Skip to main content

Advertisement

SpringerLink
Log in

Macular peeling-induced retinal damage: clinical and histopathological evaluation after using different dyes

  • Retinal Disorders
  • Published:
Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To describe functional and histopathological findings after macular peeling using different dyes.

Methods

Prospective, randomized, comparative, interventional, and immunohistochemical study. Forty-five eyes from 45 patients with idiopathic epiretinal membrane (ERM) underwent pars plana chromovitrectomy with ERM and inner limiting membrane (ILM) using trypan blue 0.15% + brilliant blue 0.05% + lutein 2% in group 1 (15 eyes), trypan blue 0.15% + brilliant blue 0.025% + polyethylene glycol 3350 4% in group 2 (15 eyes), and indocyanine green 0.05% in group 3 (15 eyes). We evaluated visual acuity (VA) and macular sensitivity (MS) preoperatively, 1, 3, and 6 months after surgery. The expression of glial fibrillary acidic protein (GFAP) and neurofilament protein (NF) was assessed immunohistochemically on the ILMs peeled as markers of glial and neuronal cells.

Results

In group 1, both mean VA and MS were significantly better at 1 and 3 months after surgery (P < 0.05), whereas no significant difference was found after 6 months. GFAP and NF expression was significantly lower in group 1 (P < 0.05).

Conclusions

The ERM/ILM peeling is thought to rip off the intraretinal tissue, based on the amounts of GFAP and NF in the specimens. The use of lutein dyes reduces iatrogenic stress to the retinal tissue and allows a faster functional recovery in the first 3 months after surgery, suggesting a less iatrogenic adhesion to the retinal tissue.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Gupta P, Yee KM, Garcia P, Rosen RB, Parikh J, Hageman GS, Sadun AA, Sebag J (2011) Vitreoschisis in macular diseases. Br J Ophthalmol 95:376–380

    Article  PubMed  Google Scholar 

  2. Romano MR, Comune C, Ferrara M, Cennamo G, De Cillà S, Toto L, Cennamo G (2015) Retinal changes induced by epiretinal tangential forces J Ophthalmol 2015:372564

  3. Joshi M, Agrawal S, Christoforidis JB (2013) Inflammatory mechanisms of idiopathic epiretinal membrane formation. Mediat Inflamm:192582

  4. Kritzenberg M, Jungas B, Framme C et al (2011) Different collagen types define two types of idiopathic epiretinal membranes. Histopathology 58:953–965

    Article  Google Scholar 

  5. Zhao F, Gandorfer A, Haritoglou C et al (2013) Epiretinal cell proliferation in macular pucker and vitreoretinal traction syndrome: analysis of flat-mounted internal limiting membrane specimens. Retina 33:77–88

    Article  PubMed  Google Scholar 

  6. Bringmann A, Wiedemann P (2009) Involvement of Muller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol 247:865–883

    Article  PubMed  Google Scholar 

  7. Steel DH, Lotery AJ (2013) Idiopathic vitreomacular traction and macular hole: a comprehensive review of pathophysiology, diagnosis, and treatment. Eye (Lond) 27(Suppl 1):S1–S21

  8. Snead DRJ, James S, Snead MP (2008) Pathological changes in the vitreoretinal junction 1: epiretinal membrane formation. Eye (Lond) 22:1310–1317

    Article  CAS  Google Scholar 

  9. Kampik A (2012) Pathology of epiretinal membrane, idiopathic macular hole, and vitreomacular traction syndrome 32 Suppl 2:S194–8; discussion S198–9

  10. Romano MR, Cennamo G, Schiemer S, Rossi C, Sparnelli F, Cennamo G (2017) Deep and superficial OCT angiography changes after macular peeling: idiopathic vs diabetic epiretinal membranes. Graefes Arch Clin Exp Ophthalmol 255(4):681–689

    Article  PubMed  Google Scholar 

  11. Romano MR, Cennamo G, Cesarano I, Cardone D, Nicoletti G, Mastropasqua R, Cennamo G (2017) Changes of tangential traction after macular peeling: correlation between en face analysis and macular sensitivity. Curr Eye Res 42(5):780–788

    Article  PubMed  Google Scholar 

  12. Kenawy N, Wong D, Stappler T et al (2010) Does the presence of an epiretinal membrane alter the cleavage plane during internal limiting membrane peeling? Ophthalmology 117:320–323

    Article  PubMed  Google Scholar 

  13. Junemann AG, Rejdak R, Huchzermeyer C, Maciejewski R, Grieb P, Kruse FE, Zrenner E, Rejdak K, Petzold A (2015) Elevated vitreous body glial fibrillary acidic protein in retinal diseases. Graefes Arch Clin Exp Ophthalmol 253:2181–2186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397–424

    Article  PubMed  CAS  Google Scholar 

  15. Lewis GP, Fisher SK (2003) Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodelling and a comparison to vimentin expression. Int Rev Cytol 230:263–290

    Article  PubMed  CAS  Google Scholar 

  16. Sousa-Martins D, Caseli L, Figueiredo MC, Sa E, Cunha C, Mota-Filipe H, Souza-Lima A, Belfort R Jr, Rodrigues E, Maia M (2015) Comparing the mode of action of intraocular lutein-based dyes with synthetic dyes. Invest Ophthalmol Vis Sci 19:1993–2000

    Article  CAS  Google Scholar 

  17. Romano MR, Romano V, Vallejo-Garcia JL, Vinciguerra R, Romano M, Cereda M, Angi M, Valldeperas X, Costagliola C, Vinciguerra P (2014) Macular hypotrophy after internal limiting membrane removal for diabetic macular edema. Retina 34:1182–1189

    Article  PubMed  Google Scholar 

  18. Ripandelli G, Scarinci F, Piaggi P, Guidi G, Pileri M, Cupo G, Sartini MS, Parisi V, Baldanzellu S, Giusti C, Nardi M, Stirpe M, Lazzeri S (2015) Macular pucker: to peel or not to peel the internal limiting membrane? A microperimetric response. Retina 35:498–507

    Article  PubMed  Google Scholar 

  19. Petzold A, Junemana A, Reidak K et al (2009) A novel biomarker for retinal degeneration: vitreous body neurofilament proteins. J Neural Transm (Vienna) 116:1601–1606

    Article  CAS  Google Scholar 

  20. Al-Halafi AM (2013) Chromovitrectomy: update. Saudi J Ophthalmol 27:271–276

    Article  PubMed  PubMed Central  Google Scholar 

  21. Romano MR, Cennamo G, Amoroso F, Montorio D, Castellani C, Reibaldi M, Cennamo G (2017) Intraretinal changes in the presence of epiretinal traction. Graefes Arch Clin Exp Ophthalmol 255(1):31–38

    Article  PubMed  Google Scholar 

  22. Patel JI, Hykin PG, Schadt M, Luong V, Fitzke F, Gregor ZJ (2006) Pars plana vitrectomy with and without peeling of the inner limiting membrane for diabetic macular edema. Retina 26:5–13

    Article  PubMed  Google Scholar 

  23. Eckardt C, Eckardt U, Groos S, Luciano L, Reale E (1997) Removal of the internal limiting membrane in macular holes. Clinical and morphological findings. Ophthalmologe 94:545–551

    Article  PubMed  CAS  Google Scholar 

  24. Terasaki H, Miyake Y, Nomura R, Piao CH, Hori K, Niwa T, Kondo M (2001) Focal macular ERGs in eyes after removal of macular ILM during macular hole surgery. Invest Ophthalmol Vis Sci 42:229–234

    PubMed  CAS  Google Scholar 

  25. Pichi F, Lembo A, Morara M, Veronese C, Alkabes M, Nucci P, Ciardella AP (2014) Early and late inner retinal changes after inner limiting membrane peeling. Int Ophthalmol 34:437–446

    Article  PubMed  Google Scholar 

  26. Romano MR, Vallejo-Garcia JL, Camesasca FI, Vincoguerra P, Costagliola C (2012) Vitreo-papillary adhesion as a prognostic factor in pseudo- and lamellar macular holes. Eye (Lond) 26:810–815

    Article  CAS  Google Scholar 

  27. Hernandez F, Alpizar-Alvarez N, Wu L (2014) Chromovitrectomy: an update. J Ophthalmic Vis Res 9:251–259

    PubMed  PubMed Central  Google Scholar 

  28. Penha FM, Pons M, Costa EF, Rodrigues EB, Maia M, Marin-Castaño ME, Farah ME (2013) Effect of vital dyes on retinal pigmented epithelial cell viability and apoptosis: implications for chromovitrectomy. Ophthalmologica 230:41–50

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Penha FM, Pons M, Costa EF Barros NM, Rodrigues EB, Cardoso EB, Dib E, Maia M, Marin-Castaño ME, Farah ME (2013) Retinal pigmented epithelial cells cytotoxicity and apoptosis through activation of the mitochondrial intrinsic pathway: role of indocyanine green, brilliant blue and implications for chromovitrectomy. PLoS One 10;8:e64094

  30. Notomi S, Hisatomi T, Kanemaru T, Takeda A, Ikeda Y, Enaida H, Kroemer G, Ishibashi T (2011) Critical involvement of extracellular ATP acting on P2RX7 purinergic receptors in photoreceptor cell death. Am J Pathol 179:2798–2809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Balaiya S, Brar VS, Murthy RK, Chalam KV (2011) Comparative in vitro safety analysis of dyes for chromovitrectomy: indocyanine green, brilliant blue green, bromophenol blue, and infracyanine green. Retina 31:1128–1136

    Article  PubMed  CAS  Google Scholar 

  32. Ejstrup R, la Cour M, Heegaard S, Kiilgaard JF (2012) Toxicity profiles of subretinal indocyanine green, Brilliant Blue G, and triamcinolone acetonide: a comparative study. Graefes Arch Clin Exp Ophthalmol 250:669–677

    Article  PubMed  CAS  Google Scholar 

  33. Haritoglou C, Mauell S, Benoit M, Schumann RG, Henrich PB, Wolf A, Kampik A (2013) Vital dyes increase the rigidity of the internal limiting membrane. Eye (Lond) 27:1308–1315

    Article  PubMed Central  CAS  Google Scholar 

  34. Wollensak G (2008) Biomechanical changes of the internal limiting membrane after indocyanine green staining. Dev Ophthalmol 42:82–90

    Article  PubMed  CAS  Google Scholar 

  35. Maia M, Furlani BA, Souza-Lima AA, Martins DS, Navarro RM, Belfort R Jr (2014) Lutein: a new dye for chromovitrectomy. Retina 34:262–272

    Article  PubMed  CAS  Google Scholar 

  36. Lüke M, Grisanti S, Lüke J; International Chromovitrectomy Collaboration (2013) The retinal biocompatibility of dyes in the ex vivo model of the isolated superfused vertebrate retina. Ophthalmologica 230 Suppl 2:21–26

  37. Brockmann T, Steger C, Westermann M, Nietzsche S, Koenigsdoerffer E, Strobel J, Dawczynski J (2011) Ultrastructure of the membrana limitans interna after dye-assisted membrane peeling. Ophthalmologica 226:228–233

    Article  PubMed  CAS  Google Scholar 

  38. Chalam KV, Li W, Koushan K (2015) Effect of distance and duration of illumination on retinal ganglion cells exposed to varying concentrations of brilliant blue green. J Clin Med Res 7:517–524

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Yanagi Y, Inoue Y, Jang WD, Kadonosono K (2006) A2e mediated phototoxic effects of endoilluminators. Br J Ophthalmol 90:229–232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Narayanan R, Kenney MC, Kamjoo S, Trinh TH, Seigel GM, Resende GP, Kuppermann BD (2005) Toxicity of indocyanine green (ICG) in combination with light on retinal pigment epithelial cells and neurosensory retinal cells. Curr Eye Res 30:471–478

    Article  PubMed  CAS  Google Scholar 

  41. Bian Q, Gao S, Jilin Z, Qin J, Taylor A, Johnson EJ, Tang G, Sparrow JR, Gierhart D, Shang F (2012) Lutein and zeaxanthin supplementation reduces hotooxidative damage and modulates the expression of inflammation-related genes in retinal pigment epithelial cells. Free Radic Biol Med 53:1298–1307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Sundelin SP, Nilsson SE (2001) Lipofuscin-formation in retinal pigment epithelial cells is reduced by antioxidants. Free Radic Biol Med 31:217–225

    Article  PubMed  CAS  Google Scholar 

  43. Kijlstra A, Yuan T, Kelly ER, Berendschot TT (2012) Lutein: more than just a filter for blue light. Prog Retin Eye Res 3:303–315

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, Humanitas University, Via Manzoni 113, Rozzano, 20089, Milan, Italy

    Mario R. Romano

  2. Department of Neuroscience, Reproductive and Odontostomatological Science, University Federico II, Naples, Italy

    Mario R. Romano, Mariantonia Ferrara, Gilda Cennamo & Giovanni Cennamo

  3. Department of Biomedical Advanced Sciences, University Federico II, Naples, Italy

    Gennaro Ilardi & Stefania Staibano

  4. Department of Ophthalmology, S. Anna Hospital, Brescia, Italy

    Barbara Parolini

  5. Department of Ophthalmology, Polytechnic University of Marche, Ancona, Italy

    Cesare Mariotti

Authors
  1. Mario R. Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gennaro Ilardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariantonia Ferrara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gilda Cennamo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Barbara Parolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cesare Mariotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stefania Staibano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giovanni Cennamo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mario R. Romano.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romano, M.R., Ilardi, G., Ferrara, M. et al. Macular peeling-induced retinal damage: clinical and histopathological evaluation after using different dyes. Graefes Arch Clin Exp Ophthalmol 256, 1573–1580 (2018). https://doi.org/10.1007/s00417-018-4029-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-018-4029-2

Keywords

Search

Navigation