Verteporfin photodynamic therapy and anti-angiogenic drugs: potential for combination therapy in exudative age-related macular degeneration

References

• Kaiser PK. Verteporfin therapy in combination with triamcinolone: published studies investigating a potential synergistic effect. Curr Med Res Opin 2005;21:705–13
   PubMed Web of Science ®Google Scholar
• Zarbin MA. Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol 2004;122:598–614
   PubMed Web of Science ®Google Scholar
• Pe’er J, Shweiki D, Itin A, et al. Hypoxia-induced expression of vascular endothelial growth factor by retinal cells is a common factor in neovascularizing ocular diseases. Lab Invest 1995;72:638–45
   Google Scholar
• Grunwald JE, Metelitsina TI, Dupont JC, et al. Reduced foveolar choroidal blood flow in eyes with increasing AMD severity. Invest Ophthalmol Vis Sci 2005;46:1033–8
   PubMed Web of Science ®Google Scholar
• Yoshida S, Yoshida A, Ishibashi T. Induction of IL-8, MCP-1, and bFGF by TNF-alpha in retinal glial cells: implications for retinal neovascularization during post-ischemic inflammation. Graefes Arch Clin Exp Ophthalmol 2004;242: 409–13
   Google Scholar
• Spaide RF. Rationale for combination therapies for choroidal neovascularization. Am J Ophthalmol 2006;141:149–56
   PubMed Web of Science ®Google Scholar
• Campochiaro PA. Ocular neovascularisation and excessive vascular permeability. Expert Opin Biol Ther 2004;4:1395–402
   PubMed Web of Science ®Google Scholar
• Shima DT, Adamis AP, Ferrara N, et al. Hypoxic induction of endothelial cell growth factors in retinal cells: identification and characterization of vascular endothelial growth factor (VEGF) as the mitogen. Mol Med 1995;1:182–93
   PubMed Web of Science ®Google Scholar
• Keyt BA, Berleau LT, Nguyen HV, et al. The carboxyl-terminal domain (111–165) of vascular endothelial growth factor is critical for its mitogenic potency. J Biol Chem 1996;271:7788–95
   PubMed Web of Science ®Google Scholar
• Park JE, Keller GA, Ferrara N. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell 1993;4:1317–26
   Google Scholar
• Ng EW, Adamis AP. Targeting angiogenesis, the underlying disorder in neovascular age-related macular degeneration. Can J Ophthalmol 2005;40:352–68
   PubMed Web of Science ®Google Scholar
• Shima DT, Kuroki M, Deutsch U, et al. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J Biol Chem 1996;271:3877–83
   Google Scholar
• Ishida S, Usui T, Yamashiro K, et al. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J Exp Med 2003;198:483–9
   PubMed Web of Science ®Google Scholar
• McColm JR, Geisen P, Hartnett ME. VEGF isoforms and their expression after a single episode of hypoxia or repeated fluctuations between hyperoxia and hypoxia: relevance to clinical ROP. Mol Vis 2004;10:512–20
   Google Scholar
• Hiromatsu Y, Toda S. Mast cells and angiogenesis. Microsc Res Tech 2003;60:64–9
   PubMed Web of Science ®Google Scholar
• Miyamoto K, Khosrof S, Bursell SE, et al. Vascular endothelial growth factor (VEGF)-induced retinal vascular permeability is mediated by intercellular adhesion molecule-1 (ICAM-1). Am J Pathol 2000;156:1733–9
   PubMed Web of Science ®Google Scholar
• Cursiefen C, Chen L, Borges LP, et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 2004;113:1040–50
   PubMed Web of Science ®Google Scholar
• Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A 1995;92:10457–61
   PubMed Web of Science ®Google Scholar
• Krzystolik MG, Afshari MA, Adamis AP, et al. Prevention of experimental choroidal neovascularization with intravitreal anti-vascular endothelial growth factor antibody fragment. Arch Ophthalmol 2002;120:338–46
   PubMed Web of Science ®Google Scholar
• Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 1994;331: 1480–7
   PubMed Web of Science ®Google Scholar
• Malecaze F, Clamens S, Simorre-Pinatel V, et al. Detection of vascular endothelial growth factor messenger RNA and vascular endothelial growth factor-like activity in proliferative diabetic retinopathy. Arch Ophthalmol 1994;112:1476–82
   Google Scholar
• Schwesinger C, Yee C, Rohan RM, et al. Intrachoroidal neovascularization in transgenic mice overexpressing vascular endothelial growth factor in the retinal pigment epithelium. Am J Pathol 2001;158:1161–72
   PubMed Web of Science ®Google Scholar
• Tolentino MJ, Miller JW, Gragoudas ES, et al. Vascular endothelial growth factor is sufficient to produce iris neovascularization and neovascular glaucoma in a nonhuman primate. Arch Ophthalmol 1996;114:964–70
   PubMed Web of Science ®Google Scholar
• Tolentino MJ, McLeod DS, Taomoto M, et al. Pathologic features of vascular endothelial growth factor-induced retinopathy in the nonhuman primate. Am J Ophthalmol 2002;133:373–85
   PubMed Web of Science ®Google Scholar
• He S, Jin ML, Worpel V, Hinton DR. A role for connective tissue growth factor in the pathogenesis of choroidal neovascularization. Arch Ophthalmol 2003;121:1283–8
   PubMed Web of Science ®Google Scholar
• Kliffen M, Sharma HS, Mooy CM, et al. Increased expression of angiogenic growth factors in age-related maculopathy. Br J Ophthalmol 1997;81:154–62
   PubMed Web of Science ®Google Scholar
• Holekamp NM, Bouck N, Volpert O. Pigment epithelium-derived factor is deficient in the vitreous of patients with choroidal neovascularization due to age-related macular degeneration. Am J Ophthalmol 2002;134:220–7
   Google Scholar
• Zhang SX, Wang JJ, Mott R, Ma J-X. Pigment epithelium-derived factor: an endogenous anti-inflammatory factor in the eye. Invest Ophthalmol Vis Sci 2005;46:E-Abstract 4705
   Google Scholar
• Schmidt-Erfurth U, Schlotzer-Schrehard U, Cursiefen C, et al. Influence of photodynamic therapy on expression of vascular endothelial growth factor (VEGF), VEGF receptor 3, and pigment epithelium-derived factor. Invest Ophthalmol Vis Sci 2003;44:4473–80
   PubMed Web of Science ®Google Scholar
• Fischer S, Renz D, Schaper W, Karliczek GF. In vitro effects of dexamethasone on hypoxia-induced hyperpermeability and expression of vascular endothelial growth factor. Eur J Pharmacol 2001;411:231–43
   PubMed Web of Science ®Google Scholar
• Folkman J. Angiogenesis and angiogenesis inhibition: an overview. EXS 1997;79:1–8
   PubMedGoogle Scholar
• Crum R, Szabo S, Folkman J. A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment. Science 1985;230:1375–8
   Google Scholar
• Penfold PL, Wen L, Madigan MC, et al. Triamcinolone acetonide modulates permeability and intercellular adhesion molecule-1 (ICAM-1) expression of the ECV304 cell line: implications for macular degeneration. Clin Exp Immunol 2000;121:458–65
   PubMed Web of Science ®Google Scholar
• Penfold PL, Wen L, Madigan MC, et al. Modulation of permeability and adhesion molecule expression by human choroidal endothelial cells. Invest Ophthalmol Vis Sci 2002;43:3125–30
   PubMed Web of Science ®Google Scholar
• Adamis AP, Shima DT. The role of vascular endothelial growth factor in ocular health and disease. Retina 2005;25:111–8
   PubMed Web of Science ®Google Scholar
• Gragoudas ES, Adamis AP, Cunningham ET, Jr., et al. Pegaptanib for neovascular age-related macular degeneration. N Engl J Med 2004;351:2805–16
   PubMed Web of Science ®Google Scholar
• Ruckman J, Green LS, Beeson J, et al. 2’-Fluoropyrimidine RNA-based aptamers to the 165-amino acid form of vascular endothelial growth factor (VEGF165). Inhibition of receptor binding and VEGF-induced vascular permeability through interactions requiring the exon 7-encoded domain. J Biol Chem 1998;273: 20556–67
   Google Scholar
• Chakravarthy U, Adamis AP, Cunningham ET, Jr., et al. Year 2 efficacy results of 2 randomized controlled clinical trials of pegaptanib for neovascular age-related macular degeneration. Ophthalmology 2006;113:1508–25
   PubMed Web of Science ®Google Scholar
• Gaudreault J, Fei D, Rusit J, et al. Preclinical pharmacokinetics of Ranibizumab (rhuFabV2) after a single intravitreal administration. Invest Ophthalmol Vis Sci 2005;46:726–33
   PubMed Web of Science ®Google Scholar
• Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 2006;355:1419–31
   PubMed Web of Science ®Google Scholar
• Brown DM, Kaiser PK, Michels M, et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 2006;355:1432–44
   PubMed Web of Science ®Google Scholar
• Heier JS, Antoszyk AN, Pavan PR, et al. Ranibizumab for treatment of neovascular age-related macular degeneration: a phase I/II multicenter, controlled, multidose study. Ophthalmology 2006;113(4):642.e1–4
   Google Scholar
• Slakter JS, Bochow TW, D’Amico DJ, et al. Anecortave acetate (15 milligrams) versus photodynamic therapy for treatment of subfoveal neovascularization in age-related macular degeneration. Ophthalmology 2006;113: 3–13
   Google Scholar
• Clark AF. AL-3789: a novel ophthalmic angiostatic steroid. Expert Opin Investig Drugs 1997;6:1867–77
   PubMedGoogle Scholar
• Benezra D, Griffin BW, Maftzir G, et al. Topical formulations of novel angiostatic steroids inhibit rabbit corneal neovascularization. Invest Ophthalmol Vis Sci 1997;38:1954–62
   PubMed Web of Science ®Google Scholar
• Clark AF, Mellon J, Li XY, et al. Inhibition of intraocular tumor growth by topical application of the angiostatic steroid anecortave acetate. Invest Ophthalmol Vis Sci 1999;40:2158–62
   PubMed Web of Science ®Google Scholar
• McNatt LG, Weimer L, Yanni J, Clark AF. Angiostatic activity of steroids in the chick embryo CAM and rabbit cornea models of neovascularization. J Ocul Pharmacol Ther 1999;15:413–23
   PubMed Web of Science ®Google Scholar
• Penn JS, Rajaratnam VS, Collier RJ, Clark AF. The effect of an angiostatic steroid on neovascularization in a rat model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 2001;42: 283–90
   PubMed Web of Science ®Google Scholar
• Anecortave Acetate Study Group. Anecortave acetate as monotherapy for the treatment of subfoveal lesions in patients with exudative age-related macular degeneration (AMD): interim (month 6) analysis of clinical safety and efficacy. Retina 2003;23:14–23
   PubMed Web of Science ®Google Scholar
• Anecortave Acetate Study Group. Anecortave acetate as monotherapy for treatment of subfoveal neovascularization in age-related macular degeneration: twelve-month clinical outcomes. Ophthalmology 2003;110:2372–83
   PubMed Web of Science ®Google Scholar
• Schmidt-Erfurth U, Michels S, Michels R, Aue A. Anecortave acetate for the treatment of subfoveal choroidal neovascularization secondary to age-related macular degeneration. Eur J Ophthalmol 2005;15:482–5
   Google Scholar
• Rosenfeld PJ, Fung AE, Puliafito CA. Optical coherence tomography findings after an intravitreal injection of bevacizumab (Avastin) for macular edema from central retinal vein occlusion. Ophthalmic Surg Lasers Imaging 2005;36:336–9
   Google Scholar
• Michels S, Rosenfeld PJ, Puliafito CA, et al. Systemic bevacizumab (Avastin) therapy for neovascular age-related macular degeneration twelve-week results of an uncontrolled open-label clinical study. Ophthalmology 2005;112:1035–47
   PubMed Web of Science ®Google Scholar
• Spaide RF, Laud K, Fine HF, et al. Intravitreal bevacizumab treatment of choroidal neovascularization secondary to age-related macular degeneration. Retina 2006;26:383–90
   PubMed Web of Science ®Google Scholar
• Avery RL, Pieramici DJ, Rabena MD, et al. Intravitreal bevacizumab (Avastin) for neovascular age-related macular degeneration. Ophthalmology 2006;113:363–72
   PubMed Web of Science ®Google Scholar
• Manzano RP, Peyman GA, Khan P, Kivilcim M. Testing intravitreal toxicity of bevacizumab (Avastin). Retina 2006;26:257–61
   PubMed Web of Science ®Google Scholar
• Kwak N, Okamoto N, Wood JM, Campochiaro PA. VEGF is major stimulator in model of choroidal neovascularization. Invest Ophthalmol Vis Sci 2000;41:3158–64
   PubMed Web of Science ®Google Scholar
• Shen J, Samul R, Silva RL, et al. Suppression of ocular neovascularization with siRNA targeting VEGF receptor 1. Gene Ther 2006;13:225–34
   PubMed Web of Science ®Google Scholar
• Ciulla TA, Criswell MH, Danis RP, et al. Squalamine lactate reduces choroidal neovascularization in a laser-injury model in the rat. Retina 2003;23:808–14
   PubMed Web of Science ®Google Scholar
• Campochiaro PA, Dong NQ, Mahmood SS, et al. Adenoviral vector-delivered pigment epithelium-derived factor for neovascular age-related macular degeneration: results of a phase I clinical trial. Hum Gene Ther 2006;17:177–9
   PubMed Web of Science ®Google Scholar
• Michels S, Schmidt-Erfurth U. Sequence of early vascular events after photodynamic therapy. Invest Ophthalmol Vis Sci 2003;44:2147–54
   PubMed Web of Science ®Google Scholar
• Schmidt-Erfurth U, Hasan T. Mechanisms of action of photodynamic therapy with verteporfin for the treatment of age-related macular degeneration. Surv Ophthalmol 2000;45: 195–214
   Google Scholar
• van den Bergh H, Ballini JP, Debefve E, Pegaz B. Video monitoring of neovessel thrombosis in real time using photodynamic therapy with verteporfin (Visudyne). Invest Ophthalmol Vis Sci 2006;47:E-Abstract 914
   Google Scholar
• Verteporfin Roundtable Participants. Guidelines for using verteporfin (Visudyne) in photodynamic therapy for choroidal neovascularization due to age-related macular degeneration and other causes: update. Retina 2005;25:119–34
   PubMed Web of Science ®Google Scholar
• Treatment of Age-Related Macular Degeneration with Photo-dynamic Therapy (TAP) Study Group. Photodynamic therapy of subfoveal choroidal neovascularization in age-related macular degeneration with verteporfin: two-year results of 2 randomized clinical trials–TAP Report 2. Arch Ophthalmol 2001;119: 198–207
   Google Scholar
• Verteporfin In Photodynamic Therapy (VIP) Study Group. Verteporfin therapy of subfoveal choroidal neovascularization in age-related macular degeneration: two-year results of a randomized clinical trial including lesions with occult with no classic choroidal neovascularization–Verteporfin In Photodynamic Therapy Report 2. Am J Ophthalmol 2001;131: 541–60
   Google Scholar
• Visudyne In Minimally Classic CNV (VIM) Study Group. Verteporfin therapy of subfoveal minimally classic choroidal neovascularization in age-related macular degeneration: 2-year results of a randomized clinical trial. Arch Ophthalmol 2005;123: 448–57
   Google Scholar
• Treatment of Age-Related Macular Degeneration with Photo-dynamic Therapy (TAP) and Verteporfin In Photodynamic Therapy (VIP) Study Groups. Verteporfin therapy of subfoveal choroidal neovascularization in age-related macular degeneration: meta-analysis of 2-year safety results in three randomized clinical trials: Treatment Of Age-Related Macular Degeneration With Photodynamic Therapy and Verteporfin In Photodynamic Therapy Study Report No. 4. Retina 2004; 24:1–12
   Google Scholar
• Treatment of Age-Related Macular Degeneration with Photo-dynamic Therapy (TAP) and Verteporfin In Photodynamic Therapy (VIP) Study Groups. Acute severe visual acuity decrease after photodynamic therapy with verteporfin: case reports from randomized clinical trials–TAP and VIP Report No. 3. Am J Ophthalmol 2004;137: 683–96
   Google Scholar
• Kaiser PK, Treatment of Age-Related Macular Degeneration with Photodynamic Therapy (TAP) Study Group. Verteporfin therapy of subfoveal choroidal neovascularization in age-related macular degeneration: 5-year results of two randomized clinical trials with an open-label extension–TAP Report No. 8. Graefes Arch Clin Exp Ophthalmol 2006;244: 1132–1142
   Google Scholar
• Semenza GL. Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol 2000;59:47–53
   PubMed Web of Science ®Google Scholar
• Michels S, Hansmann F, Geitzenauer W, Schmidt-Erfurth U. Influence of treatment parameters on selectivity of verteporfin therapy. Invest Ophthalmol Vis Sci 2006;47:371–6
   PubMed Web of Science ®Google Scholar
• Gremigni E, Falleni A, Belting C, et al. Choroidal neovascular membranes after photodynamic therapy: ultrastructural analysis of two surgically excised membranes. Eur J Ophthalmol 2004;14:555–61
   PubMed Web of Science ®Google Scholar
• Schmidt-Erfurth U, Michels S, Barbazetto I, Laqua H. Photodynamic effects on choroidal neovascularization and physiological choroid. Invest Ophthalmol Vis Sci 2002;43: 830–41
   PubMed Web of Science ®Google Scholar
• Yeh DC, Bula DV, Miller JW, et al. Expression of leukocyte adhesion molecules in human subfoveal choroidal neovascular membranes treated with and without photodynamic therapy. Invest Ophthalmol Vis Sci 2004;45:2368–73
   PubMed Web of Science ®Google Scholar
• Schmidt-Erfurth U, Laqua H, Schlotzer-Schrehard U, et al. Histopathological changes following photodynamic therapy in human eyes. Arch Ophthalmol 2002;120:835–44
   PubMedGoogle Scholar
• Husain D, Kim I, Gauthier D, et al. Safety and efficacy of intravitreal injection of ranibizumab in combination with verteporfin PDT on experimental choroidal neovascularization in the monkey. Arch Ophthalmol 2005;123:509–16
   PubMed Web of Science ®Google Scholar
• Kim IK, Husain D, Michaud N, et al. Effect of Intravitreal Injection of Ranibizumab in Combination with Verteporfin PDT on Normal Primate Retina and Choroid. Invest Ophthalmol Vis Sci 2006;47:357–63
   PubMed Web of Science ®Google Scholar
• Eyetech Study Group. Anti-vascular endothelial growth factor therapy for subfoveal choroidal neovascularization secondary to age-related macular degeneration: phase II study results. Ophthalmology 2003;110:979–86
   PubMed Web of Science ®Google Scholar
• Eyetech Pharma. Division of Anti-inflammatory, Analgesic and Ophthalmic Drug Products Advisory Committee Meeting Briefing Package for Macugen, 2004. Available at http://www. fda.gov/ohrms/dockets/ac/04/briefing/2004–4053B1_02_FDABackgrounder.pdf (Accessed October 30, 2006)
   Google Scholar
• Heier JS, Boyer DS, Ciulla TA, et al. Ranibizumab in combination with verteporfin photodynamic therapy in neovascular age-related macular degeneration (FOCUS): year 1 results. Arch Ophthalmol (in press).
   Google Scholar
• Genentech. Preliminary phase I/II data show Lucentis in combination with Visudyne maintained or improved vision in approximately 90 percent of patients with wet age-related macular degeneration. Press release 31 May, 2005. Available at http://www.gene.com/gene/news/press-releases/
   Google Scholar
• Genentech. Preliminary phase I/II study showed Lucentis improved vision in patients with wet age-related macular degeneration when used in combination with Visudyne. Press release 18 July, 2005. Available at http://www.gene.com/gene/ news/press-releases/
   Google Scholar
• Korotkin A, Kozak I, Morrison VL, et al. An emerging problem: recurrence of CNV is common after cessation of 24 month treatment with ranibizumab (Lucentis). Invest Ophthalmol Vis Sci 2006;47:E-abstract 2961
   Google Scholar
• Schmidt-Erfurth U, Gabel P, Hohman T. Preliminary results form an open-lable, multicenter, phase II study assessing the effects of same-day administration of ranibizumab (Lucentis™) and verteporfin PDT (PROTECT study). Invest Ophthalmol Vis Sci 2006;47:E-Abstract 2960
   Google Scholar
• Mieler WF, The VERITAS Trial study group. VERITAS - The rationale and design of a combination therapy trial for wet AMD. Invest Ophthalmol Vis Sci 2006;47:Abstract 5232
   Google Scholar
• Singh RP, Kaiser PK. Highlights of the Retinal Physician 2006 Symposium. Available at http://www.medscape.com/ viewarticle/536359 (Accessed October 30, 2006)
   Google Scholar