V.Yu. Evgrafov1, G.R. Kudasheva2
1,2 Pirogov Russian National Research Medical University (Moscow, Russia)
Review of the literature of international clinical guidelines, randomized clinical trials with a varying level of evidence, articles and publications. Diabetic retinopathy have been taking a leading position among retinal disorders, leading to a persistent and significant decrease in visual functions. The base of the disease is a retinal vascular microangiopathy, which induces a tissue ischemia and excessive production of vascular endothelial growth factors. The main method of treatment for this pathology is a laser photocoagulation. However, it is not always possible to perform appropriate laser photocoagulation, by that limiting its efficacy (cases of hard cataract and hemophthalmos). In addition, this type of treatment might have a number of serious complications, such as macular oedema, recurrent vitreous hemorrhages, the occurrence of fibrosis, atrophic changes in the retina, which leads to a decline in visual acuity and contrast sensitivity, worsening the visual field.
Over the past 10 years, vascular endothelial growth factor inhibitors have been introduced into clinical practice, and showed their benefits in the treatment of disorders leading to a pathological angiogenesis. But due to the limited number of systematic observations, assessing the impact of these drugs, is necessary to investigate their efficacy and safety in patients with proliferative diabetic retinopathy, in order to develop indications for their use.
Evgrafov V.Yu., Kudasheva G.R. The use of vascular endothelial growth factor inhibitors in patients with proliferative diabetic retinopathy. Technologies of Living Systems. 2022. V. 19. № 1. Р. 45-55. DOI: https://doi.org/10.18127/j20700997-202201-06 (In Russian)
- Shadrichev F.E., Shklyarov E.B., Grigoryeva N.N. Ispolzovaniye anti-VEGF terapii v lechenii diabeticheskogo makulyarnogo oteka. Oftalmologicheskiye vedomosti. 2011. T. 4(1). S. 83–92. (in Russian).
- Budzinskaya M.V., Petrachkov D.V., Savochkina O.A., Arzhukhanov D.D. Klassifikatsiya diabeticheskoy retinopatii. Vestnik oftalmologii. 2019. T. 135 (5). S. 272–277. (in Russian).
- Diabetic retinopathy. Medscape ophthalmology; last update May 22. 2019. https://emedicine.medscape.com/article/1225122-overview#a1 (in Russian).
- Poveshchenko A.F.,Konenkov V.I. Mekhanizmy i factory angiogeneza. Uspekhifiziol. nauk. 2010. T. 41(2). S. 68–89. (in Russian).
- Konenkov V.I., Klimontov V.V., Chernykh V.V., Tyan N.V. Preparaty anti-VEGF v lechenii diabeticheskogo makulyarnogo oteka. Sakharnyy diabet. 2013. T. 4. S. 78–84. (in Russian).
- Balashevich L.I., Brezheskiy V.V., Izmaylov A.S. Glaznyye proyavleniya diabeta. SPb.: Izdatelskiy dom SPbMAPO. 2004. 453 s. (in Russian).
- Lipatov D.V., Chistyakov T.A. Medikamentoznoye lazernoye i khirurgicheskoye lecheniye v torichnoy neovaskulyarnoy glaukomy u patsiyentov s sakharnym diabetom. Glaukoma. 2013. T. 2. S. 62–69.(in Russian).
- The Diabetic Retinopathy Study Research Group. Indications for photocoagulation treatment of diabetic retinopathy. Diabetic Retinopathy Study Report. Int. Ophthalmol Clin. 1987. V. 27. P. 239–253. DOI: 10.1097/00004397-198702740-00004
- Rosenstein R.B. Long-term stability and visual outcome after favorable initial response of proliferative diabetic retinopathy to panretinal photocoagulation. Ophthalmology. 1991. V. 98. P. 1575–1579. DOI: 10.1016/s0161-6420(91)32085-2
- Basic and Clinical Science Course, 12th Edition. Retina and vitreous. American Academy of Ophthalmology publishing house, San Francisco 2016-2017. P. 96–97.
- International Council of Ophthalmology Guidelines for Diabetic Eye Care. 2017. P. 9–10. http://www.icoph.org/enhancing_eyecare/diabetic_eyecare.html
- Gentile R.C., Stegman Z., Liebmann J.M., Dayan A.R., Tello C., Walsh J.B. et al. Risk factors for ciliochoroidal effusion after panretinal photocoagulation. Ophthalmology. 1996. V. 103. P. 827–832. DOI: 10.1016/s0161-6420(96)30608-8
- McDonald H.R., Schatz H. Macular edema following panretinal photocoagulation. Retina. 1985. V. 5. P. 5–10. DOI: 10.1097/00006982-198500510-00002
- Jardeleza M.S., Miller J.W. Review of anti-VEGF therapy in proliferative diabetic retinopathy. Semin Ophthalmol. 2009. V. 24. P. 87–92. DOI: 10.1080/08820530902800330
- Lipatov D.V.,Lyshkanets O.I. Intravitrealnaya terapiya diabeticheskogo makulyarnogo oteka v Rossiyskoy Federatsii: sovremennoyesostoyaniye problemy. Vestnik oftalmologii. 2019. T. 135 (4). S. 128–140. (in Russian).
- Neroyev V.V.,Sarygina O.I.,Levkina O.A. Rol sosudistogo endotelialnogo faktora rosta v patogeneze diabeticheskoy retinopatii. Vestnik oftalmologii. 2009. T. 2. S. 58–60. (in Russian).
- Karpilova M.A., Durzhinskaya M.Kh. Preparaty anti-VEGF vlechenii neovaskulyarnoy glaukomy. Vestnik oftalmologii. 2019. T. 135 (5). S. 299–304. (in Russian).
- Spaide R.F., Fisher Y.L. Intravitreal bevacizumab (Avastin) treatment of proliferative diabetic retinopathy complicated by vitreous hemorrhage. Retina. 2006. V. 26. P. 275–278.DOI: 10.1097/00006982-200603000-00004
- Avery R.L. Regression of retinal and iris neovascularization after intravitreal bevacizumab (Avastin) treatment. Retina. 2006. V. 26. P. 352–354.DOI: 10.1016/j.ophtha.2006.05.064
- Thew M. Rapid resolution of severe retinal neovascularisation in proliferative diabetic retinopathy following adjunctive intravitreal bevacizumab (Avastin). Clin. Exp. Optometry. 2009. V. 92. P. 34–37.DOI: 10.1111/j.1444-0938.2008.00295.x
- Sun J.K. The Diabetic Retinopathy Study Research Group. Rationale and Clinical Application of the DRCR.net Anti-VEGF Treatment Algorithm for Proliferative Diabetic Retinopathy. Ophthalmology. 2019. P. 87–95. DOI: https://doi.org/10.1016/j.ophtha.2018.08.001
- D’Amore P.A. Vascular endothelial cell growth factor-A: not just for endothelial cells anymore. Am. J. Pathol. 2007. V. 171. P. 14–18. DOI: 10.2353/ajpath.2007.070385
- Guidelines for the Management of Diabetic Macular Edema by the European Society of Retina Specialists (EURETINA). Ophthalmologica. 2017. V. 237. P. 196–208.
- Matsuyama K., Ogata N., Matsuoka M., Wada M., Takahashi K., Nishimura T. Plasma levels of vascular endothelial growth factor and pigment epithelium-derived factor before and after intravitreal injection of bevacizumab. Br. J. Ophthalmol. 2010. V. 94. P. 1215–1218. DOI: 10.1136/bjo.2008.156810
- Zehetner C., Kirchmair R., Huber S., Kralinger M.T., Kieselbach G.F. Plasma levels of vascular endothelial growth factor before and after intravitreal injection of bevacizumab, ranibizumab and pegaptanib in patients with age related macular degeneration, and in patients with diabetic macular oedema. Br. J. Ophthalmol. 2013. V. 97. P. 454–459. DOI: 10.1136/bjophthalmol-2012-302451
- Aiello L.P., Avery R.L., Arrigg P.G., Keyt B.A., Jampel H.D., Shah S.T., Pasquale L.R., ThiemeH.,Iwamoto M.A., Park J.E., et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N. Engl. J. Med. 1994. V. 331. P. 1480–1487. DOI: 10.1056/NEJM199412013312203
- Chen G., Li W., Tzekov R., Jiang F., Mao S., Tong Y. Ranibizumab monotherapy or combined with laser versus laser monotherapy for diabetic macular edema: a meta-analysis of randomized controlled trials. PLoS One. 2014. V. 9. P. e115797. DOI.org/10.1371/journal.pone.0115797
- Brown D.M., Nguyen Q.D., Marcus D.M., Boyer D.S., Patel S., Feiner L., Schlottmann P.G., Rundle A.C., Zhang J., Rubio R.G., Adamis A.P., Ehrlich J.S., Hopkins J.J. Long-term outcomes of ranibizumab therapy for diabetic macular edema: the 36-month results from two phase III trials: RISE and RIDE. Ophthalmology. 2013. V. 120. P. 2013–2022.DOI: 10.1016/j.ophtha.2013.02.034
- Elman M.J., Aiello L.P., Beck R.W., Bressler N.M., Bressler S.B., Edwards A.R., Ferris F.L., 3rd, Friedman S.M., Glassman A.R., Miller K.M., Scott I.U., Stockdale C.R., Sun J.K. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology. 2010. V. 117. P. 1064–1077.e1035. DOI: 10.1016/j.ophtha.2010.02.031
- Beaulieu T. Panretinal Photocoagulation Versus Ranibizumab for Proliferative Diabetic retinopathy: Patient-Centered Outcomes From a randomized Clinical Trial. Aug. 2016. DOI: 10.1016/j.ajo.2016.08.008
- FDA, Professional Drug Information for Eylea. https://www.accessdata.fda.gov/drugsatfda_docs/label/2011/125387lbl.pdf
- Electronic medicines compendium, United Kingdom. Eylea prescription information. https://www.medicines.org.uk/emc/product/2879/smpc
- FDA Approves Eylea (aflibercept) Injection for Diabetic Retinopathy, PM Regeneron May 13, 2019 – retrieved May 14, 2019. https://investor.regeneron.com/news-releases/news-release-details/fda-approves-eylear-aflibercept-injection-prefilled-syringe/
- McCannel C.A. Meta-analysis of endophthalmitis after intravitreal injection of anti-vascular endothelial growth factor agents. Retina. 2011. V. 31. P. 654–661. DOI: 10.1097/IAE.0b013e31820a67e4
- Scott I.U., Flynn Jr., H.W. Reducing the risk of endophthalmitis following intravitreal injections. Retina. 2007. V. 27. P. 10–12. DOI: 10.1097/IAE.0b013e3180307271
- Fintak D.R., Shah G.K., Kj. Blinder, Regillo C.D., Pollack J., Heier J.S. et al. Incidence of endophthalmitis related to intravitreal injection of bevacizumab and ranibizumab. Retina. 2008. V. 28. P. 1395–1399. DOI: 10.1097/IAE.0b013e3181884fd2
- Pilli S., Kotsolis A., Spaide R.F., Slakter J., Freund K.B., Sorenson J. et al. Endophthalmitis associated with intravitreal anti-vascular endothelial growth factor therapy injections in an office setting. Am. J. Ophthalmol. 2008. V. 145(5). P. 879–882. DOI: 10.1016/j.ajo.2007.12.036
- Doshi R.R., Leng T., Fung A.E. Reducing oral flora contamination of intravitreal injections with face mask or silence. Retina. 2012. V. 32(3). P. 473–476. DOI: 10.1097/IAE.0B013E31822C2958
- Wen J.C., McCannel C.A., Mochon A.B., Garner O.B. Bacterial dispersal associated with speech in the setting of intravitreous injections. Arch. Ophthalmol. 2011. V. 129(12). P. 1551–1554. DOI: 10.1001/archophthalmol.2011.227
- Yeh P.T., Yang C.M., Lin Y.C., Chen M.S., Yang C.H. Bevacizumab pretreatment in vitrectomy with silicone oil for severe diabetic retinopathy. Retina. 2009. V. 29. P. 768–774.DOI: 10.1097/IAE.0b013e3181a3b7ef
- Jonas J.B., Schmidbauer M., Rensch F. Progression of tractional retinal detachment following intravitreal bevacizumab. Acta Ophthalmol. 2009. V. 87. P. 571–572.DOI: 10.1111/j.1755-3768.2008.01225.x
- Arevalo J.F., Maia M., Flynn Jr. H.W., Saravia M., Avery R.L., Wu L., Eid Farah M. et al. Tractional retinal detachment following intravitreal bevacizumab (Avastin) in patients with severe proliferative diabetic retinopathy. Br. J. Ophthalmol. 2008. V. 92. P. 213–216.DOI. P. 10.1136/bjo.2007.127142
- Jalil A., Fenerty C., Charles S. Intravitreal bevacizumab (Avastin) causing acute glaucoma. P. an unreported complication. Eye. 2007. V. 21. P. 1541. DOI: 10.1038/sj.eye.6703018
- Ahmadieh H., Shoeibi N., Entezari M., Monshizadeh R. Intravitreal bevacizumab for prevention of early postvitrectomy hemorrhage in diabetic patients: a randomized clinical trial. Ophthalmology. 2009. V. 116. P. 1943–1948.DOI: 10.1016/j.ophtha.2009.07.001
- Arevalo J.F., Sanchez J.G., Lasave A.F., Wu L., Maia M., Bonafonte S. et al. Intravitreal bevacizumab (Avastin) for diabetic retinopathy: the 2010 GLADAOF lecture. J. Ophthalmol. 2011. V. 2011. P. 584238.DOI: 10.1155/2011/584238
- Bakri S.J., Pulido J.S., McCannel C.A., Hodge D.O., Diehl N., Hillemeier J. Immediate intraocular pressure changes following intravitreal injections of triamcinolone, pegaptanib, and bevacizumab. Eye. 2009. V. 23(1). P. 181–185. DOI: 10.1038/sj.eye.6702938
- Gismondi M., Salati C., Salvetat M.L., Zeppieri M., Brusini P. Short-term effect of intravitreal injection of Ranibizumab (Lucentis) on intraocular pressure. J. Glaucoma. 2009. V. 18(9). P. 658–661. DOI: 10.1097/IJG.0b013e31819c4893
- Frenkel R.E., Mani L., Toler A.R., Frenkel M.P. Intraocular pressure effects of pegaptanib (Macugen) injections in patients with and without glaucoma. Am. J. Ophthalmol. 2007. V. 143. P. 1034–1035.DOI: 10.1016/j.ajo.2007.01.052
- Wu L., Martı´nez-Castellanos M.A., Quiroz-Mercado H., Arevalo J.F., Berrocal M.H., Farah M.E. et al. Pan American Collaborative Retina Group (PACORES). Twelve-month safety of intravitreal injections of IVB (Avastin): results of the Pan-American Collaborative Retina Study Group (PACORES). Graefes Arch. Clin. Exp. Ophthalmol. 2008. V. 246. P. 81–87.DOI: 10.1007/s00417-007-0660-z
- Ladas I.D., Karagiannis D.A., Rouvas A.A., Kotsolis A.I., Liotsou A., Vergados I. Safety of repeat intravitreal injections of bevacizumab versus ranibizumab: our experience after 2,000 injections. Retina. 2009. V. 29(3). P. 313–318.DOI: 10.1097/IAE.0b013e31819a5f98
- Loukopoulos V., Meier C., Gerding H. Hemorrhagic complications after intravitreal injections of ranibizumab in patients under coumarin-type anticoagulation. Klin. Monbl. Augenheilkd. 2010. V. 227(4). P. 289–291. DOI: 10.1055/s-0029-1245225
- Mason 3rd J.O., Frederick P.A., Neimkin M.G., White Jr. M.F., Feist R.M., Thomley M.L. et al. Incidence of hemorrhagic complications after intravitreal bevacizumab (avastin) or ranibizumab (lucentis) injections on systemically anticoagulated patients. Retina. 2010. V. 30(9). P. 1386–1389. DOI: 10.1097/IAE.0b013e3181e09739
- Lee S.J., Koh H.J. Enlargement of the foveal avascular zone in diabetic retinopathy after adjunctive intravitreal bevacizumab (Avastin) with pars plana vitrectomy. J. Ocul. Pharmacol. Ther. 2009. V. 25. P. 173–174. DOI: 10.1089/jop.2008.0092
- Michaelides M., Fraser-Bell S., Hamilton R., Kaines A., Egan C., Bunce C., 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): P. Report 1. Retina. 2010. V. 30. P. 781–786. DOI: 10.1097/IAE.0b013e3181d2f145
- Nishijima K., Ng Y.S., Zhong L., Bradley J., Schubert W., Jo N., 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. V. 171. P. 53–67.DOI: 10.2353/ajpath.2007.061237
- Saint-Geniez M., Maharaj A.S., Walshe T.E., Tucker B.A., Sekiyama E., Kurihara T., et al. Endogenous VEGF is required for visual function. P. evidence for a survival role on Muller cells and photoreceptors. PLoS One. 2008. V. 3. P. e3554. DOI: 10.1371/journal.pone.0003554
- Maharaj A.S., D'Amore P.A. Roles for VEGF in the adult. Microvasc. Res. 2007. V. 74. P. 100–113. DOI: 10.1016/j.mvr.2007.03.004
- Csaky K. Safety implications of vascular endothelial growth factor blockade for subjects receiving intravitreal anti-vascular endothelial growth factor therapies. Am. J. Ophthalmol. 2009. V. 148. P. 647–656. DOI: 10.1016/j.ajo.2009.06.014
- Schmucker C., Ehlken C., Agostini H.T., Antes G., Ruecker G., Lelgemann M. et al. A safety review and meta-analyses of bevacizumab and ranibizumab. P. off-label versus gold standard. PLoS One. 2012. V. 7(8). P. E42701. DOI: 10.1371/journal.pone.0042701
- The Royal College of Ophthalmologists. Statement.Bevacizumab (Avastin) Use in Medical Ophthalmology 2011. https://www.rcophth.ac.uk/2014/12/use-of-avastin-bevacizumab-in-age-related-macular-degeneration-2/
- Yeh P.T., Yang C.M., Lin Y.C., Chen M.S., Yang C.H. Bevacizumab pretreatment in vitrectomy with silicone oil for severe diabetic retinopathy. Retina. 2009. V. 29. P. 768–774. DOI: 10.1097/IAE.0b013e3181a3b7ef
- Ahmadieh H., Shoeibi N., Entezari M., Monshizadeh R. Intravitreal bevacizumab for prevention of early postvitrectomy hemorrhage in diabetic patients: a randomized clinical trial. Ophthalmology. 2009. V. 116. P. 1943–1948. DOI: 10.1016/j.ophtha.2009.07.001
- Moradian S., Ahmadieh H., Malihi M., Soheilian M., Dehghan M.H., Azarmina M. Intravitreal bevacizumab in active progressive proliferative diabetic retinopathy. Graefes Arch. Clin. Exp. Ophthalmol. 2008. V. 246. P. 1699–1705. DOI: 10.1007/s00417-008-0914-4
- Filho J.A., Messias A., Almeida F.P., Ribeiro J.A., Costa R.A., Scott I.U., et al. Panretinal photocoagulation (PRP) versus PRP plus intravitreal ranibizumab for high-risk proliferative diabetic retinopathy. Acta Ophthalmol. 2011. V. 89. P. 567–572.DOI: 10.1111/j.1755-3768.2011.02184.x
- Cho W.B., Oh S.B., Moon J.W., Kim H.C. Panretinal photocoagulation combined with intravitreal bevacizumab in high-risk proliferative diabetic retinopathy. Retina. 2009. V. 29. P. 516–522.DOI: 10.1097/IAE.0b013e31819a5fc2
- Early Treatment Diabetic Retinopathy Study Research Group. Treatment techniques and clinical guidelines for photocoagulation of diabetic macular edema. EarlyTreatmentDiabeticRetinopathy Study Report Number 2. Ophthalmology. 1987. P. 761–774.