Critical appraisal of ranibizumab in the treatment of diabetic macular edema

Clinical Ophthalmology

Volumn 7, Issue , 2013, Pages 1257-1267

  Stewart, Michael W ^a  

^a MAYO CLINIC COLLEGE OF MEDICINE   (United States)

Author keywords

Afibercept; Bevacizumab; Diabetic macular edema; Diabetic retinopathy; Ranibizumab; Vascular endothelial growth factor

Indexed keywords

AFLIBERCEPT; BEVACIZUMAB; GROWTH FACTOR; PEGAPTANIB; RANIBIZUMAB; TRIAMCINOLONE ACETONIDE; VASCULOTROPIN;

ARTICLE; BLINDNESS; BLOOD RETINA BARRIER; CATARACT; DIABETIC MACULAR EDEMA; DIABETIC RETINOPATHY; DRUG APPROVAL; DRUG COST; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG MEGADOSE; ENDOPHTHALMITIS; EYE PAIN; FOOD AND DRUG ADMINISTRATION; HUMAN; HYPERTENSION; INTRAOCULAR PRESSURE; LASER COAGULATION; LOW DRUG DOSE; MEDIATOR; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); RETINA MACULA AGE RELATED DEGENERATION; SIDE EFFECT; UNITED STATES; VISUAL ACUITY;

EID: 84879491018     PISSN: 11775467     EISSN: 11775483     Source Type: Journal    
DOI: 10.2147/OPTH.S36443     Document Type: Article

References (82)

1. Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for age-related macular degeneration. N Engl J Med. 2006;355:1419-1431.
2. Brown DM, Kaiser PK, Michels M, et al. Ranibizumab versus verte-porfn for neovascular age-related macular degeneration. N Engl J Med. 2006;334:1432-1444.
3. Diabetic Retinopathy Clinical Research Network; Elman MJ, Bressler NM, Qin H, et al. Expanded 2-year follow-up of ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology. 2011;118:609-614.
4. Brown DM, Campochiaro PA, Singh RP; and CRUISE investigators. Ranibizumab for macular edema following central retinal vein occlusion. Six month primary end point results of a phase III study. Ophthalmology. 2010;117:1124-1133.
5. Brown DM, Campochiaro PA, Bhisitful RB, et al. Sustained benefts from ranibizumab for macular edema following branch retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology. 2011;118:1594-1602.
6. Aiello L P, Avery RI, Arrigg PG, et al. Vascular endothelial growth factor in ocular fuid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480-1487.
7. Funatsu H, Yamashita H, Ikeda T, Nakanishi Y, Kitano S, Hori S. Angiotensin II and vascular endothelial growth factor in the vitreous fuid of patients with diabetic macular edema and other retinal disorders. Am J Ophthalmol. 2002;133:537-543.
8. Heier JS, Brown DM, Chong V, et al. Intravitreal afibercept (VEGF Trap-Eye) in wet age-related macular degeneration. Ophthalmology. 2012;119:2537-2548.
9. American Academy of Ophthalmology Retina/Vitreous Panel. Preferred Practice Pattern Guidelines. Diabetic Retinopathy. San Francisco, CA: American Academy of Ophthalmology;2008;4. Available at: http//one.aao.org/CE/PracticeGuidelines/PPP.aspx. Accessed April 9, 2012.
10. International Diabetes Federation. IDF Diabetes Atlas. 4th ed. Brussels, Belgium: International Diabetes Federation Executive Offce; 2009. Available from: http://www.diabetesatlas.org/. Accessed April 20, 2011.
11. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care. 1998;21:1414-1431.
12. Nguyen QD, Shah SM, Heier JS, et al. Primary end point (six months) results of the ranibizumab for edema of the macula in diabetes (READ-2) study. Ophthalmology. 2009;116:2175-2181.
13. Klein R, Klein BE, Moss SE, et al. The Wisconsin Epidemiologic study of diabetic retinopathy. I V. Diabetic macular edema. Ophthalmology. 1984;91:1464-1474.
14. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin Epidemiologic study of diabetic retinopathy. II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol. 1984;102:520-526.
15. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin Epidemiologic study of diabetic retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol. 1984;102:527-532.
16. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329:977-986.
17. Photocoagulation for diabetic macular edema. Early Treatment Diabetic Retinopathy Study report number 1. Early Treatment Diabetic Retinopathy Study Research Group. Arch Ophthalmol. 1985;103: 1796-1806.
18. Schatz H, Madeira D, McDonald HR, Johnson RN. Progressive enlargement of laser scars following grid laser photocoagulation for diffuse diabetic macular edema. Arch Ophthalmol. 1991;109:1549-1551.
19. Stewart M W. Corticosteroid use for diabetic macular edema: old fad or new trend? Curr Diab Rep. 2012;12:364-375.
20. Mitchell P, Bandello F, Schmidt-Erfurth U, et al. The RESTORE study. Ranibizumab monotherapy or combined with laser versus laser monotherapy for diabetic macular edema. Ophthalmology. 2011;118: 615-625.
21. Nguyen QD, Brown DM, Marcus DM, et al; on behalf of the RISE and RIDE Research Group. Ranibizumab for diabetic macular edema: results from 2 phase III randomized trials: RISE and RIDE. Ophthalmology. 2012;119:789-801.
22. Arevalo JF, Sanchez JG, Wu L, et al. Primary intravitreal bevacizumab for diffuse diabetic macular edema. The Pan-American Collaborative Retina Study Group at 24 months. Ophthalmology. 2009;116:1488-1497.
23. Michaelides M, Kaines A, Hamilton RD, et al. A prospective randomized trial of intravitreal bevacizumab or laser therapy in the management of diabetic macular edema (BOLT study). Ophthalmology. 2010;117: 1078-1086.
24. Sultan MB, Zhou D, Loftus J, et al; for the Macugen 1013 Study Group. A phase 2/3, multicenter, randomized, double-masked, 2-year trial of pegaptanib sodium for the treatment of diabetic macular edema. Ophthalmolog y. 2011;118:1107-1118.
25. Do DV, Schmidt-Erfurth U, Gonzalez VH, et al. The DA VINCI Study: phase 2 primary results of VEGF Trap-Eye in patients with diabetic macular edema. Ophthalmology. 2011;118:1819-1826.
26. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-820.
27. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol. 2002;64:993-998.
28. Maxwell PH, Ratcliffe PJ. Oxygen sensors and angiogenesis. Semin Cell Dev Biol. 2002;13:29-37.
29. Vinores SA, Youssri AI, Luna JD, et al. Upregulation of vascular endothelial growth factor in ischemic and non-ischemic human and experimental retinal disease. Histol Histopathol. 1997;12:99-109.
30. Caldwell RB, Bartoli M, Behzadian MA, et al. Vascular endothelial growth factor and diabetic retinopathy: pathophysiological mechanisms and treatment perspectives. Diabetes Metab Res Rev. 2003;19:442-455.
31. Ejaz S, Chekarova I, Ejaz A, et al. Importance of pericytes and mechanisms of pericyte loss during diabetes retinopathy. Diabetes Obes Metab. 2008;10:53-63.
32. Stewart M W. The expanding role of vascular endothelial growth factor inhibitors in ophthalmology. Mayo Clin Proc. 2012;87:77-88.
33. Lu M, Perez VL, Ma N, et al. VEGF increases retinal vascular ICAM-1 expression in vivo. Invest Ophthalmol Vis Sci. 1999;40:1808-1812.
34. Barleon B, Sozzani S, Zhou D, et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor ft-1. Blood. 1996;87:3336-3343.
35. Miyamoto K, Khosrof S, Bursell, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A. 1999;96:10836-10841.
36. Joussen AM, Murata T, Tsujikawa A, et al. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158:147-152.
37. Michaelson IC. The mode of development of the vascular system of the retina with some observations on its signifcance for certain retinal disorders. Trans Ophthalmol Soc U K. 1948;68:1625-1710.
38. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak H F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fuid. Science. 1983;12:983-985.
39. Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specifc for vascular endothelial cells. Biochem Biophys Res Commun. 1989;161:851-858.
40. Connolly DT, Heuvelman DM, Nelson R, et al. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest. 1989;84:1470-1478.
41. Stewart M W. Afibercept (VEGF-TRAP): the next anti-VEGF drug. Infamm Allergy Drug Targets. 2011;10:497-508.
42. Ferrara N, Gerber H-P, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676.
43. Gerber H P, McMurtrey A, Kowalski J, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphotidylinosi-tol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/ KDR activation. J Biol Chem. 1998;273:30336-30343.
44. Ferrara N, Hillan KJ, Gerber H-P, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov. 2004;3:391-400.
45. Ferrara N, Damico L, Shams N, Lowman H, Kim R. Development of ranibizumab, an anti-vascular endothelial growth factor antigen binding fragment, as therapy for neovascular age-related macular degeneration. Retina. 2006;26:859-870.
46. Papadopoulos N, Martin J, Ruan Q, et al. Binding and neutralization of vascular endothelial growth factor (VEGF) and related ligands by VEGF Trap, ranibizumab and bevacizumab. Angiogenesis. 2012;15: 171-185.
47. Bakri SJ, Snyder MR, Reid JM, Pulido JS, Ezzat MK, Singh RJ. Pharmacokinetics of intravitreal ranibizumab (Lucentis). Ophthalmology. 2007;114:2179-2182.
48. Christofordis JB, Carlton MM, Knopp M V, Hinkle GH. Pet/CT imaging of I-124-radiolabeled bevacizumab and ranibizumab after intravitreal injection in a rabbit model. Invest Ophthalmol Vis Sci. 2011;52:5899-5903.
49. 125I-labeled full-length and Fab antibodies in rhesus monkeys following intravitreal administration. Toxicol Pathol. 1999;27:536-544.
50. Gaudreault J, Fei D, Rusit J, Suboc P, Shiu V. Preclinical pharmacokinet-ics of ranibizumab (rhuFabV2) after a single intravitreal administration. Invest Ophthalmol Vis Sci. 2005;46:726-733.
51. Krohne TU, Liu Z, Holz FG, Meyer CH. Intraocular pharmacokinetics of ranibizumab following a single intravitreal injection in humans. Am J Ophthalmol. 2012;154:682-686.
52. Meyer CH, Krohne TU, Holz FG. Intraocular pharmacokinetics after a single intravitreal injection of 1.5 mg versus 3.0 mg of bevacizumab in humans. Retina. 2011;31:1877-1884.
53. Xu L, Lu T, Tuomi L, et al. Pharmacokinetics of ranibizumab in patients with neovascular age-related macular degeneration: a population approach. Invest Ophthalmol Vis Sci. 2013;54:1616-1624.
54. Chakravarthy U, Harding S P, Rogers CA, et al. Ranibizumab versus bevacizumab to treat neovascular age-related macular degeneration: one-year fndings from the IVAN randomized trial. Ophthalmology. 2012;119:1399-1411.
55. Regillo CD, Brown DM, Abraham P, et al. Randomized, double-masked, sham-controlled trial of ranibizumab for neovascular age-related macular degeneration: PIER study year 1. Am J Ophthalmol. 2008;145:239-248.
56. Schmidt-Erfurth U, Eldem B, Guymer R, et al; for the EXCITE Study Group. Effcacy and safety of monthly versus quarterly ranibizumab treatment in neovascular age-related macular degeneration: the EXCITE study. Ophthalmology. 2011;118:831-839.
57. Gilbert RE, Vranes D, Berka JL, et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol. 1998;145: 574-584.
58. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 1995;108:2369-2379.
59. Qaum T, Xu Q, Joussen AM, et al. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest Ophthalmol Vis Sci. 2001;42: 2408-2413.
60. Tolentino MJ, McLeod DS, Taomoto M, Otsuji T, Adamis A P, Lutty GA. Pathologic features of vascular endothelial growth factor-induced retinopathy in the nonhuman primate. Am J Ophthalmol. 2002;133:373-385.
61. Funatsu H, Yamashita H, Noma H, Mimura T, Yamashita T, Hori S. Increased levels of vascular endothelial growth factor and interleukin-6 in the aqueous humor of diabetics with macular edema. Am J Ophthalmol. 2002;133:70-77.
62. Funatsu H, Yamashita H, Ikeda T, Mimura T, Eguchi S, Hori S. Vitreous levels of interleukin-6 and vascular endothelial growth factor are related to diabetic macular edema. Ophthalmology. 2003;110:1690-1696.
63. Campochiaro PA, Choy DF, Do DV, et al. Monitoring ocular drug therapy by analysis of aqueous samples. Ophthalmology. 2009;116:2158-2164.
64. Nguyen QD, Shah SM, Van Anden E, Sung JU, Vitale S, Campochiaro PA. Supplemental oxygen improves diabetic macular edema: a pilot study. Invest Ophthalmol Vis Sci. 2004;45:617-624.
65. Macugen Diabetic Retinopathy Study Group. A phase II randomized double-masked trial of pegaptanib, an anti-vascular endothelial growth factor aptamer, for diabetic macular edema. Ophthalmology. 2005;112: 1747-1757.
66. Nguyen QD, Tatlipinar S, Shah SM, et al. Vascular endothelial growth factor is critical stimulus for diabetic macular edema. Am J Ophthalmol. 2006;142:961-969.
67. Chun DW, Heier JS, Topping TM, Duker JS, Bankert JM. A pilot study of multiple intravitreal injections of ranibizumab in patients with center-involving clinically signifcant diabetic macular edema. Ophthalmology. 2006;113:1706-1712.
68. Nguyen QD, Shah SM, Khwaja AA, et al. Two-year outcomes of the ranibizumab for edema of the macula in diabetes (READ-2) study. Ophthalmology. 2010;117:2146-2151.
69. Do D V, Nguyen QD, Khwaja AA, et al; for the READ-2 Study Group. Ranibizumab for edema of the macula in diabetes study; 3-year outcomes and the need for prolonged frequent treatment. JAMA Ophthalmol. 2013;131:139-145.
70. Busbee BG, Ho AC, Brown DM, et al; HARBOR Study Group. Twelve-month effcacy and safety of 0.5 mg or 2 mg ranibizumab in patients with subfoveal neovascular age-related macular degeneration. Ophthalmology. January 23, 2013. [Epub ahead of print.]
71. Do DV, Campochiaro PA, Boyer DS, et al; Read 3 Research Group. Six-month and one-year interim results of the READ 3 study: ranibi-zumab for edema of the macula in diabetes. Abstract presented at the 2012 annual meeting of the Association for Research in Vision and Ophthalmology, May 6-9, 2012, Fort Lauderdale, FL.
72. Massin P, Bandello F, Garweg JG, et al. Safety and effcacy of ranibi-zumab in diabetic macular edema (RESOLVE study): a 12-month, randomized, controlled, double-masked, multicenter phase II study. Diabetes Care. 2010;33:2399-2405.
73. Diabetic Retinopathy Clinical Research Network; Elman MJ, Aiello L P, Beck RW, et al. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmolog y. 2010;117:1064-1077.
74. Manousaridis K, Talks J. Macular ischaemia: a contraindication for anti-VEGF treatment in retinal vascular disease? Br J Ophthalmol. 2012;96:179-184.
75. Soheilian M, Ramezani A, Obudi A, et al. Randomized trial of intravit-real bevacizumab alone or combined with triamcinolone versus macular photocoagulation in diabetic macular edema. Ophthalmology. 2009;116: 1142-1150.
76. Diabetic Retinopathy Clinical Research Network. A phase II randomized clinical trial of intravitreal bevacizumab for diabetic macular edema. Ophthalmolog y. 2007;114:1860-1867.
77. Solaiman KA, Diab MM, Abo-Elenin M. Intravitreal bevacizumab and/or macular photocoagulation as a primary treatment for diffuse diabetic macular edema. Retina. 2011;30:1638-1645.
78. Lam DS, Lai T Y, Lee V Y, et al. Effcacy of 1.25 mg versus 2.5 mg intravitreal bevacizumab for diabetic macular edema: six-month results of a randomized controlled trial. Retina. 2009;29:292-299.
79. Clinicaltrials.gov. Diabetic Retinopathy Clinical Research Network. Comparative effectiveness study of intravitreal afibercept, bevacizumab, and ranibizumab for DME.ClinicalTrial.gov Identifer NCT01627249. Available from: http://www.clinicaltrials.gov/ct2/show/NCT01627249. Accessed October 15, 2012.
80. Brown DM, Michels M, Kaiser PK, et al. ANCHOR Study Group. Ranibizumab versus verteporfn photodynamic therapy for neovascular age-related macular degeneration: two-year results of the ANCHOR Study. Ophthalmology. 2009;116:57-65.
81. Schmidt-Erfurth U. Clinical safety of ranibizumab in age-related macular degeneration. Expert Opin Drug Saf. 2010;9:149-165.
82. Smiddy WE. Economic considerations of macular edema therapies. Ophthalmolog y. 2011;118:1827-1833.