Anti-VEGF Therapy (Bevacizumab) for Sulfur Mustard-Induced Corneal Neovascularization Associated with Delayed Limbal Stem Cell Deficiency in Rabbits

REFERENCES

• Ma DHK, Chen JK, Zhang F, Lin KY, Yao JY, Yu JS. Regulation of corneal angiogenesis in limbal stem cell deficiency. Prog Ret Eye Res 2006;25:563–590
   PubMedGoogle Scholar
• Lim P, Fuchsluger TA, Jurkunas UV. Limbal stem cell deficiency and corneal neovascularization. Semin Ophthalmol 2009;24:139–148
   PubMed Web of Science ®Google Scholar
• Kadar T, Turez J, Fishbine E, Sahar R, Chapman S, Amir A. Characterization of acute and delayed ocular lesions induced by sulfur mustard in rabbits. Cur Eye Res 2001;22:42–53
   PubMed Web of Science ®Google Scholar
• Kadar T, Dachir S, Cohen L, Sahar R, Fishbine E, Cohen M, et al. Ocular injuries following sulfur mustard exposure – pathological mechanism and potential therapy. Toxicology 2009;263:59–69
   PubMed Web of Science ®Google Scholar
• Pleyer U, Sherif Z, Baatz H, Hartmann C. Delayed mustard gas keratopathy: clinical findings and confocal microscopy. Am J Ophthalmol 1999;128:506–507
   PubMed Web of Science ®Google Scholar
• Javadi MA, Yazdani S, Sajjadi H, Jadidi K, Karimian F, Einollahi B, et al. Chronic and delayed-onset mustard gas keratitis. Ophthalmology 2005;112:617–625
   PubMed Web of Science ®Google Scholar
• Baradaran-Rafii A, Javadi MA, Kanavi MR, Eslani M, Jamali H, Karimian F. Limbal stem cell deficiency in chronic and delayed-onset mustard gas keratopathy. Ophthalmology 2010;117:246–252
   PubMed Web of Science ®Google Scholar
• Baradaran-Rafii A, Eslani M, Tseng SC. Sulfur mustard-induced ocular surface disorders. Ocular Surf 2011;9:163–178
   PubMed Web of Science ®Google Scholar
• Kadar T, Horwitz V, Sahar R, Cohen M, Cohen L, Gez R, et al. Delayed loss of corneal epithelial stem cells in a chemical injury model associated with limbal stem cell deficiency in rabbits. Cur Eye Res 2011;36:1098–1107
   PubMed Web of Science ®Google Scholar
• McNutt P, Hamilton T, Nelson M, Adkins A, Swartz A, Lawrence R, et al. Pathogenesis of acute and delayed corneal lesions after ocular exposure to sulfur mustard vapor. Cornea 2012;31:280--290
   PubMed Web of Science ®Google Scholar
• Amano S, Rohan R, Kuroki M, Tolentino M, Adamis AP. Requirement for vascular endothelial growth factor in wound and inflammation related corneal neovascularization. Invest Ophthalmol Vis Sci 1998;39:18–22
   PubMed Web of Science ®Google Scholar
• Chang JH, Gabison EE, Kato T, Azar D. Corneal neovascularization. Opin Ophthalmol 2001;12:242–249
   PubMed Web of Science ®Google Scholar
• McNutt P, Lyman M, Swartz A, Tuznik K, Kniffin D, Whitten K, et al. Architectural and biochemical expressions of mustard gas keratopathy: preclinical indicators and pathogenic mechanisms. PLos ONE 2012;7:e42837. doi:10.1371
   PubMed Web of Science ®Google Scholar
• Van Setten GB. Vascular endothelial growth factor (VEGF) in normal human corneal epithelium: detection and physiological importance. Acta Ophthalmol Scand 1997;75:649–652
   PubMedGoogle Scholar
• Witmer AN, Vrensen GF, Van Noorden CJ, Schlingemann RO. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Ret Eye Res 2003;22:1–29
   PubMed Web of Science ®Google Scholar
• Chang JH, Garg NK, Lunde E, Han KY, Jain S, Azar DT. Corneal neovascularization: an anti-VEGF therapy review. Surv Ophthalmol 2012;57:415–429
   PubMed Web of Science ®Google Scholar
• Philip W, Speicher L, Humpel C. Expression of vascular endothelial growth factor and its receptors in inflamed and vascularized human corneas. Invest Ophthalmol Vis Sci 2000;41:2514–2522
   Google Scholar
• Cursiefen C, Rummelt C, Kuchle M. Immunohistochemical localization of vascular endothelial growth factor, transforming growth factor alpha and transforming growth factor beta 1 in human corneas with neovascularization. Cornea 2000;19:526–533
   PubMed Web of Science ®Google Scholar
• Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Streilein W. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 2004;113:1040–1050
   PubMed Web of Science ®Google Scholar
• Kvanta A. Ocular angiogenesis: the role of growth factors. Acta Ophthalmol Scand 2006;84:282–288
   PubMedGoogle Scholar
• Amir A, Turetz J, Chapman S, Fishbeine E, Meshulam J, Sahar R, et al. Beneficial effects of topical anti-inflammatory drugs against sulfur mustard-induced ocular lesions in rabbits. J Appl Toxicol 2000;20:S109–S114
   PubMedGoogle Scholar
• Stevenson W, Cheng SF, Dastjerdi MH, Ferrari G, Dana R. Corneal neovascularization and the utility of topical VEGF inhibition: ranibizumab (Lucentis) vs bevacizumab (Avastin). Ocul Surf 2012;10:67–83
   PubMed Web of Science ®Google Scholar
• Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocrine Rev 2004;25:581–611
   PubMed Web of Science ®Google Scholar
• Ferrara N, Hillan KJ, Novotny W. Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy. Biochem Biophys Res Commun 2005;333:328–335
   PubMed Web of Science ®Google Scholar
• Bock F, Konig Y, Fruse f, Baier M, Curseifen C. Bavacizumab (avastin) eye drops inhibit corneal neovascularization. Graefes Arch Clin Exp Ophthalmol 2008;246:281–284
   PubMed Web of Science ®Google Scholar
• Dastjerdi MH, Al-Arfaj KM, Nallasamy N, Hamrah P, Jurkunas UV, Pineda R, et al. Topical Bevacizumab in the treatment of corneal neovascularization. Arch Ophthalmol 2009;127:381–389
   PubMedGoogle Scholar
• Kim SW, Ha BJ, Kim EK, Tchah H, Kim T. The effect of topical bevacizumab on corneal neovascularization. Ophthalmology 2008;115:33–38
   Web of Science ®Google Scholar
• Kim T, Chung JL, Hong JP, Min K, Seo KY, Kim EK. Bevacizumab application delays epithelial healing in rabbit cornea. Invest Ophthalmol Vis Sci 2009;50:4653–4659
   PubMed Web of Science ®Google Scholar
• Cheng SF, Dastjerd MH, Ferrari G, Okanobo A, Bower KS, Ryan D, et al. Short-term bevacizumab in the treatment of stable neovascularization. Am J Ophthalmol 2012;154:940–948
   PubMed Web of Science ®Google Scholar
• Manzano RPA, Peyman GA, Khan P, Carvounis PE, Lake JC, Chvez-Barrios P. Inhibition of experimental corneal neovascularization by bevacizumab (Avastin). Br J Ophthalmol 2007;91:804–807
   PubMed Web of Science ®Google Scholar
• Papathanassiou M, Theodoropoulou S, Analitis A, Tzonou A, Theodossiadis PG. Vascular endothelial growth factor inhibitors for treatment of corneal neovascularization: a meta-analysis. Cornea 2012;4. ahead of print
   Google Scholar
• Yan J, Zeng Y, Jiang J, Zhou J, Yin Z, Wang Z, et al. The expression pattern of vascular endothelial growth factor and thrombospondin 2 after corneal alkali burn. Colloid Surf 2007;60:105–109
   PubMed Web of Science ®Google Scholar
• Pan z, Fukuoka S, Karagianni N, Guaiquil VH, Rosenblatt MI. Vascular endothelial growth factor promotes anatomical and functional recovery of injured peripheral nerves in the avascular cornea. FASEB J 2013;27:1 . doi:10.1096/fj.12-225185
   Google Scholar
• Habot-Wilner Z, Barequet IS, Ivanir Y, Moisseiev J, Rosner M. The inhibitory effect of different concentrations of topical bevacizumab on corneal neovascularization. Acta Ophthalmol 2010;88:862–867
   PubMed Web of Science ®Google Scholar
• Kim TI, Kim SW, Kim S, Kim EK. Inhibition of experimental corneal neovascularization by using subconjunctival injection of bevacizumab (Avastin). Cornea 2008;27:349–352
   PubMedGoogle Scholar
• Oner V, Kucukerdonmez C, Akova YA, Colak A, Karalezli A. Topical and subconjuinctival bevacizumab for corneal neovascularization in an experimental rat model. Ophthal Res 2012;48:118–123
   PubMed Web of Science ®Google Scholar
• Dastjerdi MH, Sadrai Z, Saban D, Zhang Q, Dana R. Corneal penetration and subconjunctival bevacizumab (Avastin). Invest Ophthalmol Vis Sci 2011;52:8718–8723
   PubMed Web of Science ®Google Scholar
• Yoeruek E, Ziemssen F, Henke-Fahle S, Tatat O, Tura A, Grisanti S, et al. Safety, penetration and efficacy of topically applied bevacizumab:evaluation of eye drops in corneal neovascularization after chemical burn. Acta Ophthalmol 2008;86:322–328
   PubMed Web of Science ®Google Scholar
• Hashemian MN, Z-Mehrjardi H, Moghimi S, Tahvildari M, Mojazi-Amiri H. Prevention of corneal neovscularization: comparison of different doses of subconjunctival bevacizumab with its topical form in experimental rats. Ophthalmic Res 2011;46:50–54
   PubMed Web of Science ®Google Scholar
• Benayoun Y, Adenis JP, Casse G, Forte R, Robert PY. Effects of subconjunctival bevacizumab on corneal neovascularization: results of a prospective study. Cornea 2012;31:937–944
   Google Scholar
• Dursun A, Arici MK, Dursun F, Ozec AV, Toker MI, Erdogan H, et al. Comparison of the effects of bevacizumab and ranibizumab injection on corneal angiogenesis in an alkali burn induced model. Int J Ophthalmol 2012;5:448–451
   PubMed Web of Science ®Google Scholar
• Vieira ACC, Hofling-Lima AL, Gomes JAP, Freitas D, Farah ME, Belfort R. Intrastromal injection of bevacizumab in patients with corneal neovascularization. Arq Bras Oftalmol 2012;75:277–279
   PubMed Web of Science ®Google Scholar
• Peters S, Julien S, Heiduschka P, et al. Anti-permeability and anti-proliferative effects of standard and frozen bevacizumab on choroidal endothelial cells. Br J Ophthalmol 2007;91:827–831
   PubMed Web of Science ®Google Scholar
• Nakao S, Zandi S, Lara-Castillo N, Taber M, Ishibashi T, Moghadam AH. Larger therapeutic window for steroid versus VEGF-A inhibitor in inflammatory angiogenesis: surprisingly similar impact on leukocyte infiltration. Invest Ophthalmol. Vis Sci 2012;53:3296–3302
   Google Scholar
• Oh JY, Kim MK, Shin MS, Lee HJ, Lee JH, Wee WR. The anti-inflammatory effect of subconjunctival bevacizumab on chemically burned rat corneas. Cur Eye Res 2009;84:85–91
   Google Scholar
• Bock F, Onderka J, Dietrich T, Bachmann B, Kruse FE, Paschke M, et al. Bavacizumab as a potent inhibitor of inflammatory corneal angiogenesis and lymphangiogenesis. Invest Ophthalmol Vis Sci 2007;48:2545–2552
   PubMed Web of Science ®Google Scholar
• Hoffart L, Matonti F, Conrath J, Daniel L, Ridings B, Masson GS, et al. Inhibition of corneal neovascularization after alkali burn: comparison of different doses of bevacizumab in monotherapy or associated with dexamethasone. Clin Exp Ophthalmol 2010;38:346–352
   PubMed Web of Science ®Google Scholar
• Rosenstein JM, Krum JM. New roles for VEGF in nervous tissue – beyond blood vessels. Exp Neurol 2004;187:246–253
   PubMed Web of Science ®Google Scholar
• Azar DT. Corneal angiogenic privilege: angiogenic and antiangiogenic factors in corneal avascularity, vasculogenesis and wound healing. Trans Am Ophthalmol Soc 2006;104:264–302
   PubMedGoogle Scholar
• Kadar T, Dachir S, Cohen M, Gutman H, Cohen L, Brandeis R, et al. Prolonged impairment of corneal innervation after exposure to sulfur mustard and its relation to the development of delayed limbal stem cell deficiency. Cornea 2013;32:e44–50
   PubMed Web of Science ®Google Scholar
• Yu CQ, Zhang M, Matis KI, Kim C, Rosenblatt MI. Vascular endothelial growth factor mediates corneal nerve repair. Invest Ophthalmol Vis Sci 2008;49:3870–3878
   PubMed Web of Science ®Google Scholar
• Li Z., Burns AR, Han L, Rumbaut RE, Smith CW. IL-17 and VEGF are necessary for efficient corneal nerve regeneration. Am J Pathol 2011;178:1106–1116
   PubMed Web of Science ®Google Scholar
• Ueno H, Ferrari G, Hattori T, Saban DR, Katikireddy KR, Chauhan SK, et al. Dependence of corneal stem/progenitor cells on ocular surface innervation. Invest Ophthalmol Vis Sci 2012;53:867–872
   PubMed Web of Science ®Google Scholar
• Ferrari G, Hajrasouliba AR, Sadrai Z, Ueno H, Chauban SK, Dana R. Nerves and neovessels inhibit each other in the cornea. Invest Ophthalmol Vis Sci 2013;54:813–820
   Google Scholar
• Colombres GA, Gramajo AL, Arrambide MP, Juarez SM, Arevalo JF, Bar J, et al. Delayed corneal epithelial healing after intravitreal bevacizumab: a clinical and experimental study. J Ophthalmic Vis Res 2011;6:18–25
   Google Scholar
• Storkebaum E, Lambrechts D, Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 2004;26:943–954
   PubMed Web of Science ®Google Scholar