Collagen cross-linking: A new treatment paradigm in corneal disease - a review

Clinical and Experimental Ophthalmology

Volumn 38, Issue 2, 2010, Pages 141-153

  Snibson, Grant R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Collagen; Corneal dystrophies; Corneal topography; Cross linking; Keratoconus progression; Riboflavin

Indexed keywords

COLLAGEN; PHOTOSENSITIZING AGENT; PILOCARPINE; REACTIVE OXYGEN METABOLITE; RIBOFLAVIN;

CONFOCAL MICROSCOPY; CORNEA CELL; CORNEA DISEASE; CORNEA DYSTROPHY; CORNEA EDEMA; CORNEA ENDOTHELIUM; CORNEA TRANSPLANTATION; CORNEA ULCER; CORNEAL ENDOTHELIAL CELL LOSS; CROSS LINKING; DISEASE COURSE; HUMAN; KERATITIS; KERATOCONUS; KERATOPATHY; NONHUMAN; PHOTOREFRACTIVE KERATECTOMY; REFRACTION ERROR; REVIEW; RISK FACTOR; STRESS STRAIN RELATIONSHIP; ULTRAVIOLET A RADIATION; VISION; VISUAL ACUITY;

COLLAGEN; CROSS-LINKING REAGENTS; HUMANS; KERATOCONUS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; RIBOFLAVIN; ULTRAVIOLET THERAPY;

EID: 77952032620     PISSN: 14426404     EISSN: 14429071     Source Type: Journal    
DOI: 10.1111/j.1442-9071.2010.02228.x     Document Type: Review

References (96)

1. Sung HW, Chang WH, Ma CY, Lee MH. Crosslinking of biological tissues using genipin and/or carbodiimide. J Biomed Mater Res A 2003, 64:427-38.
2. Robins SP. Biochemistry and functional significance of collagen cross-linking. Biochem Soc Trans 2007, 35:849-52.
3. Ashwin PT, McDonnell PJ. Collagen cross-linkage: a comprehensive review and directions for future research. Br J Ophthalmol 2009, 9:9.
4. Malik NS, Moss SJ, Ahmed N, Furth AJ, Wall RS, Meek KM. Ageing of the human corneal stroma: structural and biochemical changes. Biochim Biophys Acta 1992, 1138:222-8.
5. Daxer A, Misof K, Grabner B, Ettl A, Fratzl P. Collagen fibrils in the human corneal stroma: structure and aging. Invest Ophthalmol Vis Sci 1998, 39:644-8.
6. Elsheikh A, Wang D, Brown M, Rama P, Campanelli M, Pye D. Assessment of corneal biomechanical properties and their variation with age. Curr Eye Res 2007, 32:11-19.
7. Tuft SJ, Moodaley LC, Gregory WM, Davison CR, Buckley RJ. Prognostic factors for the progression of keratoconus. Ophthalmology 1994, 101:439-47.
8. Chace KV, Carubelli R, Nordquist RE. The role of nonenzymatic glycosylation, transition metals, and free radicals in the formation of collagen aggregates. Arch Biochem Biophys 1991, 288:473-80.
9. Seiler T, Huhle S, Spoerl E, Kunath H. Manifest diabetes and keratoconus: a retrospective case-control study. Graefes Arch Clin Exp Ophthalmol 2000, 238:822-5.
10. Cannon DJ, Foster CS. Collagen crosslinking in keratoconus. Invest Ophthalmol Vis Sci 1978, 17:63-5.
11. Andreassen TT, Simonsen AH, Oxlund H. Biomechanical properties of keratoconus and normal corneas. Exp Eye Res 1980, 31:435-41.
12. Spoerl E, Huhle M, Seiler T. Induction of cross-links in corneal tissue. Exp Eye Res 1998, 66:97-103.
13. Wollensak G. Crosslinking treatment of progressive keratoconus: new hope. Curr Opin Ophthalmol 2006, 17:356-60.
14. McCall AS, Kraft S, Edelhauser HF. Mechanisms of Corneal Tissue Cross-Linking in Response to Treatment with Topical Riboflavin and Long Wavelength Ultraviolet Radiation (UVA). Invest Ophthalmol Vis Sci 2009, 30:30.
15. Sady C, Khosrof S, Nagaraj R. Advanced Maillard reaction and crosslinking of corneal collagen in diabetes. Biochem Biophys Res Commun 1995, 214:793-7.
16. Sporl E, Huhle M, Kasper M, Seiler T. [Increased rigidity of the cornea caused by intrastromal cross-linking]. Ophthalmologe 1997, 94:902-6.
17. Wollensak G, Spoerl E, Seiler T. Stress-strain measurements of human and porcine corneas after riboflavin-ultraviolet-A-induced cross-linking. J Cataract Refract Surg 2003, 29:1780-5.
18. Kohlhaas M, Spoerl E, Schilde T, Unger G, Wittig C, Pillunat LE. Biomechanical evidence of the distribution of cross-links in corneas treated with riboflavin and ultraviolet A light. J Cataract Refract Surg 2006, 32:279-83.
19. Tanter M, Touboul D, Bercoff J, Fink M. High Resolution Quantitative Imaging of Cornea Elasticity Using Supersonic Shear Imaging. IEEE Trans Med Imaging 2009, 5:5.
20. Wollensak G, Spoerl E, Wilsch M, Seiler T. Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment. Cornea 2004, 23:43-9.
21. Wollensak G, Sporl E, Reber F, Pillunat L, Funk R. Corneal endothelial cytotoxicity of riboflavin/UVA treatment in vitro. Ophthalmic Res 2003, 35:324-8.
22. Spoerl E, Mrochen M, Sliney D, Trokel S, Seiler T. Safety of UVA-riboflavin cross-linking of the cornea. Cornea 2007, 26:385-9.
23. Dhaliwal JS, Kaufman SC. Corneal collagen cross-linking: a confocal, electron, and light microscopy study of eye bank corneas. Cornea 2009, 28:62-7.
24. Wollensak G, Iomdina E, Dittert DD, Herbst H. Wound healing in the rabbit cornea after corneal collagen cross-linking with riboflavin and UVA. Cornea 2007, 26:600-5.
25. Wollensak G, Aurich H, Pham DT, Wirbelauer C. Hydration behavior of porcine cornea crosslinked with riboflavin and ultraviolet A. J Cataract Refract Surg 2007, 33:516-21.
26. Bottos KM, Dreyfuss JL, Regatieri CV. Immunofluorescence confocal microscopy of porcine corneas following collagen cross-linking treatment with riboflavin and ultraviolet A. J Refract Surg 2008, 24:S715-19.
27. Spoerl E, Wollensak G, Dittert DD, Seiler T. Thermomechanical behavior of collagen-cross-linked porcine cornea. Ophthalmologica 2004, 218:136-40.
28. Spoerl E, Wollensak G, Seiler T. Increased resistance of crosslinked cornea against enzymatic digestion. Curr Eye Res 2004, 29:35-40.
29. Stewart JM, Schultz DS, Lee OT, Trinidad ML. Collagen cross-links reduce corneal permeability. Invest Ophthalmol Vis Sci 2009, 50:1606-12.
30. Mencucci R, Mazzotta C, Rossi F. Riboflavin and ultraviolet A collagen crosslinking: in vivo thermographic analysis of the corneal surface. J Cataract Refract Surg 2007, 33:1005-8.
31. Wollensak G, Wilsch M, Spoerl E, Seiler T. Collagen fiber diameter in the rabbit cornea after collagen crosslinking by riboflavin/UVA. Cornea 2004, 23:503-7.
32. Wollensak G, Redl B. Gel electrophoretic analysis of corneal collagen after photodynamic cross-linking treatment. Cornea 2008, 27:353-6.
33. Caporossi A, Baiocchi S, Mazzotta C, Traversi C, Caporossi T. Parasurgical therapy for keratoconus by riboflavin-ultraviolet type A rays induced cross-linking of corneal collagen: preliminary refractive results in an Italian study. J Cataract Refract Surg 2006, 32:837-45.
34. Raiskup-Wolf F, Hoyer A, Spoerl E, Pillunat LE. Collagen crosslinking with riboflavin and ultraviolet-A light in keratoconus: long-term results. J Cataract Refract Surg 2008, 34:796-801.
35. Wollensak G, Spoerl E, Seiler T. Riboflavin/ultraviolet-a-induced collagen crosslinking for the treatment of keratoconus. Am J Ophthalmol 2003, 135:620-7.
36. Wittig-Silva C, Whiting M, Lamoureux E, Lindsay RG, Sullivan LJ, Snibson GR. A randomized controlled trial of corneal collagen cross-linking in progressive keratoconus: preliminary results. J Refract Surg 2008, 24:S720-5.
37. Jankov MR, Hafezi F, Beko M. [Corneal Cross-linking for the treatment of keratoconus: preliminary results]. Arq Bras Oftalmol 2008, 71:813-18.
38. Hoyer A, Raiskup-Wolf F, Sporl E, Pillunat LE. [Collagen cross-linking with riboflavin and UVA light in keratoconus - results from Dresden.]. Ophthalmologe 2009, 106:133-40.
39. Fournie P, Galiacy S, Arne JL, Malecaze F. [Corneal collagen cross-linking with ultraviolet-A light and riboflavin for the treatment of progressive keratoconus]. J Fr Ophtalmol 2009, 32:1-7.
40. Grewal DS, Brar GS, Jain R, Sood V, Singla M, Grewal SP. Corneal collagen crosslinking using riboflavin and ultraviolet-A light for keratoconus: one-year analysis using Scheimpflug imaging. J Cataract Refract Surg 2009, 35:425-32.
41. Coskunseven E, Jankov MR, Hafezi F. Contralateral eye study of corneal collagen cross-linking with riboflavin and UVA irradiation in patients with keratoconus. J Refract Surg 2009, 25:371-6.
42. Agrawal VB. Corneal collagen cross-linking with riboflavin and ultraviolet - a light for keratoconus: results in Indian eyes. Indian J Ophthalmol 2009, 57:111-14.
43. Vinciguerra P, Albe E, Trazza S. Refractive, topographic, tomographic, and aberrometric analysis of keratoconic eyes undergoing corneal cross-linking. Ophthalmology 2009, 116:369-78.
44. Vinciguerra P, Albe E, Trazza S, Seiler T, Epstein D. Intraoperative and postoperative effects of corneal collagen cross-linking on progressive keratoconus. Arch Ophthalmol 2009, 127:1258-65.
45. Koller T, Iseli HP, Hafezi F, Vinciguerra P, Seiler T. Scheimpflug imaging of corneas after collagen cross-linking. Cornea 2009, 28:510-15.
46. Wagner H, Barr JT, Zadnik K. Collaborative Longitudinal Evaluation of Keratoconus (CLEK) Study: methods and findings to date. Cont Lens Anterior Eye 2007, 30:223-32.
47. Romppainen T, Bachmann LM, Kaufmann C, Kniestedt C, Mrochen M, Thiel MA. Effect of riboflavin-UVA-induced collagen cross-linking on intraocular pressure measurement. Invest Ophthalmol Vis Sci 2007, 48:5494-8.
48. Koller T, Mrochen M, Seiler T. Complication and failure rates after corneal crosslinking. J Cataract Refract Surg 2009, 35:1358-62.
49. Seiler T, Hafezi F. Corneal cross-linking-induced stromal demarcation line. Cornea 2006, 25:1057-9.
50. Ku JY, Niederer RL, Patel DV, Sherwin T, McGhee CN. Laser scanning in vivo confocal analysis of keratocyte density in keratoconus. Ophthalmology 2008, 115:845-50.
51. Weed KH, MacEwen CJ, Cox A, McGhee CN. Quantitative analysis of corneal microstructure in keratoconus utilising in vivo confocal microscopy. Eye (London, England) 2007, 21:614-23.
52. Mazzotta C, Balestrazzi A, Traversi C. Treatment of progressive keratoconus by riboflavin-UVA-induced cross-linking of corneal collagen: ultrastructural analysis by Heidelberg Retinal Tomograph II in vivo confocal microscopy in humans. Cornea 2007, 26:390-7.
53. Kymionis GD, Diakonis VF, Kalyvianaki M. One-year follow-up of corneal confocal microscopy after corneal cross-linking in patients with post laser in situ keratosmileusis ectasia and keratoconus. Am J Ophthalmol 2009, 147:774-8.
54. Croxatto JO, Tytiun AE, Argento CJ. Sequential in Vivo Confocal Microscopy Study of Corneal Wound Healing After Cross-Linking in Patients with Keratoconus. J Refract Surg 2009, 1-8. Epub ahead of print
55. Mazzotta C, Traversi C, Baiocchi S. Corneal healing after riboflavin ultraviolet-A collagen cross-linking determined by confocal laser scanning microscopy in vivo: early and late modifications. Am J Ophthalmol 2008, 146:527-33.
56. Hafezi F, Mrochen M, Iseli HP, Seiler T. Collagen crosslinking with ultraviolet-A and hypoosmolar riboflavin solution in thin corneas. J Cataract Refract Surg 2009, 35:621-4.
57. Angunawela RI, Arnalich-Montiel F, Allan BD. Peripheral sterile corneal infiltrates and melting after collagen crosslinking for keratoconus. J Cataract Refract Surg 2009, 35:606-7.
58. Koppen C, Vryghem JC, Gobin L, Tassignon MJ. Keratitis and corneal scarring after UVA/riboflavin cross-linking for keratoconus. J Refract Surg 2009, 25:S819-23.
59. Zamora KV, Males JJ. Polymicrobial keratitis after a collagen cross-linking procedure with postoperative use of a contact lens: a case report. Cornea 2009, 28:474-6.
60. Pollhammer M, Cursiefen C. Bacterial keratitis early after corneal crosslinking with riboflavin and ultraviolet-A. J Cataract Refract Surg 2009, 35:588-9.
61. Perez-Santonja JJ, Artola A, Javaloy J, Alio JL, Abad JL. Microbial keratitis after corneal collagen crosslinking. J Cataract Refract Surg 2009, 35:1138-40.
62. Rama P, Di Matteo F, Matuska S, Paganoni G, Spinelli A. Acanthamoeba keratitis with perforation after corneal crosslinking and bandage contact lens use. J Cataract Refract Surg 2009, 35:788-91.
63. Kymionis GD, Portaliou DM, Bouzoukis DI. Herpetic keratitis with iritis after corneal crosslinking with riboflavin and ultraviolet A for keratoconus. J Cataract Refract Surg 2007, 33:1982-4.
64. Sporl E, Raiskup-Wolf F, Pillunat LE. [Biophysical principles of collagen cross-linking]. Klin Monatsbl Augenheilkd 2008, 225:131-7.
65. Rocha KM, Ramos-Esteban JC, Qian Y, Herekar S, Krueger RR. Comparative study of riboflavin-UVA cross-linking and 'flash-linking' using surface wave elastometry. J Refract Surg 2008, 24:S748-51.
66. Hayes S, O'Brart DP, Lamdin LS. Effect of complete epithelial debridement before riboflavin-ultraviolet-A corneal collagen crosslinking therapy. J Cataract Refract Surg 2008, 34:657-61.
67. Baiocchi S, Mazzotta C, Cerretani D, Caporossi T, Caporossi A. Corneal crosslinking: riboflavin concentration in corneal stroma exposed with and without epithelium. J Cataract Refract Surg 2009, 35:893-9.
68. Wollensak G, Iomdina E. Biomechanical and histological changes after corneal crosslinking with and without epithelial debridement. J Cataract Refract Surg 2009, 35:540-6.
69. Samaras K, O'Brart DP, Doutch J, Hayes S, Marshall J, Meek KM. Effect of epithelial retention and removal on riboflavin absorption in porcine corneas. J Refract Surg 2009, 25:771-5.
70. Bakke EF, Stojanovic A, Chen X, Drolsum L. Penetration of riboflavin and postoperative pain in corneal collagen crosslinking: excimer laser superficial versus mechanical full-thickness epithelial removal. J Cataract Refract Surg 2009, 35:1363-6.
71. Bueeler M, Spoerl E, Seiler T, Mrochen M. UV collagen cross-linking of the cornea - safety aspects and design of a UV illumination system. 2008, 1-11.
72. Chan CC, Sharma M, Wachler BS. Effect of inferior-segment Intacs with and without C3-R on keratoconus. J Cataract Refract Surg 2007, 33:75-80.
73. Ertan A, Karacal H, Kamburoglu G. Refractive and topographic results of transepithelial cross-linking treatment in eyes with intacs. Cornea 2009, 1:1.
74. Alio JL, Shabayek MH, Artola A. Intracorneal ring segments for keratoconus correction: long-term follow-up. J Cataract Refract Surg 2006, 32:978-85.
75. Kymionis GD, Karavitaki AE, Kounis GA, Portaliou DM, Yoo SH, Pallikaris IG. Management of pellucid marginal corneal degeneration with simultaneous customized photorefractive keratectomy and collagen crosslinking. J Cataract Refract Surg 2009, 35:1298-301.
76. zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) der Naturwissenschaftlichen Fakultat II - Physik der Universitat Regensburg. Dissertation, vorgelegt von Jurgen Baier aus Bamberg November 2005
77. Kamburoglu G, Ertan A. Intacs implantation with sequential collagen cross-linking treatment in postoperative LASIK ectasia. J Refract Surg 2008, 24:S726-9.
78. Kohlhaas M, Spoerl E, Speck A, Schilde T, Sandner D, Pillunat LE. [A new treatment of keratectasia after LASIK by using collagen with riboflavin/UVA light cross-linking]. Klin Monatsbl Augenheilkd 2005, 222:430-6.
79. Hafezi F, Kanellopoulos J, Wiltfang R, Seiler T. Corneal collagen crosslinking with riboflavin and ultraviolet A to treat induced keratectasia after laser in situ keratomileusis. J Cataract Refract Surg 2007, 33:2035-40.
80. Randleman JB. Post-laser in-situ keratomileusis ectasia: current understanding and future directions. Curr Opin Ophthalmol 2006, 17:406-12.
81. Kanellopoulos AJ, Binder PS. Collagen cross-linking (CCL) with sequential topography-guided PRK: a temporizing alternative for keratoconus to penetrating keratoplasty. Cornea 2007, 26:891-5.
82. Ehlers N, Hjortdal J. Riboflavin-ultraviolet light induced cross-linking in endothelial decompensation. Acta Ophthalmol 2008, 86:549-51.
83. Wollensak G, Aurich H, Wirbelauer C, Pham DT. Potential use of riboflavin/UVA cross-linking in bullous keratopathy. Ophthalmic Res 2009, 41:114-17.
84. Krueger RR, Ramos-Esteban JC, Kanellopoulos AJ. Staged intrastromal delivery of riboflavin with UVA cross-linking in advanced bullous keratopathy: laboratory investigation and first clinical case. J Refract Surg 2008, 24:S730-6.
85. Corbin F. Pathogen inactivation of blood components: current status and introduction of an approach using riboflavin as a photosensitizer. Int J Hematol 2002, 76(2):253-7. Suppl
86. Kumar V, Lockerbie O, Keil SD. Riboflavin and UV-light based pathogen reduction: extent and consequence of DNA damage at the molecular level. Photochem Photobiology 2004, 80:15-21.
87. Ruane PH, Edrich R, Gampp D, Keil SD, Leonard RL, Goodrich RP. Photochemical inactivation of selected viruses and bacteria in platelet concentrates using riboflavin and light. Transfusion 2004, 44:877-85.
88. Martins SA, Combs JC, Noguera G. Antimicrobial efficacy of riboflavin/UVA combination (365 nm) in vitro for bacterial and fungal isolates: a potential new treatment for infectious keratitis. Invest Ophthalmol Vis Sci 2008, 49:3402-8.
89. Makdoumi K, Backman A, Mortensen J, Crafoord S. Evaluation of antibacterial efficacy of photo-activated riboflavin using ultraviolet light (UVA). Graefes Arch Clin Exp Ophthalmol 2009, 248:207-12.
90. Schrier A, Greebel G, Attia H, Trokel S, Smith EF. In vitro antimicrobial efficacy of riboflavin and ultraviolet light on Staphylococcus aureus, methicillin-resistant Staphylococcus aureus, and Pseudomonas aeruginosa. J Refract Surg 2009, 25:S799-802.
91. Micelli Ferrari T, Leozappa M, Lorusso M, Epifani E, Micelli Ferrari L. Escherichia coli keratitis treated with ultraviolet A/riboflavin corneal cross-linking: a case report. Eur J Ophthalmol 2009, 19:295-7.
92. Moren H, Malmsjo M, Mortensen J, Ohrstrom A. Riboflavin and ultraviolet A collagen crosslinking of the cornea for the treatment of keratitis. Cornea 2009, 31:31.
93. Iseli HP, Thiel MA, Hafezi F, Kampmeier J, Seiler T. Ultraviolet A/riboflavin corneal cross-linking for infectious keratitis associated with corneal melts. Cornea 2008, 27:590-4.
94. Schnitzler E, Sporl E, Seiler T. [Irradiation of cornea with ultraviolet light and riboflavin administration as a new treatment for erosive corneal processes, preliminary results in four patients]. Klin Monatsbl Augenheilkd 2000, 217:190-3.
95. Berman MB. Collagenase inhibitors: rationale for their use in treating corneal ulceration. Int Ophthalmol Clin 1975, 15:49-66.
96. Wang F. UVA/riboflavin-induced apoptosis in mouse cornea. Ophthalmologica 2008, 222:369-72.