and P1 amplitude were positively correlated with visual acuity (p < 0.001).

Conclusion: This study suggests that ILM peeling prevents ERM development in eyes undergoing PPV for uncomplicated macula-off RRD, but potential damage to macular structure and function were found.Trial registration Retrospectively registered on 09/24/2019 on ClinicalTrials.gov with an ID of NCT04139811.

Keywords: Electroretinography; Optical coherence tomography; Peeling of internal limiting membrane (ILM); Retina; Retinal detachment; Vitrectomy; Vitreoretinal surgery; Vitreous body.

Conflict of interest statement

Competing interestsThe authors declare that they have no competing interests.

© The Author(s) 2020.

Figures

Fig. 1
Fig. 1
a B-scan SD-OCT of the macula of a Group A patient showing a thick epiretinal membrane (ERM) causing macular pucker, thickening and cystoid degeneration after pars plana vitrectomy. b B-scan SD-OCT of the macula of a Group B patient showing dimples on the inner retinal surface after pars plana vitrectomy and peeling of the internal limiting membrane (ILM)
Fig. 2
Fig. 2
Top row represents a Group A eye. a An optical coherence tomography angiography (OCTA) macula 6 × 6 mm scan showing the slab representing the superficial capillary plexus (SCP). b En-face OCT image that corresponds to the OCTA slab in A. c The color-coded flow density map of the superficial vessel density (warmer colors represent greater flow density). Bottom row represents a Group B eye. d An OCTA macula 6 × 6 mm scan showing the slab representing the superficial capillary plexus (SCP). e En-face OCT image that corresponds to the OCTA slab in D showing retinal dimples at the level of the nerve fiber layer. f The color-coded flow density map of the superficial vessel density
Fig. 3
Fig. 3
a Multifocal electroretinogram (mfERG) of a Group A eye. Left. Amplitude of P1 in nV/deg2 in topographic display around the fovea. Right. Three-dimensional topography of P1 amplitude (nV/deg2). b Multifocal electroretinogram (mfERG) of a Group B eye. Left. Amplitude of P1 in nV/deg2 in topographic display around the fovea. Right. Three-dimensional topography of P1 amplitude (nV/deg2)

References

    1. Abdelkader E, Lois N. Internal limiting membrane peeling in vitreo-retinal surgery. Surv Ophthalmol. 2008;53(4):368–396. doi: 10.1016/j.survophthal.2008.04.006.
    1. Sandali O, El Sanharawi M, Basli E, Bonnel S, Lecuen N, Barale PO, Borderie V, Laroche L, Monin C. Epiretinal membrane recurrence: incidence, characteristics, evolution, and preventive and risk factors. Retina. 2013;33(10):2032–2038. doi: 10.1097/IAE.0b013e31828d2fd6.
    1. Fallico M, Russo A, Longo A, Pulvirenti A, Avitabile T, Bonfiglio V, Castellino N, Cennamo G, Reibaldi M. Internal limiting membrane peeling versus no peeling during primary vitrectomy for rhegmatogenous retinal detachment: A systematic review and meta-analysis. PLoS One. 2018;13:7. doi: 10.1371/journal.pone.0201010.
    1. Katira RC, Zamani M, Berinstein DM, Garfinkel RA. Incidence and characteristics of macular pucker formation after primary retinal detachment repair by pars plana vitrectomy alone. Retina. 2008;28(5):744–748. doi: 10.1097/IAE.0b013e318162b031.
    1. Martinez-Castillo V, Boixadera A, Distefano L, Zapata M, Garcia-Arumi J. Epiretinal membrane after pars plana vitrectomy for primary pseudophakic or aphakic rhegmatogenous retinal detachment: incidence and outcomes. Retina. 2012;32(7):1350–1355. doi: 10.1097/IAE.0b013e318242b965.
    1. Nam KY, Kim JY. Effect of internal limiting membrane peeling on the development of epiretinal membrane after pars plana vitrectomy for primary rhegmatogenous retinal detachment. Retina. 2015;35(5):880–885. doi: 10.1097/IAE.0000000000000421.
    1. Forlini M, Date P, Ferrari LM, Lorusso M, Lecce G, Verdina T, Neri G, Benatti C, Rossini P, Bratu A, et al. Comparative analysis of retinal reattachment surgery with or without internal limiting membrane peeling to prevent postoperative macular pucker. Retina. 2018;38(9):1770–1776. doi: 10.1097/IAE.0000000000001775.
    1. Akiyama K, Fujinami K, Watanabe K, Tsunoda K, Noda T. Internal limiting membrane peeling to prevent post-vitrectomy epiretinal membrane development in retinal detachment. Am J Ophthalmol. 2016;171:1–10. doi: 10.1016/j.ajo.2016.08.015.
    1. Eissa M, Abdelhakim M, Macky TA, Khafagy MM, Mortada HA. Functional and structural outcomes of ILM peeling in uncomplicated macula-off RRD using microperimetry & en-face OCT. Graefes Arch Clin Exp Ophthalmol. 2018;256(2):249–257. doi: 10.1007/s00417-017-3875-7.
    1. Rao RC, Blinder KJ, Smith BT, Shah GK. Internal limiting membrane peeling for primary rhegmatogenous retinal detachment repair. Ophthalmology. 2013;120(5):1102–1103. doi: 10.1016/j.ophtha.2012.12.010.
    1. Garweg JG, Deiss M, Pfister IB, Gerhardt C. Impact of inner limiting membrane peeling on visual recovery after vitrectomy for primary rhegmatogenous retinal detachment involving the fovea. Retina. 2019;39(5):853–859. doi: 10.1097/IAE.0000000000002046.
    1. Aras C, Arici C, Akar S, Muftuoglu G, Yolar M, Arvas S, Baserer T, Koyluoglu N. Peeling of internal limiting membrane during vitrectomy for complicated retinal detachment prevents epimacular membrane formation. Graefes Arch Clin Exp Ophthalmol. 2009;247(5):619–623. doi: 10.1007/s00417-008-1025-y.
    1. Foveau P, Leroy B, Berrod JP, Conart JB. Internal limiting membrane peeling in macula-off retinal detachment complicated by grade b proliferative vitreoretinopathy. Am J Ophthalmol. 2018;191:1–6. doi: 10.1016/j.ajo.2018.03.037.
    1. Blanco-Teijeiro MJ, Bande Rodriguez M, Mansilla Cunarro R, Paniagua Fernandez L, Ruiz-Oliva Ruiz F, Pineiro Ces A. Effects of internal limiting membrane peeling during vitrectomy for macula-off primary rhegmatogenous retinal detachment. Eur J Ophthalmol. 2018;28(6):706–713. doi: 10.1177/1120672117750055.
    1. Hood DC, Bach M, Brigell M, Keating D, Kondo M, Lyons JS, Marmor MF, McCulloch DL, Palmowski-Wolfe AM. ISCEV standard for clinical multifocal electroretinography (mfERG) Documenta ophthalmologica Adv Ophthalmol. 2012;124(1):1–13. doi: 10.1007/s10633-011-9296-8.
    1. Kiss CG, Richter-Muksch S, Sacu S, Benesch T, Velikay-Parel M. Anatomy and function of the macula after surgery for retinal detachment complicated by proliferative vitreoretinopathy. Am J Ophthalmol. 2007;144(6):872–877. doi: 10.1016/j.ajo.2007.08.001.
    1. Hisatomi T, Enaida H, Sakamoto T, Kanemaru T, Kagimoto T, Yamanaka I, Ueno A, Nakamura T, Hata Y, Ishibashi T. Cellular migration associated with macular hole: a new method for comprehensive bird’s-eye analysis of the internal limiting membrane. Arch Ophthalmol. 2006;124(7):1005–1011. doi: 10.1001/archopht.124.7.1005.
    1. Hisatomi T, Enaida H, Sakamoto T, Kagimoto T, Ueno A, Nakamura T, Hata Y, Ishibashi T. A new method for comprehensive bird’s-eye analysis of the surgically excised internal limiting membrane. Am J Ophthalmol. 2005;139(6):1121–1122. doi: 10.1016/j.ajo.2004.11.051.
    1. Hisatomi T, Tachibana T, Notomi S, Koyanagi Y, Murakami Y, Takeda A, Ikeda Y, Yoshida S, Enaida H, Murata T, et al. Internal limiting membrane peeling-dependent retinal structural changes after vitrectomy in rhegmatogenous retinal detachment. Retina. 2018;38(3):471–479. doi: 10.1097/IAE.0000000000001558.
    1. Deltour JB, Grimbert P, Masse H, Lebreton O, Weber M. Detrimental effects of active internal limiting membrane peeling during epiretinal membrane surgery: microperimetric analysis. Retina. 2017;37(3):544–552. doi: 10.1097/IAE.0000000000001179.
    1. Steel DH, Dinah C, Habib M, White K. ILM peeling technique influences the degree of a dissociated optic nerve fibre layer appearance after macular hole surgery. Graefes Arch Clin Exp Ophthalmol. 2015;253(5):691–698. doi: 10.1007/s00417-014-2734-z.
    1. Fukukita H, Ito Y, Iwase T, Kaneko H, Yasuda S, Kataoka K, Terasaki H. Inner macular changes after vitrectomy with internal limiting membrane peeling for rhegmatogenous retinal detachment: similarity with alport syndrome. Retina. 2018;39(12):2332–2340. doi: 10.1097/IAE.0000000000002310.
    1. Liu J, Chen Y, Wang S, Zhang X, Zhao P. Evaluating inner retinal dimples after inner limiting membrane removal using multimodal imaging of optical coherence tomography. BMC Ophthalmol. 2018;18(1):155. doi: 10.1186/s12886-018-0828-9.
    1. Alkabes M, Salinas C, Vitale L, Bures-Jelstrup A, Nucci P, Mateo C. En face optical coherence tomography of inner retinal defects after internal limiting membrane peeling for idiopathic macular hole. Invest Ophthalmol Vis Sci. 2011;52(11):8349–8355. doi: 10.1167/iovs.11-8043.
    1. Rispoli M, Le Rouic JF, Lesnoni G, Colecchio L, Catalano S, Lumbroso B. Retinal surface en face optical coherence tomography: a new imaging approach in epiretinal membrane surgery. Retina. 2012;32(10):2070–2076. doi: 10.1097/IAE.0b013e3182562076.
    1. Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G. Optical coherence tomography angiography. Prog Retin Eye Res. 2018;64:1–55. doi: 10.1016/j.preteyeres.2017.11.003.
    1. Mastropasqua L, Borrelli E, Carpineto P, Toto L, Di Antonio L, Mattei PA, Mastropasqua R. Microvascular changes after vitrectomy with internal limiting membrane peeling: an optical coherence tomography angiography study. Int Ophthalmol. 2018;38(4):1465–1472. doi: 10.1007/s10792-017-0608-1.
    1. Hood DC, Greenstein V, Frishman L, Holopigian K, Viswanathan S, Seiple W, Ahmed J, Robson JG. Identifying inner retinal contributions to the human multifocal ERG. Vision Res. 1999;39(13):2285–2291. doi: 10.1016/S0042-6989(98)00296-X.
    1. Lim JW, Cho JH, Kim HK. Assessment of macular function by multifocal electroretinography following epiretinal membrane surgery with internal limiting membrane peeling. Clin Ophthalmol. 2010;4:689–694. doi: 10.2147/OPTH.S12042.
    1. Tari SR, Vidne-Hay O, Greenstein VC, Barile GR, Hood DC, Chang S. Functional and structural measurements for the assessment of internal limiting membrane peeling in idiopathic macular pucker. Retina. 2007;27(5):567–572. doi: 10.1097/IAE.0b013e31802ea53d.

Source: PubMed

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