Challenges for further successful development of tumor necrosis factor targeting therapies for uveitis

References

• Tsirouki T, Dastiridou A, Symeonidis C, et al. A focus on the epidemiology of uveitis. Ocul Immunol Inflamm. 2018;26(1):2–16. doi: 10.1080/09273948.2016.1196713
   PubMed Web of Science ®Google Scholar
• Koronis S, Stavrakas P, Balidis M, et al. Update in treatment of uveitic macular edema. Drug Des Devel Ther. 2019;13:667–680. doi: 10.2147/DDDT.S166092
   PubMed Web of Science ®Google Scholar
• Massa H, Pipis SY, Adewoyin T, et al. Macular edema associated with non-infectious uveitis: pathophysiology, etiology, prevalence, impact and management challenges. Clin Ophthalmol. 2019;13:1761–1777. doi: 10.2147/OPTH.S180580
   PubMed Web of Science ®Google Scholar
• Jabs DA, McCluskey P, Palestine AG, et al. The standardisation of uveitis nomenclature (SUN) project. Clin Exp Ophthalmol. 2022 Sep 27;50(9):991–1000. doi: 10.1111/ceo.14175
   Web of Science ®Google Scholar
• Kaleemunnisha S, Sudharshan S, Biswas J. Quality of life in non-infectious uveitis patients on immunosuppressive therapy. Middle East Afr J Ophthalmol. 2014 Jul;21(3):225–231. doi: 10.4103/0974-9233.134675
   PubMedGoogle Scholar
• Suhler EB, Lloyd MJ, Choi D, et al. Incidence and prevalence of uveitis in veterans affairs medical centers of the pacific Northwest. Am J Ophthalmol. 2008 Dec;146(6):890–6 e8.
   PubMed Web of Science ®Google Scholar
• Thorne JE, Suhler E, Skup M, et al. Prevalence of noninfectious uveitis in the United States: a claims-based analysis. JAMA Ophthalmol. 2016 Nov 1;134(11):1237–1245. doi: 10.1001/jamaophthalmol.2016.3229
   PubMed Web of Science ®Google Scholar
• Foster CS, Kothari S, Anesi SD, et al. The ocular immunology and uveitis foundation preferred practice patterns of uveitis management. Surv Ophthalmol. 2016 Jan;61(1):1–17.
   PubMed Web of Science ®Google Scholar
• Cordero-Coma M, Sobrin L. Anti-tumor necrosis factor-alpha therapy in uveitis. Surv Ophthalmol. 2015 Nov;60(6):575–589. doi: 10.1016/j.survophthal.2015.06.004
   PubMed Web of Science ®Google Scholar
• Jiang Q, Li Z, Tao T, et al. TNF-alpha in uveitis: from bench to clinic. Front Pharmacol. 2021;12:740057. doi: 10.3389/fphar.2021.740057
   PubMed Web of Science ®Google Scholar
• Dick AD, Rosenbaum JT, Al-Dhibi HA, et al. Guidance on noncorticosteroid systemic immunomodulatory therapy in noninfectious uveitis: fundamentals of care for UveitiS (FOCUS) initiative. Ophthalmol. 2018 May;125(5):757–773.
   PubMed Web of Science ®Google Scholar
• Levy-Clarke G, Jabs DA, Read RW, et al. Expert panel recommendations for the use of anti-tumor necrosis factor biologic agents in patients with ocular inflammatory disorders. Ophthalmol. 2014 Mar;121(3):785–96 e3.
   PubMed Web of Science ®Google Scholar
• Jaffe GJ, Dick AD, Brezin AP, et al. Adalimumab in patients with active noninfectious uveitis. N Engl J Med. 2016 Sep 8;375(10):932–43. doi: 10.1056/NEJMoa1509852
   PubMed Web of Science ®Google Scholar
• Nguyen QD, Merrill PT, Jaffe GJ, et al. Adalimumab for prevention of uveitic flare in patients with inactive non-infectious uveitis controlled by corticosteroids (VISUAL II): a multicentre, double-masked, randomised, placebo-controlled phase 3 trial. Lancet. 2016 Sep 17;388(10050):1183–92. doi: 10.1016/S0140-6736(16)31339-3
   PubMed Web of Science ®Google Scholar
• Suhler EB, Adan A, Brezin AP, et al. Safety and efficacy of adalimumab in patients with noninfectious uveitis in an ongoing open-label study: VISUAL III. Ophthalmol. 2018 Jul;125(7):1075–1087.
   PubMed Web of Science ®Google Scholar
• Ramanan AV, Dick AD, Jones AP, et al. Adalimumab plus Methotrexate for Uveitis in Juvenile Idiopathic Arthritis. N Engl J Med. 2017 Apr 27;376(17):1637–1646. doi: 10.1056/NEJMoa1614160
   PubMed Web of Science ®Google Scholar
• Liu W, Bai D, Kou L. Comparison of infliximab with adalimumab for the treatment of non-infectious uveitis: a systematic review and meta-analysis. BMC Ophthalmol. 2023 May 29;23(1):240.
   PubMed Web of Science ®Google Scholar
• Alizadegan F, Yalcinbayir O, Ucan Gunduz G, et al. Infliximab therapy in Behcet’s uveitis. J Fr Ophtalmol. 2022 Nov;45(9):1036–1041.
   PubMed Web of Science ®Google Scholar
• Cecchin V, Zannin ME, Ferrari D, et al. Longterm safety and efficacy of adalimumab and infliximab for uveitis associated with juvenile idiopathic arthritis. J Rheumatol. 2018 Aug;45(8):1167–1172.
   PubMed Web of Science ®Google Scholar
• Baughman RP, Lower EE, Bradley DA, et al. Etanercept for refractory ocular sarcoidosis: results of a double-blind randomized trial. Chest. 2005 Aug;128(2):1062–47.
   PubMed Web of Science ®Google Scholar
• Foster CS, Tufail F, Waheed NK, et al. Efficacy of etanercept in preventing relapse of uveitis controlled by methotrexate. Arch Ophthalmol. 2003 Apr;121(4):437–440.
   PubMed Web of Science ®Google Scholar
• Fabiani C, Vitale A, Lopalco G, et al. Different roles of TNF inhibitors in acute anterior uveitis associated with ankylosing spondylitis: state of the art. Clin Rheumatol. 2016 Nov;35(11):2631–2638.
   PubMed Web of Science ®Google Scholar
• van Bentum RE, Heslinga SC, Nurmohamed MT, et al. Reduced occurrence rate of acute anterior uveitis in ankylosing spondylitis treated with golimumab - the GO-EASY study. J Rheumatol. 2019 Feb;46(2):153–159.
   PubMed Web of Science ®Google Scholar
• Cordero-Coma M, Salom D, Diaz-Llopis M, et al. Golimumab for uveitis. Ophthalmol. 2011 Sep;118(9):1892 e3–4.
   PubMed Web of Science ®Google Scholar
• Palmou-Fontana N, Calvo-Rio V, Martin-Varillas JL, et al. Golimumab in refractory uveitis associated to juvenile idiopathic arthritis: multicentre study of 7 cases and literature review. Clin Exp Rheumatol. 2018 Jul;36(4):652–657.
   PubMed Web of Science ®Google Scholar
• Tosi GM, Sota J, Vitale A, et al. Efficacy and safety of certolizumab pegol and golimumab in the treatment of non-infectious uveitis. Clin Exp Rheumatol. 2019 Jul;37(4):680–683.
   PubMed Web of Science ®Google Scholar
• Brito-Zeron P, Perez-Alvarez R, Ramos-Casals M, et al. Etanercept and uveitis: friends or foes? Curr Med Res Opin. 2015 Feb;31(2):251–2.
   PubMed Web of Science ®Google Scholar
• Lim LL, Fraunfelder FW, Rosenbaum JT. Do tumor necrosis factor inhibitors cause uveitis? A registry-based study. Arthritis Rheum. 2007 Oct;56(10):3248–52. doi: 10.1002/art.22918
   PubMed Web of Science ®Google Scholar
• Sharon Y, Chu DS. Certolizumab pegol - Tumor necrosis factor inhibitor for refractory uveitis. Am J Ophthalmol Case Rep. 2020 Jun;18:100633. doi: 10.1016/j.ajoc.2020.100633
   PubMedGoogle Scholar
• Bessette AP, Sharma S. Adalimumab for Noninfectious Uveitis. Ophthalmol Retina. 2017 May;1(3):179–180. doi: 10.1016/j.oret.2017.02.005
   PubMedGoogle Scholar
• Roda G, Jharap B, Neeraj N, et al. Loss of response to anti-TNFs: definition, epidemiology, and management. Clin Transl Gastroenterol. 2016 Jan 7;7(1):e135. doi: 10.1038/ctg.2015.63
   PubMed Web of Science ®Google Scholar
• Kempen JH, Daniel E, Gangaputra S, et al. Methods for identifying long-term adverse effects of treatment in patients with eye diseases: the systemic immunosuppressive therapy for eye diseases (SITE) cohort study. Ophthal Epidemiol. 2008 Jan;15(1):47–55.
   PubMed Web of Science ®Google Scholar
• Kempen JH, Newcomb CW, Washington TL, et al. Use of immunosuppression and the risk of subsequent overall or cancer mortality. Ophthalmol. 2023 Dec;130(12):1258–1268.
   PubMed Web of Science ®Google Scholar
• Deaner JD, Srivastava SK, Hajj-Ali RA, et al. Recurrence rates of inflammation after switching from the originator infliximab to biosimilar infliximab-abda for noninfectious uveitis. Am J Ophthalmol. 2021 May;225:172–177.
   PubMedGoogle Scholar
• Murray GM, Griffith N, Sinnappurajar P, et al. Clinical efficacy of biosimilar switch of adalimumab for management of uveitis. Ocul Immunol Inflamm. 2023 Feb;21:1–5.
   Google Scholar
• Kumar N, Follestad T, Sen HN, et al. A systematic switch from originator infliximab to biosimilar infliximab in patients with non-infectious uveitis. Am J Ophthalmol. 2021 May;225:178–184.
   PubMed Web of Science ®Google Scholar
• Coghlan J, He H, Schwendeman AS. Overview of Humira(R) Biosimilars: Current European Landscape and Future Implications. J Pharm Sci. 2021 Apr;110(4):1572–1582. doi: 10.1016/j.xphs.2021.02.003
   PubMed Web of Science ®Google Scholar
• Jabs DA, Berkenstock MK, Altaweel MM, et al. The conundrum of clinical trials for the uveitides: appropriate outcome measures for one treatment used in several diseases. Epidemiol Rev. 2022 Dec 21;44(1):2–16. doi: 10.1093/epirev/mxac001
   PubMed Web of Science ®Google Scholar
• Okada AA. Noninfectious uveitis: a scarcity of randomized clinical trials. Arch Ophthalmol. 2005 May;123(5):682–3. doi: 10.1001/archopht.123.5.682
   PubMedGoogle Scholar
• Lee RW, Dick AD. Current concepts and future directions in the pathogenesis and treatment of non-infectious intraocular inflammation. Eye (Lond). 2012 Jan;26(1):17–28. doi: 10.1038/eye.2011.255
   PubMed Web of Science ®Google Scholar
• Rosenbaum JT, Asquith M. The microbiome and HLA-B27-associated acute anterior uveitis. Nat Rev Rheumatol. 2018 Dec;14(12):704–713. doi: 10.1038/s41584-018-0097-2
   PubMed Web of Science ®Google Scholar
• Rodriguez-Fernandez CA, Iglesias MB, de Domingo B, et al. Microbiome in Immune-Mediated Uveitis. Int J Mol Sci. 2022 Jun 24;23(13):7020. doi: 10.3390/ijms23137020
   PubMed Web of Science ®Google Scholar
• Kempen JH, Ganesh SK, Sangwan VS, et al. Interobserver agreement in grading activity and site of inflammation in eyes of patients with uveitis. Am J Ophthalmol. 2008 Dec;146(6):813–8 e1.
   PubMed Web of Science ®Google Scholar
• Halim MS, Hasanreisoglu M, Onghanseng N, et al. Correlation of clinical aqueous flare grading to semi-automated flare measurements using laser flare photometry. Ocul Immunol Inflamm. 2022 Oct;30(7–8):1906–1912.
   PubMed Web of Science ®Google Scholar
• Pichi F, Carreno E. The vitreous in uveitis: characterizing the invisible with optical coherence tomography. Ocul Immunol Inflamm. 2022 Apr 3;30(3):690–696.
   PubMed Web of Science ®Google Scholar
• Hassan M, Sadiq MA, Ormaechea MS, et al. Utilisation of composite endpoint outcome to assess efficacy of tocilizumab for non-infectious uveitis in the STOP-Uveitis study. Br J Ophthalmol. 2023 Aug;107(8):1197–1201.
   PubMed Web of Science ®Google Scholar
• Cordoba G, Schwartz L, Woloshin S, et al. Definition, reporting, and interpretation of composite outcomes in clinical trials: systematic review. BMJ. 2010 Aug 18;341(aug18 3):c3920. doi: 10.1136/bmj.c3920
   PubMedGoogle Scholar
• McCall B Filgotinib reduces flare risk in uveitis in phase 2 study Medscape2022. https://www.medscape.com/s/viewarticle/980731?form=fpf
   Google Scholar
• Pascual-Camps I, Hernandez-Martinez P, Monje-Fernandez L, et al. Update on intravitreal anti-tumor necrosis factor alpha therapies for ocular disorders. J Ophthalmic Inflamm Infect. 2014;4(1):26. doi: 10.1186/s12348-014-0026-8
   PubMedGoogle Scholar
• Varela-Fernandez R, Diaz-Tome V, Luaces-Rodriguez A, et al. Drug delivery to the posterior segment of the eye: biopharmaceutic and pharmacokinetic considerations. Pharmaceutics. 2020 Mar 16;12(3):269. doi: 10.3390/pharmaceutics12030269
   PubMed Web of Science ®Google Scholar
• Leal I, Rodrigues FB, Sousa DC, et al. Efficacy and safety of intravitreal anti-tumour necrosis factor drugs in adults with non-infectious uveitis - a systematic review. Acta Ophthalmol. 2018 Sep;96(6):e665–e675.
   PubMed Web of Science ®Google Scholar
• Patel D, Patel SN, Chaudhary V, et al. Complications of intravitreal injections: 2022. Curr Opin Ophthalmol. 2022 May 1;33(3):137–146. doi: 10.1097/ICU.0000000000000850
   PubMed Web of Science ®Google Scholar
• Xu Y, Tan CS. Safety and complications of intravitreal injections performed in an Asian population in Singapore. Int Ophthalmol. 2017 Apr;37(2):325–332. doi: 10.1007/s10792-016-0241-4
   PubMed Web of Science ®Google Scholar
• Theodossiadis PG, Liarakos VS, Sfikakis PP, et al. Intravitreal administration of the anti-TNF monoclonal antibody infliximab in the rabbit. Graefes Arch Clin Exp Ophthalmol. 2009 Feb;247(2):273–81.
   PubMed Web of Science ®Google Scholar
• Zayit-Soudry S, Vainer I, Zemel E, et al. Infliximab exerts a dose-dependent effect on retinal safety in the albino rabbit. Doc Ophthalmol. 2017 Dec;135(3):175–185.
   PubMed Web of Science ®Google Scholar
• Giansanti F, Ramazzotti M, Vannozzi L, et al. A pilot study on ocular safety of intravitreal infliximab in a rabbit model. Invest Ophthalmol Vis Sci. 2008 Mar;49(3):1151–6.
   PubMed Web of Science ®Google Scholar
• Manzano RP, Peyman GA, Carvounis PE, et al. Ocular toxicity of intravitreous adalimumab (Humira) in the rabbit. Graefes Arch Clin Exp Ophthalmol. 2008 Jun;246(6):907–911.
   PubMed Web of Science ®Google Scholar
• Durmaz Engin C, Cilaker Micili S, Yilmaz O, et al. Ocular toxicity of intravitreal golimumab in a rabbit model. Turk J Med Sci. 2020 Jun 23;50(4):1111–1122. doi: 10.3906/sag-1911-11
   PubMed Web of Science ®Google Scholar
• Giganti M, Beer PM, Lemanski N, et al. Adverse events after intravitreal infliximab (Remicade). Retina. 2010 Jan;30(1):71–80.
   PubMed Web of Science ®Google Scholar
• Rosenfeld PJ, Goodman KW. When is off-label drug use in the patient’s best interest? Am J Ophthalmol. 2009 May;147(5):761–3. doi: 10.1016/j.ajo.2009.01.011
   PubMed Web of Science ®Google Scholar
• Arias L, Caminal JM, Badia MB, et al. Intravitreal infliximab in patients with macular degeneration who are nonresponders to antivascular endothelial growth factor therapy. Retina. 2010 Nov;30(10):1601–8.
   PubMed Web of Science ®Google Scholar
• Wu LR. Correspondence to: intravitreal tumor necrosis factor inhibitors in the treatment of refractory diabetic macular edema: a pilot study from the pan-american collaborative retina study group. Retina. 2013 Jun;33(6):1287–1290. doi: 10.1097/IAE.0b013e31828bcb2f
   PubMedGoogle Scholar
• Wu L, Arevalo JF, Hernandez-Bogantes E, et al. Intravitreal tumor necrosis factor-alpha inhibitors for neovascular age-related macular degeneration suboptimally responsive to antivascular endothelial growth factor agents: a pilot study from the Pan American Collaborative Retina study Group. J Ocul Pharmacol Ther. 2013 Apr;29(3):366–71.
   PubMed Web of Science ®Google Scholar
• Pulido JS, Pulido JE, Michet CJ, et al. More questions than answers: a call for a moratorium on the use of intravitreal infliximab outside of a well-designed trial. Retina. 2010 Jan;30(1):1–5. doi: 10.1097/IAE.0b013e3181cde727
   PubMed Web of Science ®Google Scholar
• Markomichelakis N, Delicha E, Masselos S, et al. Intravitreal infliximab for sight-threatening relapsing uveitis in Behcet disease: a pilot study in 15 patients. Am J Ophthalmol. 2012 Sep;154(3):534–541 e1.
   PubMed Web of Science ®Google Scholar
• Hamza MM, Macky TA, Sidky MK, et al. Intravitreal infliximab in refractory uveitis in behcet’s disease: a safety and efficacy clinical study. Retina. 2016 Dec;36(12):2399–2408.
   PubMed Web of Science ®Google Scholar
• Androudi S, Tsironi E, Kalogeropoulos C, et al. Intravitreal adalimumab for refractory uveitis-related macular edema. Ophthalmol. 2010 Aug;117(8):1612–6.
   PubMed Web of Science ®Google Scholar
• Hamam RN, Barikian AW, Antonios RS, et al. Intravitreal Adalimumab in Active Noninfectious Uveitis: A Pilot Study. Ocul Immunol Inflamm. 2016 Jun;24(3):319–26.
   PubMed Web of Science ®Google Scholar
• Evangelatos G, Bamias G, Kitas GD, et al. The second decade of anti-TNF-a therapy in clinical practice: new lessons and future directions in the COVID-19 era. Rheumatol Int. 2022 Sep;42(9):1493–1511.
   PubMed Web of Science ®Google Scholar
• Nash P, Smolen JS. Response to: ‘correspondence on ‘points to consider for the treatment of immune-mediated inflammatory diseases with Janus kinase inhibitors: a consensus statement’’ by banday et al. Ann Rheum Dis. 2023 May;82(5):e105.
   PubMed Web of Science ®Google Scholar
• Wen J, Hu H, Chen M, et al. Role of Janus Kinase (JAK) inhibitor in autoimmune ocular inflammation: a systematic review. J Immunol Res. 2021;2021:2324400. doi: 10.1155/2021/2324400
   PubMed Web of Science ®Google Scholar
• Bellur S, McHarg M, Kongwattananon W, et al. Antidrug antibodies to tumor necrosis factor alpha inhibitors in patients with noninfectious uveitis. JAMA Ophthalmol. 2023 Feb 1;141(2):150–156. doi: 10.1001/jamaophthalmol.2022.5584
   PubMed Web of Science ®Google Scholar
• Liew SH, Nichols KK, Klamerus KJ, et al. Tofacitinib (CP-690,550), a Janus kinase inhibitor for dry eye disease: results from a phase 1/2 trial. Ophthalmol. 2012 Jul;119(7):1328–1335.
   PubMed Web of Science ®Google Scholar
• Ramanan AV, Guly CM, Keller SY, et al. Clinical effectiveness and safety of baricitinib for the treatment of juvenile idiopathic arthritis-associated uveitis or chronic anterior antinuclear antibody-positive uveitis: study protocol for an open-label, adalimumab active-controlled phase 3 clinical trial (JUVE-BRIGHT). Trials. 2021 Oct 9;22(1):689. doi: 10.1186/s13063-021-05651-5
   PubMed Web of Science ®Google Scholar
• Karkhur S, Hasanreisoglu M, Vigil E, et al. Interleukin-6 inhibition in the management of non-infectious uveitis and beyond. J Ophthalmic Inflamm Infect. 2019 Sep 16;9(1):17. doi: 10.1186/s12348-019-0182-y
   PubMed Web of Science ®Google Scholar
• Haruta H, Ohguro N, Fujimoto M, et al. Blockade of interleukin-6 signaling suppresses not only th17 but also interphotoreceptor retinoid binding protein-specific Th1 by promoting regulatory T cells in experimental autoimmune uveoretinitis. Invest Ophthalmol Vis Sci. 2011 May 17;52(6):3264–3271. doi: 10.1167/iovs.10-6272
   PubMed Web of Science ®Google Scholar
• Sepah YJ, Sadiq MA, Chu DS, et al. Primary (month-6) outcomes of the STOP-Uveitis study: evaluating the safety, tolerability, and efficacy of tocilizumab in patients with noninfectious uveitis. Am J Ophthalmol. 2017 Nov;183:71–80. doi: 10.1016/j.ajo.2017.08.019
   PubMed Web of Science ®Google Scholar
• Mesquida M, Molins B, Llorenc V, et al. Long-term effects of tocilizumab therapy for refractory uveitis-related macular edema. Ophthalmol. 2014 Dec;121(12):2380–6.
   PubMed Web of Science ®Google Scholar
• Uludag G, Karaca I, Akhavanrezayat A, et al. Efficacy and safety of tocilizumab in the management of non-infectious uveitis failed with conventional immunomodulatory and anti-TNFalpha therapies. Ocul Immunol Inflamm. 2022 Dec;21:1–7.
   Google Scholar
• Karaca I, Uludag G, Matsumiya W, et al. Six-month outcomes of infliximab and tocilizumab therapy in non-infectious retinal vasculitis. Eye (Lond). 2023 Aug;37(11):2197–2203.
   PubMed Web of Science ®Google Scholar
• Sfikakis PP, Markomichelakis N, Alpsoy E, et al. Anti-TNF therapy in the management of Behcet’s disease–review and basis for recommendations. Rheumatology (Oxford). 2007 May;46(5):736–741.
   PubMed Web of Science ®Google Scholar
• Tai F, Mehraban Far P, Pechlivanoglou P, et al. Efficacy and safety of adalimumab and infliximab for noninfectious uveitis. Ophthalmol. 2022 Mar;129(3):357–359.
   PubMed Web of Science ®Google Scholar