Macular ischaemia: A contraindication for anti-VEGF treatment in retinal vascular disease?

British Journal of Ophthalmology

Volumn 96, Issue 2, 2012, Pages 179-184

  Manousaridis, Kleanthis ^a   Talks, James ^a  

^a ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; RANIBIZUMAB; VASCULOTROPIN; VASCULOTROPIN INHIBITOR;

ANGIOGENESIS; CENTRAL RETINA VEIN OCCLUSION; DIABETIC MACULAR EDEMA; DISEASE SEVERITY; DRUG CONTRAINDICATION; EYE ISCHEMIA; FLUORESCENCE ANGIOGRAPHY; HUMAN; ISCHEMIA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); RETINA BLOOD FLOW; RETINA BLOOD VESSEL; RETINA ISCHEMIA; RETINA MACULA EDEMA; RETINA MACULAR ISCHEMIA; REVIEW; SIDE EFFECT; SYSTEMATIC REVIEW; VISUAL ACUITY;

ANGIOGENESIS INHIBITORS; ANTIBODIES, MONOCLONAL, HUMANIZED; CAPILLARY PERMEABILITY; DIABETIC RETINOPATHY; HUMANS; ISCHEMIA; MACULAR EDEMA; RETINAL VEIN OCCLUSION; RETINAL VESSELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VISUAL ACUITY;

EID: 84856057394     PISSN: 00071161     EISSN: 14682079     Source Type: Journal    
DOI: 10.1136/bjophthalmol-2011-301087     Document Type: Review

References (79)

1. Early Treatment Diabetic Retinopathy Study Research Group. Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Ophthalmology 1991;98(Suppl 5):766-85.
2. The Branch Vein Occlusion Study Group. Argon laser photocoagulation for macular edema in branch retinal vein occlusion. Am J Ophthalmol 1984;98:271-82.
3. The Central Retinal Vein Occlusion Study Group. Evaluation of grid pattern photocoagulation for macular edema in central retinal vein occlusion. The Cental Vein Occlusion Study Group M report. Ophthalmology 1995;102:1425-33.
4. Mitchell P, Bandello F, Schmidt-Erfirth U, et al. The RESTORE Study: ranibizumab monotherapy or combined with laser versus laser monotherapy for diabetic macular edema. Ophthalmology 2011;118:615-25.
5. Massin P, Bandello F, Garweg JG, et al. Safety and efficacy of ranibizumab for diabetic macular edema (RESOLVE study): a 12-month, randomized, controlled double masked, multicenter phase II study. Diabetes Care 2010;33:2399-405.
6. Elman MJ, Aiello LP, Beck RW, et al Diabetic Retinopathy Clinical Research Network. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology 2010;117:1064-77.e35.
7. Elman MJ, Bressler NM, Qin H, et al Diabetic Retinopathy Clinical Research Network. Expanded 2-year follow-up of ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology 2011;118:609-14.
8. 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;117:2146-51.
9. Chang LK, Spaide RF, Klancnik JM, et al. Longer term outcomes of a prospective study of intravitreal ranibizumab as a treatment for decreased visual acuity secondary to central retinal vein occlusion. Retina 2011;31:821-8.
10. Wu L, Arevalo JF, Berrocal MH, et al. Comparison of two doses of intravitreal bevacizumab as primary treatment for macular edema secondary to central retinal vein occlusion. Results of the Pan-American Collaborative Retina Study Group at 24 months. Retina 2010;30:1002-11.
11. Campochiaro PA, Heier JS, Feiner L, et al. Ranibizumab for macular edema following branch retinal vein occlusion. Six- month primary end point results of a phase III study. Ophthalmology 2010;117:1102-12.e1.
12. Brown DM, Campochiaro PA, Singh RP, et al. Ranibizumab for macular edema following central retinal vein occlusion. Six- month primary end point results of a phase III study. Ophthalmology 2010;117:1124-33.e1.
13. Brown DM, Campochiaro PA, Bhisitkul RB, et al. Sustained benefits of ranibizumab for macular edema following branch retinal vein occlusion: 12- month outcomes of a phase III study. Ophthalmology 2011;118:1594-602.
14. Campochiaro PA, Brown DM, Awh CC, et al. Sustained benefits from ranibizumab for macular edema following central retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology 2011;118:2041-9.
15. Van der Reis MI, La Heij EC, De Jong Hesse Y, et al. A systematic review of the adverse events of intravitreal anti- vascular endothelial growth factor injections. Retina 2011;31:1449-69.
16. Tolentino M. Systemic and ocular safety of intravitreal anti-VEGF therapies for ocular neovascular disease. Surv Ophthalmol 2011;56:95-113.
17. Salam A, DaCosta J, Sivaprasad S. Anti-vascular endothelial growth factor agents for diabetic maculopathy. Br J Ophthalmol 2010;94:821-6.
18. 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;118:1819-26.
19. Early Treatment Diabetic Retinopathy Study Research Group. Early treatment diabetic retinopathy study report number 1. Photocoagulation for diabetic macular edema. Arch Ophthalmol 1985;103:1796-806.
20. Chung EJ, Roh MI, Kwon OW, et al. Effects of macular ischaemia on the outcome of intravitreal bevacizumab therapy for diabetic macular edema. Retina 2008;28:957-63.
21. Early Treatment Diabetic Retinopathy Study Research Group. Classification of diabetic retinopathy from fluorescein angiograms. ETDRS report 11. Ophthalmology 1991;98(Suppl 5):807-22.
22. Conrath J, Giorgi R, Raccah D, et al. Foveal avascular zone in diabetic retinopathy: quantitative vs qualitative assessment. Eye (Lond) 2005;19:322-6. (Pubitemid 40484828)
23. Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 1989;161:851-8. (Pubitemid 19162712)
24. Kaur C, Sivakumar V, Foulds WS. Early response of neurons and glial cells to hypoxia in the retina. Invest Ophthalmol Vis Sci 2006;47:1126-41.
25. Aiello LP, Northrup JM, Keyt BA, et al. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol 1995;113:1538-44.
26. Funatsu H, Yamashita H, Noma H, et al. Increased levels of vascular endothelial growth factor and interleukin-6 in the aqueous humor of diabetics with macular edema. Am J Ophthalmol 2002;133:70-7. (Pubitemid 34076505)
27. Funk M, Kriechbaum K, Prager F, et al. Intraocular concentrations of growth factors and cytokines in retinal vein occlusion and the effect of therapy with bevacizumab. Invest Ophthalmol Vis Sci 2009;50:1025-32.
28. Tischer E, Mitchell R, Hartman T, et al. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 1991;266:11947-54.
29. Aiello LP, Wong JS. Role of vascular endothelial growth factor in diabetic vascular complications. Kidney Int Suppl 2000;77:S113-19.
30. Esser S, Lampugnani MG, Corada M, et al. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 1998;111:1853-65. (Pubitemid 28370530)
31. Dobrogowska DH, Lossinsky AS, Tarnawski M, et al. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 1998;27:163-73. (Pubitemid 28253067)
32. Kaur C, Foulds WS, Ling EA. Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog Retin Eye Res 2008;27:622-47.
33. Deissler H, Deissler H, Lang S, et al. VEGF- induced effects on proliferation, migration and tight junctions are restored by ranibizumab (Lucentis) in microvascular endothelial cells. Br J Ophthalmol 2008;92:839-43. (Pubitemid 351839580)
34. Nguyen QD, Tatlipinar S, Shah SM, et al. Vascular endothelial growth factor is a critical stimulus for diabetic macular edema. Am J Ophthalmol 2006;142:961-9.
35. Nishijima K, Ng YS, Zhong L, et al. Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 2007;171:53-67. (Pubitemid 47339226)
36. Martinez-Vila E, Sieira PI. Current status and perspectives of neuroprotection in ischemic stroke treatment. Cerebrovasc Dis 2001;11(Suppl 1):60-70.
37. Ran R, Xu H, Lu A, et al. Hypoxia preconditioning in the brain. Dev Neurosci 2005;27:87-92. (Pubitemid 41096213)
38. Takahashi K, Kishi S, Muraoka K, et al. Reperfusion of occluded capillary beds in diabetic retinopathy. Am J Ophthalmol 1998;126:791-7. (Pubitemid 29001628)
39. Muraoka K, Shimizu K. Intraretinal neovascularization in diabetic retinopathy. Ophthalmology 1984;91:1440-6. (Pubitemid 15197013)
40. Clayton JA, Chalothron D, Faber JE. Vascular endothelial growth factor-A specifies formation of native collaterals and regulates collateral growth in ischaemia. Circ Res 2008;103:1027-36.
41. Babiak A, Schumm AM, Wangler C, et al. Coordinated activation of VEGFR-1 and VEGFR-2 is a potent arteriogenic stimulus leading to enhancement of regional perfusion. Cardiovasc Res 2004;61:789-95. (Pubitemid 38249478)
42. Ferrara DC, Koizumi H, Spaide RF. Early bevacizumab treatment of central retinal vein occlusion. Am J Ophthalmol 2007;144:864-71. (Pubitemid 350122344)
43. McLeod D. A chronic grey matter penumbra, lateral microvascular intussusception and venous peduncular avulsion underlie diabetic vitreous haemorrhage. Br J Ophthalmol 2007;91:677-89. (Pubitemid 46716542)
44. Mendrinos E, Mangioris G, Papadopoulou DN, et al. One year results of the effect of intravitreal ranibizumab on the retinal arteriolar diameter in patients with neovascular age- related macular degeneration. Invest Ophthalmol Vis Sci 13 Dec 2011 [Epub ahead of print].
45. Papadopoulou DN, Mendrinos E, Mangioris G, et al. Intravitreal ranibizumab may induce retinal arteriolar vasoconstriction in patients with age-related macular degeneration. Ophthalmology 2009;116:1755-61.
46. Marneros AG, Fan J, Yokoyama Y, et al. Vascular endothelial growth factor expression in the retinal pigment epithelium is essential for choriocapillaris development and visual function. Am J Pathol 2005;167:1451-9. (Pubitemid 41541430)
47. Peters S, Heiduschka P, Julien S, et al. Ultrastructural findings in the primate eye after intravitreal injection of bevacizumab. Am J Ophthalmol 2007;143:995-1002.
48. Funk M, Schidinger G, Maar N, et al. Angiogenic and inflammatory markers in the intraocular fluid of eyes with diabetic macular edema and influence of therapy with bevacizumab. Retina 2010;30:1412-19.
49. Michaelides M, Fraser-Bell S, Hamilton R, et al. Macular perfusion determined by fundus fluorescein angiography at the 4-month time point in a prospective randomized trial of intravitreal bevacizumab or laser therapy in the management of diabetic macular edema (BOLT Study): report 1. Retina 2010;30:781-6.
50. 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). Report 2: 12 month data. Ophthalmology 2010;117:1078-86.e2.
51. Channa R, Smith M, Campochiaro PA. Treatment of macular edema due to retinal vein occlusions. Clin Ophthalmol 2011;5:705-13.
52. Campochiaro PA, Hafiz G, Channa R, et al. Antagonism of vascular endothelial growth factor for macular edema caused by retinal vein occlusion: two- year outcomes. Ophthalmology 2010;117:2387-94.e1-5.
53. Early Treatment Diabetic Retinopathy Study Research Group. Focal photocoagulation treatment of diabetic macular edema. Relationship of treatment effect to fluorescein angiographic and other retinal characteristics at baseline: ETDRS Report 19. Arch Ophthalmol 1995;113:1144-55.
54. Arend O, Wolf S, Jung F, et al. Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 1991;75:514-18.
55. Mansour AM, Schachat A, Bodiford G, et al. Foveal avascular zone in diabetes mellitus. Retina 1993;13:125-8. (Pubitemid 23177776)
56. Bonini-Filho M, Costa RA, Calucci D, et al. Intravitreal bevacizumab for diabetic macular edema associated with severe capillary loss: one-year results of a pilot study. Am J Ophthalmol 2009;147:1022-30.
57. Kook D, Wolf A, Kreutzer T, et al. Long- term effect of intravitreal bevacizumab (avastin) in patients with chronic diffuse diabetic macular edema. Retina 2008;28:1053-60.
58. Spaide RF. Peripheral areas of nonperfusion in treated central retinal vein occlusion as imaged by wide-field fluorescein angiography. Retina 2011;31:829-37.
59. Terui T, Kondo M, Sugita T, et al. Changes in areas of capillary nonperfusion after intravitreal injection of bevacizumab in eyes with branch retinal vein occlusion. Retina 2011;31:1068-74.
60. Chung EJ, Hong YT, Lee SC, et al. Prognostic factors for visual outcome after intravitreal bevacizumab for macular edema due to branch retinal vein occlusion. Graefes Arch Clin Exp Ophthalmol 2008;246:1241-7.
61. Costa RA, Jorge R, Calucci D, et al. Intravitreal bevacizumab (avastin) for central and hemicentral retinal vein occlusions: IBeVO study. Retina 2007;27:141-9.
62. Neubaurer AS, Kook D, Haritoglou C, et al. Bevacizumab and retinal ischaemia. Ophthalmology 2007;114:2096.
63. Lee SJ, Koh HJ. Enlargement of the foveal avascular zone in diabetic retinopathy after adjunctive intravitreal bevacizumab (Avastin) with pars plana Vitrectomy. J Ocul Pharmacol Ther 2009;25:173-4.
64. Sabet-Peyman EJ, Heussen FM, Thorne JE, et al. Progression of macular ischaemia following intravitreal bevacizumab. Ophthalmic Surg Lasers Imaging 2009;40:316-18.
65. Kim KS, Chang HR, Song S. Ischaemic change after intravitreal bevacizumab (avastin) injection for macular edema secondary to non-ischaemic central retinal vein occlusion. Acta Ophthalmol 2008;86:925-7.
66. Yokoyama K, Choshi T, Kimoto K, et al. Retinal circulatory disturbances following intracameral injection of bevacizumab for neovascular glaucoma. Acta Ophthalmol 2008;86:927-8.
67. Kim RN, Chin HS. Progression of impending central retinal vein occlusion to the ischemic variant following intravitreal bevacizumab. Korean J Ophthalmol 2010;24:179-81.
68. Chen E, Hsu J, Park CH. Acute visual acuity loss following intravitreal bevacizumab for diabetic macular edema. Ophthalmic Surg Lasers Imaging 2009;40:68-70.
69. Goel N, Kumar V, Ghosh B. Ischemic maculopathy following intravitreal bevacizumab for refractory diabetic macular edema. Int Ophthalmol 2011;31:39-42.
70. Shimura M, Yasuda K. Macular ischaemia after intravitreal bevacizumab injection in patients with central retinal vein occlusion and a history of diabetes and vascular disease. Br J Ophthalmol 2010;94:381-3.
71. Ganssauge M, Wilhelm H, Bartz-Schmidt KU, et al. Non-arteriitic anterior ischemic optic neuropathy (NA-AION) after intravitreal injection of bevacizumab (Avastin) for treatment of angioid streaks in pseudoxanthoma elasticum. Graefes Arch Clin Exp Ophthalmol 2009;247:1707-10.
72. Kofoed PK, Munch IC, Larsen M. Profound retinal ischaemia after ranibizumab administration in an eye with ocular ischaemic syndrome. Acta Ophthalmol 2010;88:808-10.
73. Huang ZL, Lin KH, Lee YC, et al. Acute vision loss after intravitreal injection of bevacizumab (avastin) associated with ocular ischemic syndrome. Ophthalmologica 2010;224:86-9.
74. Battaglia Parodi M, Iacono P, Cascavilla ML, et al. Sequential anterior ischemic optic neuropathy and central retinal artery and vein occlusion after ranibizumab for diabetic macular edema. Eur J Ophthalmol 2010;20:1076-8.
75. Huang JY, Ozaki H, Hayashi H, et al. Anterior ischemic optic neuropathy following intravitreal bevacizumab. Jpn J Ophthalmol 2010;54:252-4.
76. Hosseini H, Razeghinejad MR. Anterior ischemic optic neuropathy after intravitreal injection of bevacizumab. J Neuroophthalmol 2009;29:160-1.
77. von Hanno T, Kinge B, Fossen K. Retinal artery occlusion after intravitreal anti-VEGF therapy. Acta Ophthalmol 2010;88:263-6.
78. Furino C, Boscia F, Cardascia N, et al. Hemorrhagic macular infarction after intravitreal bevacizumab for central retinal vein occlusion. Ophthalmic Surg Lasers Imaging 2010;9:1-2.
79. Mansour AM, Bynoe LA, Welch JC, et al. Retinal vascular events after intravitreal bevacizumab. Acta Ophthalmol 2010;88:730-5.