Biological Therapies for Rheumatoid Arthritis: An Overview for the Clinician

References

• Aletaha D, Smolen J. Diagnosis and management of rheumatoid arthritis: a review. JAMA. 2018;320(13):1360–1372. doi:10.1001/jama.2018.13103
   PubMed Web of Science ®Google Scholar
• Crowson CS, Rollefstad S, Ikdahl E, et al. Impact of risk factors associated with cardiovascular outcomes in patients with rheumatoid arthritis. Ann Rheum Dis. 2018;77(1):48–54. doi:10.1136/annrheumdis-2017-211735
   PubMed Web of Science ®Google Scholar
• Almutair K, Nossent J, Preen D, Keen H, Inderjeeth C. The global prevalence of rheumatoid arthritis: a meta-analysis based on a systematic review. Rheumatol Int. 2021;41(5):863–877. doi:10.1007/s00296-020-04731-0
   Web of Science ®Google Scholar
• Smolen J, Aaletaha D, Barton A, et al. Rheumatoid arthritis. Nat Rev Dis Primers. 2018;4:18001. doi:10.1038/nrdp.2018.1
   PubMed Web of Science ®Google Scholar
• Brennan FM, Maini RN, Feldmann M. TNF alpha – a pivotal role in rheumatoid arthritis? Br J Rheumtol. 1992;31(5):293. doi:10.1093/rheumatology/31.5.293
   Google Scholar
• Keystone E, Genovese M, Klareskog L, et al. Golimumab, a human antibody to tumour necrosis factor {alpha} given by monthly subcutaneous injections, in active rheumatoid arthritis despite methotrexate therapy: the GO‐FORWARD Study. Ann Rheum Dis. 2009;68(6):789–796. doi:10.1136/ard.2008.099010
   PubMed Web of Science ®Google Scholar
• Maini R, St Clair E, Breedveld F, et al. Infliximab (chimeric anti‐tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomized Phase III trial. Lancet. 1999;354(9194):1932–1939. doi:10.1016/s0140-6736(99)05246-0
   PubMed Web of Science ®Google Scholar
• Keystone E, Kavanaugh A, Sharp J, et al. Radiographic, clinical, and functional outcomes of treatment with Adalimumab (a human anti‐tumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy. A randomized, placebo‐controlled, 52‐week trial. Arthritis Rheum. 2004;50(5):1400–1411. doi:10.1002/art.20217
   PubMed Web of Science ®Google Scholar
• Keystone E, van der Heijde D, Mason D, et al. Certolizumab pegol plus methotrexate is significantly more effective than placebo plus methotrexate in active rheumatoid arthritis: findings of a fifty-two–week, Phase III, multicenter, randomized, double-blind, placebo-controlled, parallel-group study. Arthritis Rheum. 2008;58(11):3319–3329. doi:10.1002/art.23964
   PubMed Web of Science ®Google Scholar
• Weinblatt M, Kremer J, Bankhurst A, et al. A trial of etanercept, a recombinant tumour necrosis factor receptor: fcfusion protein, in patients with rheumatoid arthritis receiving methotrexate. N Engl J Med. 1999;340(4):253‐259. doi:10.1056/NEJM199901283400401
   Web of Science ®Google Scholar
• Breedveld FC, Weisman MH, Kavanaugh AF, et al. The PREMIER study—a multicenter, randomized, double-blind clinical trial of combination therapy with adalimumab plus methotrexate versus methotrexate alone or adalimumab alone in patients with early, aggressive rheumatoid arthritis who had not had previous methotrexate treatment. Arthritis Rheum. 2006;54(1):26–37. doi:10.1002/art.21519
   PubMed Web of Science ®Google Scholar
• Smolen JS, Kay J, Doyle MK, et al. Golimumab in patients with active rheumatoid arthritis after treatment with tumour necrosis factor alpha inhibitors (GO‐AFTER study): a multicentre, randomised, double‐blind, placebo‐controlled, phase III trial. Lancet. 2009;374(9685):210–221. doi:10.1016/S0140-6736(09)60506-7
   PubMed Web of Science ®Google Scholar
• Gottenberg JE, Brocq O, Perdriger A, et al. Non-TNF-targeted biologic vs a second anti-TNF drug to treat rheumatoid arthritis in patients with insufficient response to a first anti-TNF drug: a randomized clinical trial. JAMA. 2016;316(11):1172–1180. doi:10.1001/jama.2016.13512
   PubMed Web of Science ®Google Scholar
• Fraenkel L, Bathon J, England B, et al. 2021 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Care Res. 2021;73(7):924–939. doi:10.1002/acr.24596
   PubMed Web of Science ®Google Scholar
• Dubois E, Cohen A. Abatacept. Br J Clin Pharmacol. 2009;68(4):480–481. doi:10.1111/j.1365-2125.2009.03502.x
   Web of Science ®Google Scholar
• Westhovens R, Robles M, Zimenes AC, et al. Clinical efficacy and safety of abatacept in methotrexate-naive patients with early rheumatoid arthritis and poor prognostic factors. Ann Rheum Dis. 2009;68(12):1870–1877. doi:10.1136/ard.2008.101121
   PubMed Web of Science ®Google Scholar
• Kremer K, Genant H, Moreland L, et al. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann Intern Med. 2006;144(12):865–876. doi:10.7326/0003-4819-144-12-200606200-00003
   PubMed Web of Science ®Google Scholar
• Schiff M, Keiserman M, Codding C, et al. Efficacy and safety of abatacept or infliximab vs placebo in ATTEST: a phase III, multi-centre, randomised, double-blind, placebo-controlled study in patients with rheumatoid arthritis and an inadequate response to methotrexate. Ann Rheum Dis. 2008;67(8):1096–1103. doi:10.1136/ard.2007.080002
   PubMed Web of Science ®Google Scholar
• Genovese MC, Becker JC, Schiff M, et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med. 2005;353(11):1114–1123. doi:10.1056/NEJMoa050524
   PubMed Web of Science ®Google Scholar
• Burmester GR, Rigby WF, van Vollenhoven RF, et al. Tocilizumab in early progressive rheumatoid arthritis: FUNCTION, a randomised controlled trial. Ann Rheum Dis. 2015;75(6):1081–1091. doi:10.1136/annrheumdis-2015-207628
   Web of Science ®Google Scholar
• Emery P, Keystone E, Tony HP, et al. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis. 2008;67(11):1516–1523. doi:10.1136/ard.2008.09293
   PubMed Web of Science ®Google Scholar
• Gabay C, Emery P, van Vollenhoven R, et al. Tocilizumab monotherapy versus adalimumab monotherapy for treatment of rheumatoid arthritis (ADACTA): a randomised, double-blind, controlled Phase 4 trial. Lancet. 2013;381(9877):1541–1550. doi:10.1016/S0140-6736(13)60250-0
   PubMed Web of Science ®Google Scholar
• Burmester GR, Lin Y, Patel R, et al. Efficacy and safety of sarilumab monotherapy versus adalimumab monotherapy for the treatment of patients with active rheumatoid arthritis (MONARCH): a randomised, double-blind, parallel-group phase III trial. Ann Rheum Dis. 2017;76(5):840–847. doi:10.1136/annrheumdis-2016-210310
   PubMed Web of Science ®Google Scholar
• Vershueren P, Emery P, van Hoogstraten H, et al. Efficacy of sarilumab in patients with rheumatoid arthritis with and without previous response to tocilizumab. Ann Rheum Dis. 2018;77(supp 2):327–328. doi:10.1136/annrheumdis-2018-eular.1376
   Web of Science ®Google Scholar
• Porter D, van Melckebeke J, Dale J, et al. Tumour necrosis factor inhibition versus rituximab for patients with rheumatoid arthritis who require biological treatment (ORBIT): an open-label, randomised controlled, non-inferiority, trial. Lancet. 2016;18(388):239–247. doi:10.1016/S0140-6736(16)00380-9
   Web of Science ®Google Scholar
• Emery P, Gottenberg JE, Rubbert-Roth A, et al. Rituximab versus an alternative TNF inhibitor in patients with rheumatoid arthritis who failed to respond to a single previous TNF inhibitor: SWITCH-RA, a global, observational, comparative effectiveness study. Ann Rheum Dis. 2015;74(6):979–984. doi:10.1136/annrheumdis-2013-203993
   PubMed Web of Science ®Google Scholar
• Merten M, Singh J. Anakinra for rheumatoid arthritis. Cochrane Database Syst Rev. 2009. doi:10.1002/14651858.CD005121.pub3
   Web of Science ®Google Scholar
• Smolen J, Goncalves J, Quinn M, Benedetti F, Lee JY. Era of biosimilars in rheumatology: reshaping the healthcare environment. RMD Open. 2019;5(1):e000900. doi:10.1136/rmdopen-2019-000900
   PubMed Web of Science ®Google Scholar
• Feagan BG, Marabani M, Wu JJ, Facacin F, Spronk C, Castaneda-Hernandez G. The challenges of switching therapies in an evolving multiple biosimilars landscape: a narrative review of current evidence. Adv Ther. 2020;37(11):4491–4518. doi:10.1007/s12325-020-01472-1
   PubMed Web of Science ®Google Scholar
• Van Vollenhoven RF, Fleischmann R, Cohen S, et al. Tofacitinib or adalimumab versus placebo in rheumatoid arthritis. N Engl J Med. 2012;367(6):508–519. doi:10.1056/NEJMoa1112072
   PubMed Web of Science ®Google Scholar
• Ramiro S, Gaujoux-Viala C, Nam JL, et al. Safety of synthetic and biological DMARDs: a systematic literature review informing the 2013 update of the EULAR recommendations for management of rheumatoid arthritis. Ann Rheum Dis. 2014;73(3):529–535. doi:10.1136/annrheumdis-2013-204575
   PubMed Web of Science ®Google Scholar
• Ehlers S. Role of tumour necrosis factor (TNF) in host defence against tuberculosis: implications for immunotherapies targeting TNF. Ann Rheum Dis. 2003;62(2):37–42. doi:10.1136/ard.62.suppl_2.ii37
   Web of Science ®Google Scholar
• Listing J, Gerhold K, Zink A. The risk of infection associated with rheumatoid arthritis, with its comorbidity and treatment. Rheumatology. 2012;51(1):53–61. doi:10.1093/rheumatology/kes305
   Web of Science ®Google Scholar
• Askling J, Fored CM, Brandt L, et al. Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum. 2005;53(7):1986–1992. doi:10.1002/art.21137
   Web of Science ®Google Scholar
• Dixon WG, Hyrich KL, Watson KD, et al. Drug-specific risk of tuberculosis in patients with rheumatoid arthritis treated with anti-TNF therapy: results from the British Society for Rheumatology Biologics Register (BSRBR). Ann Rheum Dis. 2010;69(3):522–528. doi:10.1136/ard.2009.118935
   PubMed Web of Science ®Google Scholar
• Mitka M. FDA: increased HBV reactivation risk with ofatumumb or rituximab. JAMA. 2012;310(16):1664. doi:10.1001/jama.2013.281115
   Web of Science ®Google Scholar
• Clifford DB, Ances B, Costello C, et al. Rituximab-associated progressive multifocal leukoencephalopathy in rheumatoid arthritis. Arch Neurol. 2001;68(9):1156–1164. doi:10.1001/archneurol.2011.103
   Google Scholar
• Chen SK, Liao KP, Liu J, Kim SC. Risk of hospitalized infection and initiation of abatacept versus tumor necrosis factor inhibitors among patients with rheumatoid arthritis: a propensity score-matched cohort study. Arthritis Care Res. 2020;72(1):9–17. doi:10.1002/acr.23824
   Web of Science ®Google Scholar
• Holroyd CR, Seth R, Bukhari M, et al. The British Society for Rheumatology biologic DMARD safety guidelines in inflammatory arthritis. Rheumatology. 2019;58(2):e3–e42. doi:10.1093/rheumatology/key208
   PubMed Web of Science ®Google Scholar
• Mercer LK, Askling J, Raaschou P, et al. Risk of invasive melanoma in patients with rheumatoid arthritis treated with biologics: results from a collaborative project of 11 European biologic registries. Ann Rheum Dis. 2017;76(2):386–391. doi:10.1136/annrheumdis-2016-209285
   PubMed Web of Science ®Google Scholar
• Wang KL, Yin WJ, Zhou LY, et al. Risk of non-melanoma skin cancer for rheumatoid arthritis patients receiving TNF antagonist: a systematic review and meta-analysis. Clin Rheumatol. 2020;39(3):769–778. doi:10.1007/s10067-019-04865-y
   PubMed Web of Science ®Google Scholar
• Chatzidionysiou K, Delcoigne B, Frisell T, et al. How do we use biologics in rheumatoid arthritis patients with a history of malignancy? An assessment of treatment patterns using Scandinavian registers. RMD Open. 2020;6(2):e001363. doi:10.1136/rmdopen-2020-001363
   Web of Science ®Google Scholar
• Regierer AC, Strangfeld A. Rheumatoid arthritis treatment in patients with a history of cancer. Curr Opin Rheumatol. 2018;30(3):288–294. doi:10.1097/BOR.0000000000000492
   Web of Science ®Google Scholar
• Pappas D, Rebello S, Liu M, et al. Therapy with biologic agents after diagnosis of solid malignancies: results from the corrona registry. J Rheumatol. 2019;46(11):1438–1444. doi:10.3899/jrheum.171457
   Web of Science ®Google Scholar
• Brahmer JR, Lacchetti C, Schneider BJ, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinic practice guideline. J Clin Oncol. 2018;36(17):1714–1768. doi:10.1200/JCO.2017.77.6385
   PubMed Web of Science ®Google Scholar
• Chen AY, Wolchok JD, Bass AR. TNF in the era of immune checkpoint inhibitors: friend or foe? Nat Rev Rheumatol. 2021;17(4):213–223. doi:10.1038/s41584-021-00584-4
   PubMed Web of Science ®Google Scholar
• Mohan N, Edwards ET, Cupps TR, et al. Demyelination occurring during anti-tumor necrosis factor alpha therapy for inflammatory arthritides. Arthritis Rheum. 2001;44(12):2862–2869. doi:10.1002/1529-0131(200112)44:12<2862::aid-art474>3.0.co;2-w
   PubMed Web of Science ®Google Scholar
• Kwon HJ, Cote TR, Cuffe MS, Kramer JM, Braun MM. Case reports of heart failure after therapy with a tumor necrosis factor antagonist. Ann Intern Med. 2003;138(10):807–811. doi:10.7326/0003-4819-138-10-200305200-00008
   PubMed Web of Science ®Google Scholar
• Strangfeld A, Richter A, Siegmund B, et al. Risk for lower intestinal perforations in patients with rheumatoid arthritis treated with tocilizumab in comparison to treatment with other biologic or conventional synthetic DMARDs. Ann Rheum Dis. 2017;76(3):504–510. doi:10.1136/annrheumdis-2016-209773
   PubMed Web of Science ®Google Scholar
• Smolen JS, Landewe RB, Bijlsma JW, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2019 update. Ann Rheum Dis. 2019;79(6):685–699. doi:10.1136/annrheumdis-2019-216655
   Web of Science ®Google Scholar
• Bykerk VP, Massarotti EM. The new ACR/EULAR remission criteria: rationale for developing new criteria for remission. Rheumatology. 2012;51(supp6):vi16–vi20. doi:10.1093/rheumatology/kes281
   Web of Science ®Google Scholar
• Schaeverbeke T, Truchetet ME, Kostine M, Barnetche T, Bannwarth B, Richez C. Immunogenicity of biologic agents in rheumatoid arthritis patients: lessons for clinical practice. Rheumatology. 2016;55(2):210–220. doi:10.1093/rheumatology/kev277
   PubMed Web of Science ®Google Scholar
• Skorpen CG, Hoeltzenbein M, Rincani A, et al. The EULAR points to consider for use of antirheumatic drugs before pregnancy, and during pregnancy and lactation. Ann Rheum Dis. 2015;75(5):795–810. doi:10.1136/annrheumdis-2015-208840
   Web of Science ®Google Scholar
• Mariette X, Forger F, Abraham B, et al. Lack of placental transfer of certolizumab pegol during pregnancy: results from CRIB, a prospective, postmarketing, pharmacokinetic study. Ann Rheum Dis. 2017;77(2):228–233. doi:10.1136/annrheumdis-2017-212196
   Web of Science ®Google Scholar
• Monti S, Balduzzi S, Delvino P, Bellis E, Quadrelli VS, Montecucco C. Clinical course of COVID-19 in a series of patients with chronic arthritis treated with immunosuppressive targeted therapies. Ann Rheum Dis. 2020;79(5):667–668. doi:10.1136/annrheumdis-2020-217424
   PubMed Web of Science ®Google Scholar
• Conticini E, Bargagli E, Bardelli M, et al. COVID-19 pneumonia in a large cohort of patients treated with biological and targeted synthetic antirheumatic drugs. Ann Rheum Dis. 2021;80(2):e14. doi:10.1136/annrheumdis-2020-217681
   Web of Science ®Google Scholar
• Haberman R, Axelrad J, Chen A, et al. COVID-19 in immune-mediated inflammatory diseases - case series from New York. N Engl J Med. 2020;383(1):85–88. doi:10.1056/NEJMc2009567
   PubMed Web of Science ®Google Scholar
• Gianfrancesco M, Hyrich KL, Al-Adely S, et al. Characteristics associated with hospitalisation for COVID-19 in people with rheumatic disease: data from the COVID-19 global rheumatology alliance physician-reported registry. Ann Rheum Dis. 2020;79(7):859–866. doi:10.1136/annrheumdis-2020-217871
   PubMed Web of Science ®Google Scholar
• Damiani G, Pacifico A, Bragazzi NL, Malagoli P. Biologics increase the risk of SARS-CoV-2 infection and hospitalization, but not ICU admission and death: real-life data from a large cohort during red-zone declaration. Dermatol Ther. 2020;33(5):e13475. doi:10.1111/dth.13475
   PubMed Web of Science ®Google Scholar
• Mikuls TR, Johnson SR, Fraenkel L, et al. American College of Rheumatology guidance for the management of rheumatic disease in adult patients during the COVID-19 pandemic: version 3. Arthritis Rheumatol. 2021;73(2):e1–e12. doi:10.1002/art.41596
   Web of Science ®Google Scholar
• RECOVERY Collaborative Group. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): a randomized, controlled, open-label, platform trial. Lancet. 2021;397(10285):1637–1645. doi:10.1016/S0140-6736(21)00676-0.
   PubMed Web of Science ®Google Scholar
• Curtis JR, Johnson SR, Anthony DD, et al. American College of Rheumatology guidance for COVID-19 vaccination in patients with rheumatic and musculoskeletal diseases: version 1. Arthritis Rheumatol. 2021;73(7):1093–1107. doi:10.1002/art.41734
   PubMed Web of Science ®Google Scholar
• Youssef P, Marcal B, Button P, et al. Reasons for biologic and targeted synthetic disease-modifying antirheumatic drug cessation and persistence of second-line treatment in a rheumatoid arthritis dataset. J Rheumatol. 2020;47(8):1174–1181. doi:10.3899/jrheum.190535
   PubMed Web of Science ®Google Scholar
• Ebina K, Hirano T, Maeda Y, et al. Drug retention of 7 biologics and tofacitinib in biologics-naïve and biologics-switched patients with rheumatoid arthritis: the ANSWER cohort study. Arthritis Res Ther. 2020;22(1):142. doi:10.1186/s13075-020-02232-w
   Web of Science ®Google Scholar
• Movaahedi M, Couta S, Cesta C, et al. Time to discontinuation of biologic therapy by mechanism of action in rheumatoid arthritis: results from the Ontario best practice research initiative (OBRI) cohort. Ann Rheum Dis. 2018;77(supp 2):958. doi:10.1136/annrheumdis-2018-eular.2131
   Web of Science ®Google Scholar
• Blaess J, Walther J, Petitdemange A, et al. Immunosuppressive agents for rheumatoid arthritis: a systematic review of clinical trials and their current development stage. Ther Adv Musculoskelet Dis. 2020;12:1759720X20959971. doi:10.1177/1759720X20959971
   Web of Science ®Google Scholar
• Emery P, Fleischmann R, Filipowicz-Sosnowska A, et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 2006;54(5):1390–1400. doi:10.1002/art.21778
   PubMed Web of Science ®Google Scholar
• Cohen S, Emery P, Greenwald M, et al. Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum. 2006;54(9):2793–2806. doi:10.1002/art.22025
   PubMed Web of Science ®Google Scholar
• Gary M.H. Misan. Australian Medicines Handbook 2020. Adelaide: Australian Medicines Handbook Pty Ltd; July, 2020. Available from https://amhonline.amh.net.au/. Accessed August 3, 2021.
   Google Scholar