Oftalmol Zh.2014;3:94-103
https://doi.org/10.31288/oftalmolzh2014394103
Physical Characteristics of the Internal Limiting Membrane and their Significance in Ocular Surgery and Beyond
Paul B. Henrich1; Christophe A. Monnier 2, Marko Loparic 2, Valmaggia C. 3, Lang C. 4, Philippe C. Cattin 4
1University Hospital Basel, Department of Ophthalmology, Basel (Switzerland);
2The University of Basel, Biozentrum and the Swiss Nanoscience Institute, Basel, (Switzerland);
3Department of Ophthalmology, Cantonal hospital, St. Gallen, (Switzerland)
4University of Basel, Medical Image Analysis Center, Basel, (Switzerland)
E-mail: Henzichp@uhbs.ch
Key words: Atomic force microscopy, brilliant blue G, chromaticity analysis, chromovitrectomy, indocyanine green, internal limiting membrane, trypan blue, vital dyes.
Introduction: Efforts to render surgical removal of the internal limiting membrane safer and easier depend on an in-depth understanding of its physical characteristics.
Purpose: Studying the internal limiting membrane is particularly gratifying, as it represents the most easily accessible of all human basement membranes and many findings may contribute to an improved comprehension of human basement membranes in general.
Data sources: MEDLINE with no language restriction through March 2014. Data selection: Overview of recent research results from the authors own study group as well as a context of the current literature.
Conclusion: New examination techniques such as chromaticity analysis and trans-lational use of established techniques like atomic force microscopy allow new insights into mechanical properties of the internal limiting membrane. Chromaticity analysis permits objective measurements of the contrast behavior of the internal limiting membrane when exposed to vital dyes. Compared to various approved dyes, indocyanine green shows the best visible contrast, in accordance with its popularity despite its off-label status. Atomic force microscopy allows the examination of the native internal limiting membrane. It, thus, enabled the study group to provide an extensive topographic map including surface structure, thickness and stiffness, avoiding the fixation artifacts of previous descriptions. Surface structure, stiffness, rolling behavior and cell adhesion were found to be asymmetrical between the two opposite surfaces of the membrane and the same asymmetry could be reproduced for several other ocular basement membranes challenging the current model of basement membrane ultrastructure.
References
1.Bottos J. Vitreomacular traction syndrome / J. Bottos, J. Elizalde, J. Arevalo, E. Rodrigues, M. Maia // J Ophthalmic Vis Res — 2012. — Vol.7. — P.148-161.
2.Koerner F. Vitrectomy for macular pucker and vitreomacular traction syndrome / F. Koerner, J. Garweg // Doc Ophthalmol — 1999. — Vol.97. — P.449- 458.
Crossref
3.Sayegh R. High-resolution optical coherence tomography after surgery for vitreomacular traction: a 2-year follow-up / R. Sayegh, M. Georgopoulos, W. Geitzenauer, C. Simad-er, et al. // Ophthalmology — 2010. P.117. — 2010- 2017.
Crossref
4.Schmidt-Erfurth U. Three-dimensional ultrahigh-resolu-tion optical coherence tomography of macular diseases / U. Schmidt-Erfurth, R. Leitgeb, S. Michels, et al. // Invest Ophthalmol Vis Sci — 2005. — Vol.46. — P.3393-3402.
Crossref
5.Puliafito C. Imaging of macular diseases with optical coherence tomography / C. Puliafito , M. Hee, C. Lin, et al. // Ophthalmology. — 1995. — Vol.102. P.217- 229.
Crossref
6.Hikichi T. Course of vitreomacular traction syndrome / T. Hikichi, A. Yoshida, C. Trempe // Am J Ophthalmol — 1995. Vol.119. P.55-61.
Crossref
7.Gregor Z. Surgery for idiopathic full-thickness macular holes / Z. Gregor // Eye (Lond) — 1996. — Vol.10. — P.685- 690.
Crossref
8.Simpson A. Vitreomacular adhesion and neovascular age-related macular degeneration/A. Simpson , R. Petrarca, T. Jackson // Surv Ophthalmol — 2012. — Vol.57. — P.498-509.
Crossref
9.Bressler N. Age-related macular degeneration is the leading cause of blindness / N. Bressler // Jama — 2004. — Vol.291. — P.1900- 1901.
Crossref
10.Smiddy W. Vitrectomy for macular traction caused by in-complete vitreous separation / W. Smiddy , R. Michels,
B. Glaser, S. Bustros // Arch Ophthalmol — 1988. — Vol.106. — P.624- 628.
11.Schwatz S. Recognition ofvitreoschisis in proliferative diabetic retinopathy. A useful landmark in vitrectomy for diabetic traction retinal detachment / S. Schwatz, R. Alex¬ander, P. Hiscott, Z. Gregor // Ophthalmology — 1996. —Vol.103. — P.323-328.
12.Gandorfer A. Epiretinal pathology of vitreomacular traction syndrome / A. Gandorfer, M. Rohleder, A. Kampik // Br J Ophthalmol — 2002. — Vol.86. — P.902- 909.
13.Gandorfer A. Objective of Pharmacologic Vitreolysis / A. Gandorfer // Dev Ophthalmol — 2009. — Vol.44. — P.1-6.
14.Trese M. Prognostic criteria / M. Trese, D. Chandler, R. Machemer Macular pucker. I. // Graefes Arch Clin Exp Ophthalmol — 1983. — Vol.221. — P.12-15.
15.Kelly N. Vitreous surgery for idiopathic macular holes. Results of a pilot study / N. Kelly , R. Wendel // Arch Ophthalmol — 1991. — Vol.109. — P.654- 659.
16.Park D. W. Macular hole surgery with internal-limiting membrane peeling and intravitreous air / D. Park, J. Sip-perley, S. Sneed, P. Dugel, et al. // Ophthalmology — 1999. — Vol.106. — P.1392- 1397; discussion 1397- 1398.
17.Henrich P. Anatomical and functional outcome in brilliant blue G assisted chromovitrectomy / P. Henrich , C. Hari- toglou, P. Meyer, et al.// Acta Ophthalmol — 2009. — Vol.23. — P.23.
18.Haritoglou C. Paracentral scotomata: a new finding after vitrectomy for idiopathic macular hole / C. Haritoglou, 0.Ehrt, C. Gass, N. Kristin, et al./ Br J Ophthalmol — 2001. — Vol.85. — P.231- 233.
19.Kadonosono K. Staining of internal limiting membrane in macular hole surgery / K. Kadonosono, N. Itoh, E. Uchio, S. Nakamura, et al.// Arch Ophthalmol — 2000. — Vol.118. — P.1116-1118.
20.Banker A. Vision-threatening complications of surgery for full-thickness macular holes. Vitrectomy for Macular Hole Study Group / A. Banker , W. Freeman, J. Kim, D. Mun-guia, et al. // Ophthalmology — 1997. — Vol.104. — P. 1442- 1452; discussion 1452- 1443.
21.Burk S. Indocyanine green-assisted peeling of the retinal internal limiting membrane / S. Burk, A. Da Mata, M. Snyder, R. Rosa, et al. // Ophthalmology — 2000. — Vol.107. — P.2010- 2014.
22.Maguire A. Clinicopathologic correlation of recurrent epiretinal membranes after previous surgical removal / A. Maguire, W. Smiddy, S. Nanda, R. Michels, et al. // Retina — 1990. — Vol.10. — P.213-222.
23.Livingstone B. Retrospective study of macular holes treated with pars plana vitrectomy / B. Livingstone, R. Bourke // Aust N Z J Ophthalmol -1999. — Vol.27. — P.331- 341.
24.Lewis J. Diamond-dusted silicone cannula for epiretinal membrane separation during vitreous surgery / J. Lewis, 1.Park, M. Ohji, Y Saito, et al.// Am J Ophthalmol — 1997. — Vol.124. — P.552- 554.
25.Rodrigues E. Chromovitrectomy: a new field in vitreo- retinal surgery / E. Rodrigues, C. Meyer, P. Kroll // Graefes Arch Clin Exp Ophthalmol -200З. — Vol.243. — P.291— 293.
26.Haritoglou C. Indocyanine green-assisted peeling of the internal limiting membrane in macular hole surgery affects visual outcome: a clinicopathologic correlation / C. Hari-toglou, A. Gandorfer, C. Gass, M. Schaumberger, et al.// Am J Ophthalmol — 2002. — Vol.134. — P.836— 841.
27.Iriyama A. Effects of indocyanine green on retinal ganglion cells / A. Iriyama, S. Uchida, Y. Yanagi, et al.// Invest Ophthalmol Vis Sci — 2004. — Vol^. — P.943— 947.
28.Maia M. Effects of indocyanine green injection on the retinal surface and into the subretinal space in rabbits / M. Maia, L. Kellner, E. Juan, et al.// Retina — 2004. — Vol.24. — P.80—91.
29.Sato Y. Evaluation of indocyanine green toxicity to rat retinas / Y. Sato, H. Tomita, E. Sugano, H. Isago, et al.// Ophthalmologica — 2006. — Vol.220.
30.Gandorfer A. Retinal damage from indocyanine green in experimental macular surgery / A. Gandorfer, C. Harito-glou, A. Gandorfer, A. Kampik //Invest Ophthalmol Vis Sci — 2003. — Vol.44. — P.316— 323.
31.Ando F. Optic nerve atrophy after vitrectomy with indo-cyanine green-assisted internal limiting membrane peeling in diffuse diabetic macular edema. Adverse effect of ICG-assisted ILM peeling. Optic nerve atrophy after vitrectomy with indocyanine green-assisted internal limiting mem¬brane peeling in diffuse diabetic macular edema. Adverse effect of ICG-assisted ILM peeling./ F. Ando, O. Yasui, H. Hirose, N. Ohba // Graefes Arch Clin Exp Ophthal-mol — 2004. — Vol.242. — P.995- 999.
32.Hisatomi T. Staining ability and biocompatibility of brilliant blue G: preclinical study of brilliant blue G as an adjunct for capsular staining / T. Hisatomi, H. Enaida, H. Matsumoto, et al. // Arch Ophthalmol — 2006. — Vol.124. — P^M^W.
33.Enaida H. Preclinical investigation of internal limiting membrane staining and peeling using intravitreal brilliant blue G / H. Enaida, T. Hisatomi, Y. Goto, et al.// Reti¬na — 2006. — Vol.26. — P.623— 630.
34.Enaida H. Brilliant blue G selectively stains the internal limiting membrane/brilliant blue G-assisted membrane peeling / H. Enaida, T. Hisatomi, Y. Hata, et al.// Reti¬na — 2006. — Vol.26. — P.631— 636.
3З. Henrich P. Quantification of Contrast Recognizability during Brilliant Blue G- and Indocyanine Green-Assisted Chromovitrectomy / P. Henrich, S. Priglinger, C. Hari-toglou, et al. // Invest Ophthalmol Vis Sci — 2011. — Vol^. — P.4345- 4349.
36.Macadam D. Visual Sensitivities to Color Differences in Daylight / D. Macadam // Journal of the OPTICAL SO¬CIETY of AMERICA — 1942. — Vol.32. — P.247— 273.
37.Logvinenko A. An object-color space / A. Logvinenko// J Vis — 2009. — Vol^. — P.1—23.
38.Kadonosono K. Internal limiting membrane contrast after staining with indocyanine green and brilliant blue g during macular surgery / K. Kadonosono, A. Arakawa, M. Inoue, et al. //Retina — 2013. — Vol.11. — P.11.
39.Meyer C. Trypan blue has a high affinity to cellular structures such as epiretinal membrane / C. Meyer , E. Rodrigues, P. Kroll // Am J Ophthalmol — 2004. — Vol.137. — P.207— 208.
40.Perrier M. Epiretinal membrane surgery assisted by try-pan blue / M. Perrier, M. Sebag // Am J Ophthalmol — 2003. — Vol.^. — P.909— 911.
41.Zhao F. Epiretinal cell proliferation in macular pucker and vitreomacular traction syndrome: analysis of flat-mounted in-ternal limiting membrane specimens / F. Zhao, A. Gandorfer, C.Haritoglou, et al. // Retina — 2013. — Vol.33. — P.77— 88.
42.Melles G. Trypan blue capsule staining to visualize the capsulorhexis in cataract surgery / G. Melles, P. Waard, J. Pameyer, W. Houdijn Beekhuis // J Cataract Refract Surg — 1999. — Vol^. — P.7—9.
43.Li K. Double peel using triamcinolone acetonide and trypan blue in the management of myopic macular hole with reti¬nal detachment: a case-control study / K. Li, E. Tang, P. Li, D.Wong // Clin Experiment Ophthalmol — 2010. — P.24.
44.Li K. Trypan blue staining of internal limiting membrane and epiretinal membrane during vitrectomy: visual results and histopathological findings / K. Li, D. Wong, P. Hiscott, P. Stanga, et al. // Br J Ophthalmol — 2003. — Vol.87. — P.216—219. 4З. Lee K. A comparison of outcomes after indocyanine green and trypan blue assisted internal limiting membrane peel¬ing during macular hole surgery / K. Lee, S. Dean, S. Guest // Br J Ophthalmol — 200З. — Vol.89. — P.420— 424.
46.Perrier M. Trypan blue-assisted peeling of the internal limiting membrane during macular hole surgery / M. Per-rier, M. Sebag // Am J Ophthalmol — 2003. — Vol.^. — P.903- 905.
47.Teba F. Trypan blue staining in vitreoretinal surgery / F. Teba , A. Mohr, C. Eckardt, et al. // Ophthalmology — 2003. — Vol.110. — P.2409— 2412.
48.Henrich P. Quantification of Contrast Recognizability in Sequential Epiretinal membrane Removal and Internal limiting membrane Peeling in Trypan blue-assisted Macu-lar Surgery / P. Henrich , C. Haritoglou, R. Schumann, R. Strauss, et al. // Retina — 2012.
49.Schumann R. Sequential epiretinal membrane removal with internal limiting membrane peeling in brilliant blue G-assisted macular surgery / R. Schumann, A. Gandorfer, K. Eibl, P. Henrich, et al. // Br J Ophthalmol. — 1369. — Vol.94. — P.1369— 1372.
30.Rodrigues E. Trypan blue stains the epiretinal membrane but not the internal limiting membrane / E. Rodrigues, C. Meyer, J. Schmidt, P. Kroll // Br J Ophthalmol. — 2003. — Vol.87. — P.1431— 1432.
31.Farah M. Current concepts of trypan blue in chromov-itrectomy / M. Farah, M. Maia, B. Furlani, et al.// Dev Ophthalmol. — 2008. — Vol.42. — P.91—100.
32.Veckeneer M. Novel 'heavy' dyes for retinal membrane staining during macular surgery: multicenter clinical assessment / M. Veckeneer, A. Mohr, E. Alharthi, et al.// Acta Ophthalmol. — 2013. — Vol.12. — P.208.
33.Luke C. Effects of patent blue on human retinal function / C. Luke, M. Luke, W. Sickel, T. Schneider // Graefes Arch Clin Exp Ophthalmol. — 2006. — Vol.244. — P.1188— 1190.
34.Dib E. Vital dyes in chromovitrectomy / E. Dib , E. Ro-drigues, M. Maia, et al. // Arq Bras Oftalmol. — 2009. — Vol.72. — P.845- 850.
ЗЗ. Balaiya S. Comparative in vitro safety analysis of dyes for chromovitrectomy: indocyanine green, brilliant blue green, bromophenol blue, and infracyanine green / S. Balaiya, V. Brar, R. Murthy, K. Chalam // Retina. — 2011. — Vol.31. — P.1128— 1136. З6. Haritoglou C. Experimental evaluation of aniline and methyl blue for intraocular surgery / C. Haritoglou, S. Priglinger, R. Liegl, et al. // Retina. — 2009. — Vol.29. — P.1266— 1273.
57.Kushner D. Pharmacological uses and perspectives of heavy water and deuterated compounds / D. Kushner, A. Baker, T. Dunstall // Can J Physiol Pharmacol. — 1999. — Vol.77. — P.79- 88.
58.Gerding H. Intravital staining of the internal limiting membrane with a novel heavy solution of brilliant blue G / H. Gerding, M. Timmermann, U. Thelen // Klin Monbl Augenheilkd. — 2011. — Vol.228. — P.298- 301.
59.Haritoglou C. Heavy brilliant blue G for internal limit¬ing membrane staining / C. Haritoglou, R. Schumann, A. Kampik, A. Gandorfer // Retina. — 2011. — Vol.31. — P.405- 407.
60.Henrich P. Contrast recognizability during brilliant blue G — and heavier-than-water brilliant blue G-assisted chromovitrectomy: a quantitative analysis / P. Henrich, C. Valmaggia, C. Lang, et al. // Acta Ophthalmol. — 2012. — Vol.20. — P.12005.
61.Rosenblum Y Spectral filters in low-vision correction / Y. Rosenblum , P. Zak, M. Ostrovsky, et al. // Ophthalmic Physiol Opt. — 2000. — Vol.20. — P.335-341.
62.Biesen P. Endoillumination during vitrectomy and phototoxicity thresholds / P. Biesen, T. Berenschot, R. Verdaasdonk, H. Weelden, et al.// Br J Ophthalmol. — 2000. — Vol.84. — P.1372-1375.
63.Kraushar M. Monochromatic endoillumination for epimacular membrane surgery / M. Kraushar, M. Harris, P. Morse // Ophthalmic Surg. — 1989. Vol.20. — P.508- 510.
64.Henrich P. Influence of Endoilluminator Spectral Filters on Contrast Recognisability During Brilliant Blue G Assisted Chromovitrectomy. A Quantitative Analysis / P. Henrich, C. Valmaggia, C. Lang, S. Priglinger // Acta Ophthalmol. — 2012.
65.Henrich P. Nanoscale topographic and biomechani-cal studies of the human internal limiting / P. Henrich, C.Monnier, C. Monnier, W. Halfter, et al. // Invest Oph-thalmol Vis Sci. — 2012. — Vol.53. — P.2561- 2570.
66.Wollensak G. Biomechanical changes in the anterior lens capsule after trypan blue staining / G. Wollensak , E. Sporl, D.Pham // J Cataract Refract Surg — 2004. — Vol.30. — P.1526-1530.
67.Balasubramani M. / Molecular interactions in the retinal basement membrane system: a proteomic approach // M. Balasubramani, E. Schreiber, J. Candiello, G. Balasu-bramani // Matrix Biol. — Vol.29. — P.471- 483.
68.Erickson A. Still more complexity in mammalian basement membranes / A. Erickson, J. Couchman // J Histochem Cytochem. — 2000. — Vol.48. — P.1291-1306.
69.Candiello J. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane // J. Candiello, G. Cole, W. Halfter // Matrix Biol. — Vol.29. — P.402-410.
70.Halfter W. Regulation of eye size by the retinal basement membrane and vitreous body / W. Halfter, U. Winzen, P. Bishop, A. Eller // Invest Ophthalmol Vis Sci. — 2006. — Vol.47. — P.3586-3594.
71.Hogan M. The Vitreous, Its Structure, and Relation to the Ciliary Body and Retina. Proctor Award Lecture / M. Hogan // Invest Ophthalmol. — 1963. — Vol.2. — P.418-445.
72.Fine B. Limiting membranes of the sensory retina and pigment epithelium. An electron microscopic study / B. Fine // Arch Ophthalmol. — 1961. — Vol.66. — P.847-860.
73.Foos R. Vitreoretinal juncture; topographical variations / R. Foos // Invest Ophthalmol. — 1972. Vol.11. — P.801- 808.
74.Plodinec M. Atomic force microscopy for biological imaging and mechanical testing across length scales / M. Plodinec , M. Loparic, U. Aebi // Cold Spring Harb Protoc. — 2010:pdb top86.
75.Plodinec M. Force Microscopy for Biological Imaging and Mechanical Testing across Length Scales, in Live Cell Imaging: A laboratory manual / M. Plodinec, U. Aebi // Cold Spring Harbor Laboratory Press. — 2010.
76.Binnig G. Atomic force microscope / G. Binnig , C. Quate, C.Gerber // Phys Rev Lett. — 1986. — Vol.56. — P.930- 933.
77.Last J. The applications of atomic force microscopy to vi¬sion science / J. Last, P. Russell, P. Nealey., C. Murphy // Invest Ophthalmol Vis Sci. — Vol.51. — P.6083- 6094.
78.Wollensak G. Influence of indocyanine green staining on the biomechanical strength of porcine internal limiting membrane / G. Wollensak, E. Spoerl, C. Wirbelauer, D.Pham // Ophthalmologica. — 2004. — Vol.218. — P.278-282.
79.Haritoglou C. Vital dyes increase lens capsule stiffness / C. Haritoglou, R. Schumann, P. Henrich, A. Wolf, et al.// J Cataract Refract Surg. — 2013.
80.Candiello J. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane / J. Candiello, G. Cole, W. Halfter// Ma¬trix Biol. — 2010. — Vol.29. — P.402- 410.
81.Yurchenco P. Developmental and pathogenic mechanisms of basement membrane assembly / P. Yurchenco , B. Patton // Curr Pharm Des. — 2009. — Vol.15. — P.1277- 1294.
82.Halfter W. The bi-functional organization of human basement membranes / W. Halfter, C. Monnier, D. Muller, et al.// PLoS One. — 2013. — Vol.8.