Efficacy and Safety of Adalimumab in Patients with Behçet Uveitis: A Systematic Review and Meta-Analysis

References

• Evereklioglu C. Current concepts in the etiology and treatment of Behçet disease. Surv Ophthalmol. 2005;50(4):297–350. doi:10.1016/j.survophthal.2005.04.009.
   PubMed Web of Science ®Google Scholar
• Evereklioglu C. Managing the symptoms of Behçet’s disease. Expert Opin Pharmacother. 2004;5(2):317–328. doi:10.1517/14656566.5.2.317.
   PubMed Web of Science ®Google Scholar
• Azizlerli G, Akdağ Köse A, Sarıca R, et al. Prevalence of Behçet’s disease in Istanbul, Turkey. Int J Dermatol. 2003;42(10):803–806. doi:10.1046/j.1365-4362.2003.01893.x.
   PubMed Web of Science ®Google Scholar
• Krause I, Yankevich A, Fraser A, et al. Prevalence and clinical aspects of Behcet’s disease in the north of Israel. Clin Rheumatol. 2007;26(4):555–560. doi:10.1007/s10067-006-0349-4.
   PubMed Web of Science ®Google Scholar
• Kaçmaz RO, Kempen JH, Newcomb C, et al. Ocular inflammation in Behçet disease: incidence of ocular complications and of loss of visual acuity. Am J Ophthalmol. 2008;146(6):828–836. doi:10.1016/j.ajo.2008.06.019.
   PubMed Web of Science ®Google Scholar
• Kitaichi N, Miyazaki A, Iwata D, Ohno S, Stanford MR, Chams H. Ocular features of Behçet’s disease: an international collaborative study. Br J Ophthalmol. 2007;91(12):1579–1582. doi:10.1136/bjo.2007.123554.
   PubMed Web of Science ®Google Scholar
• Evereklioglu C, Er H, Türköz Y, Çekmen M. Serum levels of TNF-α, sIL-2R, IL-6, and IL-8 are increased and associated with elevated lipid peroxidation in patients with Behçet’s disease. Mediators Inflamm . 2002;11(2):87–93. doi:10.1080/09629350220131935.
   PubMed Web of Science ®Google Scholar
• Evereklioglu C, Borlu M. Sustained remission after infliximab in a child with vasculitis refractory to conventional immunosuppressives including interferon-α. Br J Ophthalmol. 2008;92(8):1034. doi:10.1136/bjo.2007.127522.
   PubMed Web of Science ®Google Scholar
• Atzeni F, Turiel M, Capsoni F, Doria A, Meroni P, Sarzi-puttini P. Autoimmunity and anti-TNF-α agents. Ann N Y Acad Sci. 2005;1051(1):559–569. doi:10.1196/annals.1361.100.
   PubMedGoogle Scholar
• Jaffe GJ, Dick AD, Brézin AP, et al. Adalimumab in patients with active noninfectious uveitis. N Engl J Med. 2016;375(10):932–943. 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;388(10050):1183–1192. doi:10.1016/S0140-6736(16)31339-3.
   PubMed Web of Science ®Google Scholar
• Evereklioglu C. Ocular Behçet disease: current therapeutic approaches. Curr Opin Ophthalmol. 2011;22(6):508–516. doi:10.1097/ICU.0b013e32834bbe91.
   PubMed Web of Science ®Google Scholar
• Leclercq M, Andrillon A, Maalouf G, et al. Anti-TNF-α versus tocilizumab in the treatment of refractory uveitic macular edema: a multicenter study from the French uveitis network. Ophthalmology. 2021. doi:10.1016/j.ophtha.2021.11.013.
   PubMedGoogle Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg. 2021;88:105906. doi:10.1016/j.ijsu.2021.105906.
   PubMed Web of Science ®Google Scholar
• Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–605. doi:10.1007/s10654-010-9491-z.
   PubMed Web of Science ®Google Scholar
• Holladay JT. Proper Method for Calculating Average Visual Acuity. Vol 13. NJ: SLACK Incorporated Thorofare; 1997:388–391. doi: 10.3928/1081-597X-19970701-16.
   Google Scholar
• Holladay JT. Visual acuity measurements. J Cataract Refract Surg. 2004;30(2):287–290. doi:10.1016/j.jcrs.2004.01.014.
   PubMed Web of Science ®Google Scholar
• Schulze-Bonsel K, Feltgen N, Burau H, Hansen L, Bach M. Visual acuities “hand motion” and “counting fingers” can be quantified with the Freiburg visual acuity test. Invest Ophthalmol Vis Sci. 2006;47(3):1236–1240. doi:10.1167/iovs.05-0981.
   PubMed Web of Science ®Google Scholar
• Group SoUNW. Standardization of uveitis nomenclature for reporting clinical data. Results of the first international workshop. Am J Ophthalmol. 2005;140(3):509–516. doi:10.1016/j.ajo.2005.03.057.
   PubMed Web of Science ®Google Scholar
• Nussenblatt RB, Palestine AG, Chan -C-C, Roberge F. Standardization of vitreal inflammatory activity in intermediate and posterior uveitis. Ophthalmology. 1985; 92(4):467–471.
   PubMed Web of Science ®Google Scholar
• Hogan MJ, Kimura SJ, Thygeson P. Signs and symptoms of uveitis: I. Anterior uveitis. Am J Ophthalmol. 1959;47(5):155–170. doi:10.1016/S0002-9394(14)78239-X.
   PubMed Web of Science ®Google Scholar
• Tugal-Tutkun I, Herbort CP, Khairallah M. Scoring of dual fluorescein and ICG inflammatory angiographic signs for the grading of posterior segment inflammation (dual fluorescein and ICG angiographic scoring system for uveitis). Int Ophthalmol. 2010;30(5):539–552. doi:10.1007/s10792-008-9263-x.
   PubMedGoogle Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. 2003;327(7414):557–560. doi:10.1136/bmj.327.7414.557.
   PubMed Web of Science ®Google Scholar
• Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14(1):1–13. doi:10.1186/1471-2288-14-135.
   PubMed Web of Science ®Google Scholar
• Luo D, Wan X, Liu J, Tong T. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat Methods Med Res. 2018;27(6):1785–1805. doi:10.1177/0962280216669183.
   PubMed Web of Science ®Google Scholar
• Kunimi K, Usui Y, Asakage M, et al. Anti-TNF-alpha therapy for refractory uveitis associated with Behcet’s syndrome and sarcoidosis: a single center study of 131 patients. Ocul Immunol Inflamm. 2022;30(1):223–230. doi:10.1080/09273948.2020.1791346.
   PubMed Web of Science ®Google Scholar
• Yang SZ, Huang ZH, Liu XX, et al. Comparative study of adalimumab versus conventional therapy in sight-threatening refractory Behcet’s uveitis with vasculitis. Int Immunopharmacol. 2021;93:7. doi:10.1016/j.intimp.2021.107430.
   Web of Science ®Google Scholar
• Yang SZ, Huang ZH, Hu YW, et al. The efficacy of adalimumab as an initial treatment in patients with Behcet’s retinal vasculitis. Front Pharmacol. 2021;12:10.
   Web of Science ®Google Scholar
• Soheilian M, Ebrahimiadib N, Hedayatfar A, Hosseini M, Zarei M, Anjidani N. Efficacy of biosimilar adalimumab in the treatment of Behçet’s uveitis. Ocul Immunol Inflamm. 2021;30(6):1495–1500. doi:10.1080/09273948.2021.1900276.
   PubMed Web of Science ®Google Scholar
• Kim BH, Park UC, Park SW, Yu HG. Ultra-widefield fluorescein angiography to monitor therapeutic response to adalimumab in Behcet’s uveitis. Ocul Immunol Inflamm. 2021;30(6):1347–1353. doi:10.1080/09273948.2021.1872652.
   PubMed Web of Science ®Google Scholar
• Atienza-Mateo B, Martin-Varillas JL, Calvo-Rio V, et al. Comparative study of infliximab versus adalimumab in refractory uveitis due to Behcet’s disease: national multicenter study of 177 cases. Arthritis Rheumatol. 2019;71(12):2081–2089. doi:10.1002/art.41026.
   PubMed Web of Science ®Google Scholar
• Fabiani C, Sota J, Vitale A, et al. Cumulative retention rate of adalimumab in patients with Behçet’s disease-related uveitis: a four-year follow-up study. Br J Ophthalmoly. 2018;102(5):637–641. doi:10.1136/bjophthalmol-2017-310733.
   PubMed Web of Science ®Google Scholar
• Fabiani C, Vitale A, Emmi G, et al. Efficacy and safety of adalimumab in Behçet’s disease-related uveitis: a multicenter retrospective observational study. Clin Rheumatol. 2017;36(1):183–189. doi:10.1007/s10067-016-3480-x.
   PubMed Web of Science ®Google Scholar
• Interlandi E, Leccese P, Olivieri I, Latanza L. Adalimumab for treatment of severe Behçet’s uveitis: a retrospective long-term follow-up study. Clin Experimental Rheumatol. 2014; 32(4 Suppl 84):S58–62.
   PubMed Web of Science ®Google Scholar
• Bawazeer A, Raffa LH, Nizamuddin. Clinical experience with adalimumab in the treatment of ocular Behcet disease. Ocul Immunol Inflamm. 2010;18(3):226–232. doi:10.3109/09273948.2010.483314.
   PubMed Web of Science ®Google Scholar
• Ahn JK, Yu HG, Chung H, Park YG. Intraocular cytokine environment in active Behçet uveitis. Am J Ophthalmol. 2006;142(3):429–434. e421. doi:10.1016/j.ajo.2006.04.016.
   PubMed Web of Science ®Google Scholar
• Hale S, Lightman S. Anti-TNF therapies in the management of acute and chronic uveitis. Cytokine. 2006;33(4):231–237. doi:10.1016/j.cyto.2005.12.012.
   PubMed Web of Science ®Google Scholar
• Whitcup SM, Sen HN. Whitcup and Nussenblatt’s Uveitis: Fundamentals and Clinical Practice. New York: Elsevier Health Sciences; 2021.
   Google Scholar
• Dick AD, Forrester JV, Liversidge J, Cope AP. The role of tumour necrosis factor (TNF-α) in experimental autoimmune uveoretinitis (EAU). Prog Ret Eye Res. 2004;23(6):617–637. doi:10.1016/j.preteyeres.2004.06.005.
   PubMed Web of Science ®Google Scholar
• Rothova A, Suttorp-van Schulten M, Treffers WF, Kijlstra A. Causes and frequency of blindness in patients with intraocular inflammatory disease. Br J Ophthalmol. 1996;80(4):332–336. doi:10.1136/bjo.80.4.332.
   PubMed Web of Science ®Google Scholar
• Markomichelakis NN, Halkiadakis I, Pantelia E, et al. Course of macular edema in uveitis under medical treatment. Ocul Immunol Inflamm. 2007;15(2):71–79. doi:10.1080/09273940701244509.
   PubMed Web of Science ®Google Scholar
• Gritz DC, Schwaber EJ, Wong IG. Complications of uveitis: the northern California epidemiology of uveitis study. Ocul Immunol Inflamm. 2018;26(4):584–594. doi:10.1080/09273948.2016.1247174.
   PubMed Web of Science ®Google Scholar
• Tomkins-Netzer O, Talat L, Bar A, et al. Long-term clinical outcome and causes of vision loss in patients with uveitis. Ophthalmology. 2014;121(12):2387–2392. doi:10.1016/j.ophtha.2014.07.007.
   PubMed Web of Science ®Google Scholar
• Hassan M, Karkhur S, Bae JH, et al. New therapies in development for the management of non-infectious uveitis: a review. Clin Exp Ophthalmol. 2019;47(3):396–417. doi:10.1111/ceo.13511.
   PubMed Web of Science ®Google Scholar
• Hu Y, Huang Z, Yang S, Chen X, Su W, Liang D. Effectiveness and safety of anti-tumor necrosis factor-alpha agents treatment in Behcets’ disease-associated uveitis: a systematic review and meta-analysis. Front Pharmacol. 2020;11:941. doi:10.3389/fphar.2020.00941.
   PubMed Web of Science ®Google Scholar
• Maccora I, Fusco E, Marrani E, Ramanan AV, Simonini G. Changing evidence over time: updated meta-analysis regarding anti-TNF efficacy in childhood chronic uveitis. Rheumatology. 2021;60(2):568–587. doi:10.1093/rheumatology/keaa595.
   PubMed Web of Science ®Google Scholar
• Ming S, Xie K, He H, Li Y, Lei B. Efficacy and safety of adalimumab in the treatment of non-infectious uveitis: a meta-analysis and systematic review. Drug Des Devel Ther. 2018;12:2005. doi:10.2147/DDDT.S160431.
   PubMed Web of Science ®Google Scholar
• Dick AD, Tundia N, Sorg R, et al. Risk of ocular complications in patients with noninfectious intermediate uveitis, posterior uveitis, or panuveitis. Ophthalmology. 2016;123(3):655–662. doi:10.1016/j.ophtha.2015.10.028.
   PubMed Web of Science ®Google Scholar
• Tugal-Tutkun I, Ozdal PC, Oray M, Onal S. Review for diagnostics of the year: multimodal imaging in Behçet uveitis. Ocul Immunol Inflamm. 2017;25(1):7–19. doi:10.1080/09273948.2016.1205100.
   PubMed Web of Science ®Google Scholar
• Díaz-Llopis M, Salom D, Garcia-de-Vicuña C, et al. Treatment of refractory uveitis with adalimumab: a prospective multicenter study of 131 patients. Ophthalmology. 2012;119(8):1575–1581. doi:10.1016/j.ophtha.2012.02.018.
   PubMed Web of Science ®Google Scholar
• Ali A, Ku JH, Suhler EB, Choi D, Rosenbaum JT. The course of retinal vasculitis. Br J Ophthalmol. 2014;98(6):785–789. doi:10.1136/bjophthalmol-2013-303443.
   PubMed Web of Science ®Google Scholar
• Fardet L, Kassar A, Cabane J, Flahault A. Corticosteroid-induced adverse events in adults. Drug Saf. 2007;30(10):861–881. doi:10.2165/00002018-200730100-00005.
   PubMed Web of Science ®Google Scholar
• Namba K, Kaburaki T, Tsuruga H, Ogawa Y, Iwashita E, Goto H. Long-term safety and effectiveness of adalimumab in Japanese patients with noninfectious intermediate, posterior, or panuveitis: post-marketing surveillance of 251 Patients. Ophthalmol Ther. 2022;11(3):1147–1161. doi:10.1007/s40123-022-00493-z.
   PubMed Web of Science ®Google Scholar
• Sonmez HK, Evereklioglu C, Gulmez Sevim D. Prompt and sustained suppression of intraocular inflammation with adalimumab in pediatric patients with non-infectious uveitis resistant to traditional managements: a 6-month follow-up research. Ocul Immunol Inflamm. 2022;1–5. [In Press]. doi:10.1080/09273948.2022.2139274.
   Web of Science ®Google Scholar
• Hatemi G, Christensen R, Bang D, et al. 2018 update of the EULAR recommendations for the management of Behçet’s syndrome. Ann Rheum Dis. 2018;77(6):808–818. doi:10.1136/annrheumdis-2018-213225.
   PubMed Web of Science ®Google Scholar