Anti–Vascular Endothelial Growth Factor Agents in the Treatment of Retinal Disease: From Bench to Bedside

Ophthalmology

Volumn 123, Issue 10, 2016, Pages S78-S88

  Campochiaro, Peter A ^a   Aiello, Lloyd Paul ^b   Rosenfeld, Philip J ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFLIBERCEPT; ANGIOPOIETIN 2; BEVACIZUMAB; CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; PEGAPTANIB; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN TYROSINE PHOSPHATASE; RANIBIZUMAB; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN; VASCULOTROPIN 165; VASCULOTROPIN A; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

AGE RELATED MACULAR DEGENERATION; ANTIANGIOGENIC ACTIVITY; ARTICLE; BEST CORRECTED VISUAL ACUITY; BONE MARROW CELL; DIABETIC MACULAR EDEMA; DIABETIC RETINOPATHY; HUMAN; HYPOXIA; MACULAR EDEMA; MOLECULAR PATHOLOGY; MULTICENTER STUDY (TOPIC); NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); POLYPOIDAL CHOROIDAL VASCULOPATHY; PRIORITY JOURNAL; PROLIFERATIVE DIABETIC RETINOPATHY; RANDOMIZED CONTROLLED TRIAL (TOPIC); RETINA DISEASE; RETINA HEMORRHAGE; RETINA ISCHEMIA; RETINA NEOVASCULARIZATION; RETINA VEIN OCCLUSION; SUBRETINAL NEOVASCULARIZATION; UPREGULATION;

EID: 84992597388     PISSN: 01616420     EISSN: 15494713     Source Type: Journal    
DOI: 10.1016/j.ophtha.2016.04.056     Document Type: Article

References (93)

1. 1 Michaelson, I., The mode of development of the vascular system of the retina with some observations on its significance for certain retinal diseases. Trans Ophthalmol Soc UK 68 (1948), 137–180.
2. 2 Ashton, N., Retinal vascularization in health and disease. Am J Ophthalmol 44 (1957), 7–17.
3. 3 Baird, A., Esch, F., Gospodarowicz, D., Guillemin, R., Retina- and eye-derived endothelial cell growth factors: partial molecular characterization and identity with acidic and basic fibroblast growth factors. Biochemistry 24 (1985), 7855–7860.
4. 4 Montesano, R., Vassali, J.D., Baird, A., et al. Basic fibroblast growth factor induces angiogenesis in vitro. Proc Natl Acad Sci U S A 83 (1986), 7297–7301.
5. 5 Tobe, T., Ortega, S., Luna, J.D., et al. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am J Pathol 153 (1998), 1641–1646.
6. 6 Senger, D.R., Galli, S.J., Dvorak, A.M., et al. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219 (1983), 983–985.
7. 7 Leung, D.W., Cachianes, G., Kuang, W.-J., et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246 (1989), 1306–1309.
8. 8 Keck, P.J., Hauser, S.D., Krivi, G., et al. Vacular permeability factor, an endothelial cell mitogen related to PDGF. Science 246 (1989), 1309–1312.
9. 9 Plate, K.H., Breier, G., Welch, H.A., Risau, W., Vascular endothelial growth factor is a potential tumor angiogenesis factor in human gliomas in vivo. Nature 359 (1992), 845–848.
10. 10 Shweiki, D., Itin, A., Soffer, D., Keshet, E., Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359 (1992), 843–845.
11. 11 Aiello, L.P., Avery, R.L., Arrigg, P.G., et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331 (1994), 1480–1487.
12. 12 Miller, J.W., Adamis, A.P., Shima, D.T., et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol 145 (1994), 574–584.
13. 13 Smith, L.E.H., Wesolowski, E., McLellan, A., et al. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35 (1994), 101–111.
14. 14 Pierce, E.A., Avery, R.L., Foley, E.D., et al. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A 92 (1995), 905–909.
15. 15 Alon, T., Hemo, I., Itin, A., et al. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nature Med 1 (1995), 1024–1028.
16. 16 Aiello, L.P., Pierce, E.A., Foley, E.D., 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 92 (1995), 10457–10461.
17. 17 Tolentino, M.J., Miller, J.W., Gragoudas, E.S., et al. Vascular endothelial growth factor is sufficient to produce iris neovascularization and neovascular glaucoma in a nonhuman primate. Arch Ophthalmol 114 (1996), 964–970.
18. 18 Tolentino, M.J., Miller, J.W., Gragoudas, E.S., et al. Intravitreous injections of vascular endothelial growth factor produce retinal ischemia and microangiopathy in an adult primate. Ophthalmology 103 (1996), 1820–1828.
19. 19 Ozaki, H., Hayashi, H., Vinores, S.A., et al. Intravitreal sustained release of VEGF causes retinal neovascularization in rabbits and breakdown of the blood-retinal barrier in rabbits and primates. Exp Eye Res 64 (1997), 505–517.
20. 20 Okamoto, N., Tobe, T., Hackett, S.F., et al. Transgenic mice with increased expression of vascular endothelial growth factor in the retina: a new model of intraretinal and subretinal neovascularization. Am J Pathol 151 (1997), 281–291.
21. 21 Ryan, S.J., Subretinal neovascularization: natural history of an experimental model. Arch Ophthalmol 100 (1982), 1804–1809.
22. 22 Dobi, E.T., Puliafito, C.A., Destro, M., A new model of choroidal neovascularization in the rat. Arch Ophthalmol 107 (1989), 264–269.
23. 23 Kwak, N., Okamoto, N., Wood, J.M., Campochiaro, P.A., VEGF is an important stimulator in a model of choroidal neovascularization. Invest Ophthalmol Vis Sci 41 (2000), 3158–3164.
24. 24 Kryzstolik, M.G., Afshari, M.A., Adamis, A.P., et al. Prevention of experimental choroidal neovascularization with intravitreal anti-vascular endothelial growth factor antibody fragment. Arch Ophthalmol 120 (2002), 338–346.
25. R1R2 suppresses choroidal neovascularization and VEGF-induced breakdown of the blood-retinal barrier. J Cell Physiol 195 (2003), 241–248.
26. 26 Ozaki, H., Yu, A., Della, N., et al. Hypoxia inducible factor-1a is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci 40 (1999), 182–189.
27. 27 Semenza, G.L., HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 88 (2000), 1474–1480.
28. 28 Campochiaro, P.A., Molecular pathogenesis of retinal and choroidal vascular diseases. Prog Retin Eye Res 49 (2015), 67–81.
29. 29 Vinores, S.A., Xiao, W.H., Aslam, S., et al. Implication of the hypoxia response element of the VEGF promoter in mouse models of retinal and choroidal neovascularization, but not retinal vascular development. J Cell Physiol 206 (2006), 749–758.
30. 30 Oshima, Y., Oshima, S., Nambu, H., et al. Different effects of angiopoietin 2 in different vascular beds in the eye; new vessels are most sensitive. FASEB J 19 (2005), 963–965.
31. 31 Ng, E.W., Shima, D.T., Calias, P., et al. Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat Rev Drug Discov 5 (2006), 123–132.
32. 32 Gragoudas, E.S., Adamis, A.P., Cunningham, E.T. Jr., et al. Pegaptanib for neovascular age-related macular degeneration. N Engl J Med 351 (2004), 2805–2816.
33. 33 Michels, S., Rosenfeld, P.J., Puliafito, C.A., et al. Systemic bevacizumab (Avastin) therapy for neovascular age-related macular degeneration. Ophthalmology 112 (2005), 1035–1047.
34. 34 Moshfeghi, A.A., Rosenfeld, P.J., Puliafito, C.A., et al. Systemic bevacizumab (Avastin) therapy for neovascular age-related macular degeneration. Twenty-four-week results of an uncontrolled open-label clinical study. Ophthalmology 113 (2006), 2002–2011.
35. 35 Nguyen, Q.D., Shah, S.M., Hafiz, G., et al. Intravenous bevacizumab causes regression of choroidal neovascularization secondary to diseases other than age-related macular degeneration. Am J Ophthalmol 145 (2008), 257–266.
36. 36 Chen, Y., Wiesmann, C., Fuh, G., et al. Selection and analysis of an optimized anti-VEGF antibody: crystal structure of an affinity-matured Fab in complex with antigen. J Mol Biol 293 (1999), 865–881.
37. 37 Ferrara, N., Hillan, K.J., Novotny, W., Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy. Biochm Biophys Res Commun 333 (2005), 328–335.
38. 38 Rosenfeld, P.J., Moshfeghi, A.A., Puliafito, C.A., Optical coherence tomography findings after an intravitreal injection of bevacizumab (Avastin) for neovascular age-related macular degeneration. Ophthalmic Surg Lasers Imaging 36 (2005), 331–335.
39. 39 Rosenfeld, P.J., Brown, D.M., Heier, J.S., et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355 (2006), 1419–1431.
40. 40 Brown, D.M., Kaiser, P.K., Michels, M., et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355 (2006), 1432–1444.
41. 41 CATT Research Group, Martin, D.F., Maguire, M.G., et al. Ranibizumab and bevacizumab for neovascular age-related macular degeneration. N Engl J Med 364 (2011), 1897–1908.
42. 42 The Ivan Study Investigators, Chakravarthy, U., Harding, S.P., et al. Ranibizumab versus bevacizumab to treat neovascular age-related macular degeneration. One year findings from the IVAN randomized trial. Ophthalmology 119 (2012), 1399–1411.
43. 43 Berg, K., Pedersen, T.R., Sandvik, L., Bragadottir, R., Comparison of ranibizumab and bevacizumab for neovascular age-related macular degeneration according to LUCAS treat-and-extend protocol. Ophthalmology 122 (2015), 146–152.
44. 44 Holash, J., Davis, S., Papadoupoulos, N., et al. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci U S A 99 (2002), 11393–11398.
45. 45 Heier, J.S., Brown, D.M., Chong, V., et al. Intravitreal aflibercept (VEGF Trap-Eye) in wet age-related macular degeneration. Ophthalmology 119 (2012), 2537–2548.
46. 46 Fung, A.E., Lalwani, G.A., Rosenfeld, P.J., et al. An optical coherence tomography-guided, variable dosing regimen with intravitreal ranibizumab (Lucentis) for neovascular age-related macular degeneration. Am J Ophthalmol 143 (2007), 566–583.
47. 47 Lalwani, G.A., Rosenfeld, P.J., Fung, A.E., et al. A variable-dosing regimen with intravitreal ranibizumab for neovascular age-related macular degeneration: year 2 of PrONTO Study. Am J Ophthalmol 148 (2009), 43–58.
48. 48 Berg, K., Hadzalic, E., Gjertsen, I., et al. Ranibizumab or bevacizumab for neovascular age-related macular degeneration according to the Lucentis Compared to Avastin Study Treat-and-Extend Protocol: two-year results. Ophthalmology 123 (2016), 51–59.
49. 49 Comparison of Age-Related Macular Degeneration Treatments Trials (CATT) Research Group, Martin, D.F., Maguire, M.G., et al. Ranibizumab and bevacizumab for treatment of neovascular age-related macular degeneration: two-year results. Ophthalmology 119 (2012), 1388–1398.
50. 50 Grunwald, J.E., Daniel, E., Huang, J., et al. Risk of geographic atrophy in the Comparison of Age-Related Macular Degeneration Treatments Trials. Ophthalmology 121 (2012), 150–161.
51. 51 Channa, R., Sophie, R., Bagheri, S., et al. Regression of choroidal neovascularization results in macular atrophy in anti-vascular endothelial growth factor-treated eyes. Am J Ophthalmol 159 (2015), 9–19.
52. 52 Tanaka, E., Chaikitmongkol, V., Bressler, S.B., Bressler, N.M., Vision-threatening lesions developing with longer-term follow-up after treatment of neovascular age-related macular degeneration. Ophthalmology 122 (2015), 153–161.
53. 53 Busbee, B.G., Ho, A.C., Brown, D.M., et al. Twelve-month efficacy and safety of 0.5 mg or 2.0 mg ranibizumab in patients with subfoveal neovascular age-related macular degeneration. Ophthalmology 120 (2013), 1046–1056.
54. 54 Ho, A.C., Busbee, B.G., Regillo, C.D., et al. Twenty-four-month efficacy and safety of 0.5 mg or 2.0 mg ranibizumab in patients with subfoveal neovascular age-related macular degeneration. Ophthalmology 121 (2014), 2181–2192.
55. 55 Koh, A., Lee, W.K., Chen, L.J., et al. EVEREST study: efficacy and safety of verteporfin photodynamic therapy in combination with ranibizumab or alone versus ranibizumab monotherapy in patients with symptomatic macular polypoidal choroidal vasculopathy. Retina 32 (2012), 1453–1464.
56. 56 Nguyen, Q.D., Shah, S.M., Van Anden, E., et al. Supplemental inspired oxygen improves diabetic macular edema: a pilot study. Invest Ophthalmol Vis Sci 45 (2003), 617–624.
57. 57 Ozaki, H., Seo, M.-S., Ozaki, K., et al. Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am J Pathol 156 (2000), 697–707.
58. 58 Campochiaro, P.A., C99-PKC412-003 Study Group. Reduction of diabetic macular edema by oral administration of the kinase inhibitor PKC412. Invest Ophthalmol Vis Sci 45 (2004), 922–931.
59. 59 Nguyen, Q.D., Tatlipinar, S., Shah, S.M., et al. Vascular endothelial growth factor is a critical stimulus for diabetic macular edema. Am J Ophthalmol 142 (2006), 961–969.
60. 60 Nguyen, Q.D., Shah, S.M., Heier, J.S., et al. Primary end point (six months) results of the Ranibizumab for Edema of the mAcula in Diabetes (READ-2) study. Ophthalmology 116 (2009), 2175–2181.
61. 61 The Diabetic Retinopathy Clinical Research Network, Elman, M.J., Aiello, L.M., et al. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology 117 (2010), 1064–1077.
62. 62 Nguyen, Q.D., Brown, D.M., Marcus, D.M., et al. Ranibizumab for diabetic macular edema. Results from 2 phase III randomized trials: RISE and RIDE. Ophthalmology 119 (2012), 789–801.
63. 63 Korobelnik, J.F., Do, D.V., Schmidt-Erfurth, U., et al. Intravitreal aflibercept for diabetic macular edema. Ophthalmology 121 (2014), 2247–2254.
64. 64 The Diabetic Retinopathy Clinical Research Network. Aflibercept, bevacizumab, or ranibizumab for diabetic macular edema. N Engl J Med 372 (2015), 1193–1203.
65. 65 Wells, J.A., Glassman, A.R., Ayala, A.R., et al. Aflibercept, bevacizumab, or ranibizumab for diabetic macular edema. Two-year results from a comparative effectiveness randomized clinical trial. Ophthalmology 123 (2016), 1351–1359.
66. 66 Adamis, A.P., Miller, J.W., Bernal, M.-T., et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol 118 (1994), 445–450.
67. 67 Mendrinos, E., Donati, G., Pournaras, C.J., Rapid and persistent regression of severe new vessels on the disc in proliferative diabetic retinopathy after a single intravitreal injection of pegaptanib. Acta Ophthalmol 87 (2009), 683–684.
68. 68 Avery, R.L., Pearlman, J., Pieramici, D.J., et al. Intravitreal bevacizumab (Avastin) in the treatment of proliferative diabetic retinopathy. Ophthalmology 113 (2006), 1695.e1–1695.e15.
69. 69 Erdol, H., Turk, A., Akyol, N., Imamoglu, H.I., The results of intravitreal bevacizumab injections for persistent neovascularizations in proliferative diabetic retinopathy after photocoagulation therapy. Retina 30 (2010), 570–577.
70. 70 Mirshahi, A., Roohipoor, R., Lashay, A., et al. Bevacizumab-augmented retinal laser photocoagulation in proliferative diabetic retinopathy: a randomized double-masked clinical trial. Eur J Ophthalmol 18 (2008), 263–269.
71. 71 Tonello, M., Costa, R.A., Almeida, F.P., et al. Panretinal photocoagulation versus PRP plus intravitreal bevacizumab for high-risk proliferative diabetic retinopathy (IBeHi study). Acta Ophthalmol 86 (2008), 385–389.
72. 72 Writing Committee for the Diabetic Retinopathy Clinical Research Network, Gross, J.G., Glassman, A.R., et al. Panretinal photocoagulation vs intravitreous ranibizumab for proliferative diabetic retinopathy: a randomized clinical trial. JAMA 314 (2015), 2137–2146.
73. 73 Ip, M.S., Domalpally, A., Hopkins, J.J., et al. Long-term effects of ranibizumab on diabetic retinopathy severity and progression. Arch Ophthalmol 130 (2012), 1145–1152.
74. 74 Bressler, S.B., Qin, H., Melia, M., et al. Exploratory analysis of the effect of intravitreal ranibizumab or triamcinolone on worsening of diabetic retinopathy in a randomized clinical trial. JAMA Ophthalmol 131 (2013), 1033–1040.
75. 75 Campochiaro, P.A., Wykoff, C.C., Shapiro, H., et al. Neutralization of vascular endothelial growth factor slows progression of retinal nonperfusion in patients with diabetic macular edema. Ophthalmology 121 (2014), 1783–1789.
76. 76 Adamis, A.P., Shima, D.T., Tolentino, M.J., et al. Inhibition of vascular endothelial growth factor prevents retinal ischemia-associated iris neovascularization. Arch Ophthalmol 114 (1996), 66–71.
77. 77 Campochiaro, P.A., Hafiz, G., Shah, S.M., et al. Ranibizumab for macular edema due to retinal vein occlusions: implication of VEGF as a critical stimulator. Mol Ther 16 (2008), 791–799.
78. 78 Campochiaro, P.A., Heier, J.S., Feiner, L., et al. Ranibizumab for macular edema following branch retinal vein occlusion: 6-month primary endpoint results of a phase III study. Ophthalmology 117 (2010), 1102–1112.
79. 79 Brown, D.M., Campochiaro, P.A., Singh, R.P., et al. Efficacy and safety of ranibizumab in the treatment of macular edema secondary to central retinal vein occlusion: 6-month results of the phase III CRUISE study. Ophthalmology 117 (2010), 1124–1133.
80. 80 Campochiaro, P.A., Brown, D.M., Awh, C.C., et al. Sustained benefits from ranibizumab for macular edema following central retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology 118 (2011), 2041–2049.
81. 81 Brown, D.M., Campochiaro, P.A., Bhisitkul, R.B., et al. Sustained benefits from ranibizumab for macular edema following branch retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology 118 (2011), 1594–1602.
82. 82 Boyer, D., Heier, J., Brown, D.M., et al. Vascular endothelial growth factor trap-eye for macular edema secondary to central retinal vein occlusion. Six-month results of the phase 3 COPERNICUS study. Ophthalmology 119 (2012), 1024–1032.
83. 83 Brown, D.M., Heier, J.S., Clark, L.W., et al. Intravitreal aflibercept injection for macular edema secondary to central retinal vein occlusion: 1-year results from the phase 3 COPERNICUS study. Am J Ophthalmol 155 (2013), 429–437.
84. 84 Holz, F.G., Roider, J., Ogura, Y., et al. VEGF Trap-Eye for macular oedema secondary to central retinal vein occlusion: 6-month results of the phase III GALILEO study. Br J Ophthalmol 97 (2013), 278–284.
85. 85 Korobelnik, J.F., Holz, F.G., Roider, J., et al. Intravitreal aflibercept injection for macular edema resulting from central retinal vein occlusion. One-year results of the phase 3 GALILEO study. Ophthalmology 121 (2014), 202–208.
86. 86 Epstein, D.L., Algvere, P.V., von Wendt, G., et al. Bevacizumab for macular edema in central retinal vein occlusion: a prospective, randomized, double-masked clinical study. Ophthalmology 119 (2012), 1184–1189.
87. 87 Sophie, R., Hafiz, G., Scott, A., et al. Long term outcomes in ranibizumab-treated patients with retinal vein occlusion: the role of progression of retinal nonperfusion. Am J Ophthalmol 156 (2013), 693–705.
88. 88 Campochiaro, P.A., Sophie, R., Pearlman, J., et al. Long-term outcomes in patients with retinal vein occlusion treated with ranibizumab: The RETAIN Study. Ophthalmology 121 (2014), 209–219.
89. 89 Campochiaro, P.A., Bhistikul, R.B., Shapiro, H., Rubio, R.G., Vascular endothelial growth factor promotes progressive retinal nonperfusion in patients with retinal vein occlusion. Ophthalmology 120 (2013), 795–802.
90. 90 Mir, T.A., Kherani, S., Hafiz, G., et al. Changes in retinal nonperfusion associated with suppression of vascular endothelial growth factor in retinal vein occlusion. Ophthalmology 123 (2016), 625–634.
91. 91 Avery, R.L., Castellarin, A.A., Steinle, N.C., et al. Systemic pharmacokinetics following intravitreal injections of ranibizumab, bevacizumab or aflibercept in patients with neovascular AMD. Br J Ophthalmol 98 (2014), 1543–1546.
92. 92 Hanhart, J., Tiosano, L., Averbukh, E., et al. Fellow eye effect of unilateral intravitreal bevacizumab injection in eyes with diabetic macular edema. Eye (Lond) 28 (2014), 646–653.
93. 93 Virgili, G., Parravano, M., Menchini, F., Evans, J.R., Anti-vascular endothelial growth factor for diabetic macular oedema. Cochrane Database Syst Rev, 10, 2014, CD007419.