Efficacy and safety of subcutaneous infliximab versus adalimumab, etanercept and intravenous infliximab in patients with rheumatoid arthritis: a systematic literature review and meta-analysis

References

• Safiri S, Kolahi AA, Hoy D, et al. Global, regional and national burden of rheumatoid arthritis 1990-2017: a systematic analysis of the Global Burden of Disease study 2017. Ann Rheum Dis. 2019;78(11):1463–1471.
   PubMed Web of Science ®Google Scholar
• Guo Q, Wang Y, Xu D, et al. Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone Res. 2018;6:15.
   PubMed Web of Science ®Google Scholar
• Katchamart W, Narongroeknawin P, Chanapai W, et al. Health-related quality of life in patients with rheumatoid arthritis. BMC Rheumatol. 2019;3:34.
   PubMedGoogle Scholar
• Smolen JS, Landewe RBM, Bijlsma JWJ, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2019 update. Ann Rheum Dis. 2020;79(6):685–699.
   PubMed Web of Science ®Google Scholar
• Singh JA, Saag KG, Bridges SL Jr., et al. 2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol. 2016;68(1):1–26.
   PubMed Web of Science ®Google Scholar
• Lau CS, Chia F, Dans L, et al. 2018 update of the APLAR recommendations for treatment of rheumatoid arthritis. Int J Rheum Dis. 2019;22(3):357–375.
   PubMed Web of Science ®Google Scholar
• Brodszky V, Biro A, Szekanecz Z, et al. Determinants of biological drug survival in rheumatoid arthritis: evidence from a Hungarian rheumatology center over 8 years of retrospective data. Clinicoecon Outcomes Res. 2017;9:139–147.
   PubMed Web of Science ®Google Scholar
• Sugiyama N, Kawahito Y, Fujii T, et al. Treatment patterns, direct cost of biologics, and direct medical costs for rheumatoid arthritis patients: A real-world analysis of nationwide Japanese claims data. Clin Ther. 2016;38(6):1359–1375.e1.
   PubMed Web of Science ®Google Scholar
• Silvagni E, Bortoluzzi A, Carrara G, et al. Comparative effectiveness of first-line biological monotherapy use in rheumatoid arthritis: a retrospective analysis of the RECord-linkage On Rheumatic Diseases study on health care administrative databases. BMJ Open. 2018;8(9):e021447.
   PubMed Web of Science ®Google Scholar
• Sullivan E, Kershaw J, Blackburn S, et al. Biologic disease-modifying antirheumatic drug prescription patterns for rheumatoid arthritis among United States physicians. Rheumatol Ther. 2020;7(2):383–400.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. Humira summary of product characteristics [Internet]. 2009 cited 2020 May 26. Available from: https://www.ema.europa.eu/en/documents/product-information/humira-epar-product-information_en.pdf.
   Google Scholar
• European Medicines Agency. Remicade summary of product characteristics [Internet]. 2009 cited 2020 May 26. Available from: https://www.ema.europa.eu/en/documents/product-information/remicade-epar-product-information_en.pdf.
   Google Scholar
• European Medicines Agency. Enbrel summary of product characteristics [Internet]. 2009 cited 2020 May 26. Available from: https://www.ema.europa.eu/en/documents/product-information/enbrel-epar-product-information_en.pdf.
   Google Scholar
• US Food and Drug Administration. Humira prescribing information [Internet]. 2002 cited 2020 May 26. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/125057Orig1s411lbl.pdf.
   Google Scholar
• US Food and Drug Administration. Enbrel prescribing information [Internet]. 2012 cited 2020 May 26. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/103795s5503lbl.pdf.
   Google Scholar
• US Food and Drug Administration. Remicade prescribing information [Internet]. 2013 cited 2020 May 26. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2013/103772s5359lbl.pdf.
   Google Scholar
• European Medicines Agency. European Medicines Agency database [Internet]. 2020 cited 2020 May 26. Available from: https://www.ema.europa.eu/en/medicines.
   Google Scholar
• Favalli EG, Bugatti S, Biggioggero M, et al. Treatment comparison in rheumatoid arthritis: head-to-head trials and innovative study designs. Biomed Res Int. 2014;831603:2014.
   Google Scholar
• Smolen JS, Burmester GR, Combe B, et al. Head-to-head comparison of certolizumab pegol versus adalimumab in rheumatoid arthritis: 2-year efficacy and safety results from the randomised EXXELERATE study. Lancet. 2016;388(10061):2763–2774.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. Remsima summary of product characteristics [Internet]. 2020 cited 2020 Dec 7. Available from: https://www.ema.europa.eu/en/documents/product-information/remsima-epar-product-information_en.pdf.
   Google Scholar
• European Medicines Agency. Assessment report on extension(s) of marketing authorisation: Remsima [Internet]. 2019 cited 2020 Jun 26. Available from: https://www.ema.europa.eu/en/documents/variation-report/remsima-h-c-2576-x-0062-epar-assessment-report-variation_en.pdf.
   Google Scholar
• Westhovens R, Wiland P, Zawadzki M, et al. A novel formulation of CT-P13 for subcutaneous administration: 30 week results from a Part 2 of Phase I/III randomized controlled trial in patients with rheumatoid arthritis [Abstract SAT0170]. Ann Rheum Dis. 2019;78(Suppl 2):1158–1159.
   Google Scholar
• Westhovens R, Wiland P, Zawadzki M, et al. Efficacy, pharmacokinetics and safety of subcutaneous versus intravenous CT-P13 in rheumatoid arthritis: a randomized phase I/III trial. Rheumatology. 2020 Nov 23 [Epub ahead of print]. doi: https://doi.org/10.1093/rheumatology/keaa580.
   Google Scholar
• Combe B, Allanore Y, Alten R, et al. Comparative efficacy of subcutaneous (CT-P13) and intravenous infliximab in adult patients with rheumatoid arthritis: a network meta-regression of individual patient data from two randomised trials. 2020.
   Google Scholar
• McCabe S, Watson J, Rubikaite A. Systematic review of the comparative efficacy of anti-TNFα therapies in rheumatoid arthritis, ulcerative colitis and Crohn’s disease. PROSPERO 2019 CRD42019149621 [Internet]. 2019 cited 2020 May 26. Available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42019149621.
   Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
   PubMed Web of Science ®Google Scholar
• Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med. 1997;127(9):820–826.
   PubMed Web of Science ®Google Scholar
• DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188.
   PubMedGoogle Scholar
• Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22(4):719–748.
   PubMed Web of Science ®Google Scholar
• R Core Team. R: A language and environment for statistical computing [Internet]. 2019 cited 2020 May 26. Available from: https://www.R-project.org/.
   Google Scholar
• Schwarzer G. Meta: An R package for meta-analysis. R News. 2007;7(3):40–45.
   Google Scholar
• National Institute for Health and Care Excellence. NICE technology appraisal submission templates: user guide for submission template (Word). 2018 cited 2020 Aug 9. Available from: https://www.nice.org.uk/about/what-we-do/our-programmes/nice-guidance/nice-technology-appraisal-guidance.
   Google Scholar
• Takeuchi T, Miyasaka N, Tatsuki Y, et al. Baseline tumour necrosis factor alpha levels predict the necessity for dose escalation of infliximab therapy in patients with rheumatoid arthritis. Ann Rheum Dis. 2011;70(7):1208–1215.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Choe JY, Prodanovic N, et al. Comparing biosimilar SB2 with reference infliximab after 54 weeks of a double-blind trial: clinical, structural and safety results. Rheumatology (Oxford). 2017;56(10):1771–1779.
   PubMed Web of Science ®Google Scholar
• Cohen S, Genovese MC, Choy E, et al. Efficacy and safety of the biosimilar ABP 501 compared with adalimumab in patients with moderate to severe rheumatoid arthritis: a randomised, double-blind, phase III equivalence study. Ann Rheum Dis. 2017;76(10):1679–1687.
   PubMed Web of Science ®Google Scholar
• Weinblatt ME, Baranauskaite A, Dokoupilova E, et al. Switching from reference adalimumab to SB5 (adalimumab biosimilar) in patients with rheumatoid arthritis: fifty-two-week phase III randomized study results. Arthritis Rheumatol. 2018;70(6):832–840.
   PubMed Web of Science ®Google Scholar
• Fleischmann RM, Alten R, Pileckyte M, et al. A comparative clinical study of PF-06410293, a candidate adalimumab biosimilar, and adalimumab reference product (Humira®) in the treatment of active rheumatoid arthritis. Arthritis Res Ther. 2018;20(1):178.
   PubMedGoogle Scholar
• Yamanaka H, Ishiguro N, Takeuchi T, et al. Recovery of clinical but not radiographic outcomes by the delayed addition of adalimumab to methotrexate-treated Japanese patients with early rheumatoid arthritis: 52-week results of the HOPEFUL-1 trial. Rheumatology (Oxford). 2014;53(5):904–913.
   PubMed Web of Science ®Google Scholar
• Smolen JS, van der Heijde DM, Keystone EC, et al. Association of joint space narrowing with impairment of physical function and work ability in patients with early rheumatoid arthritis: protection beyond disease control by adalimumab plus methotrexate. Ann Rheum Dis. 2013;72(7):1156–1162.
   PubMed Web of Science ®Google Scholar
• Detert J, Bastian H, Listing J, et al. Induction therapy with adalimumab plus methotrexate for 24 weeks followed by methotrexate monotherapy up to week 48 versus methotrexate therapy alone for DMARD-naive patients with early rheumatoid arthritis: HIT HARD, an investigator-initiated study. Ann Rheum Dis. 2013;72(6):844–850.
   PubMed Web of Science ®Google Scholar
• Kavanaugh A, Fleischmann RM, Emery P, et al. Clinical, functional and radiographic consequences of achieving stable low disease activity and remission with adalimumab plus methotrexate or methotrexate alone in early rheumatoid arthritis: 26-week results from the randomised, controlled OPTIMA study. Ann Rheum Dis. 2013;72(1):64–71.
   PubMed Web of Science ®Google Scholar
• Matucci-Cerinic M, Allanore Y, Kavanaugh A, et al. Efficacy, safety and immunogenicity of GP2015, an etanercept biosimilar, compared with the reference etanercept in patients with moderate-to-severe rheumatoid arthritis: 24-week results from the comparative phase III, randomised, double-blind EQUIRA study. RMD Open. 2018;4(2):e000757.
   PubMed Web of Science ®Google Scholar
• Dougados MR, van der Heijde DM, Brault Y, et al. When to adjust therapy in patients with rheumatoid arthritis after initiation of etanercept plus methotrexate or methotrexate alone: findings from a randomized study (COMET). J Rheumatol. 2014;41(10):1922–1934.
   PubMed Web of Science ®Google Scholar
• Emery P, Vencovsky J, Sylwestrzak A, et al. A phase III randomised, double-blind, parallel-group study comparing SB4 with etanercept reference product in patients with active rheumatoid arthritis despite methotrexate therapy. Ann Rheum Dis. 2017;76(1):51–57.
   PubMed Web of Science ®Google Scholar
• Emery P, Vencovsky J, Sylwestrzak A, et al. Long-term efficacy and safety in patients with rheumatoid arthritis continuing on SB4 or switching from reference etanercept to SB4. Ann Rheum Dis. 2017;76(12):1986–1991.
   PubMed Web of Science ®Google Scholar
• Yamanaka H, Nagaoka S, Lee SK, et al. Discontinuation of etanercept after achievement of sustained remission in patients with rheumatoid arthritis who initially had moderate disease activity-results from the ENCOURAGE study, a prospective, international, multicenter randomized study. Mod Rheumatol. 2016;26(5):651–661.
   PubMed Web of Science ®Google Scholar
• Matsuno H, Matsubara T. A randomized double-blind parallel-group phase III study to compare the efficacy and safety of NI-071 and infliximab reference product in Japanese patients with active rheumatoid arthritis refractory to methotrexate. Mod Rheumatol. 2019;29(6):919–927.
   PubMed Web of Science ®Google Scholar
• Choe JY, Prodanovic N, Niebrzydowski J, et al. A randomised, double-blind, phase III study comparing SB2, an infliximab biosimilar, to the infliximab reference product Remicade in patients with moderate to severe rheumatoid arthritis despite methotrexate therapy. Ann Rheum Dis. 2017;76(1):58–64.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Choe JY, Prodanovic N, et al. Safety, immunogenicity and efficacy after switching from reference infliximab to biosimilar SB2 compared with continuing reference infliximab and SB2 in patients with rheumatoid arthritis: results of a randomised, double-blind, phase III transition study. Ann Rheum Dis. 2018;77(2):234–240.
   PubMed Web of Science ®Google Scholar
• Alten R, Batko B, Hala T, et al. Randomised, double-blind, phase III study comparing the infliximab biosimilar, PF-06438179/GP1111, with reference infliximab: efficacy, safety and immunogenicity from week 30 to week 54. RMD Open. 2019;5(1):e000876.
   PubMed Web of Science ®Google Scholar
• Cohen SB, Alten R, Kameda H, et al. A randomized controlled trial comparing PF-06438179/GP1111 (an infliximab biosimilar) and infliximab reference product for treatment of moderate to severe active rheumatoid arthritis despite methotrexate therapy. Arthritis Res Ther. 2018;20(1):155.
   PubMedGoogle Scholar
• Yoo DH, Hrycaj P, Miranda P, et al. A randomised, double-blind, parallel-group study to demonstrate equivalence in efficacy and safety of CT-P13 compared with innovator infliximab when coadministered with methotrexate in patients with active rheumatoid arthritis: the PLANETRA study. Ann Rheum Dis. 2013;72(10):1613–1620.
   PubMed Web of Science ®Google Scholar
• Yoo DH, Racewicz A, Brzezicki J, et al. A phase III randomized study to evaluate the efficacy and safety of CT-P13 compared with reference infliximab in patients with active rheumatoid arthritis: 54-week results from the PLANETRA study. Arthritis Res Ther. 2016;18:82.
   PubMed Web of Science ®Google Scholar
• Takeuchi T, Yamanaka H, Tanaka Y, et al. Evaluation of the pharmacokinetic equivalence and 54-week efficacy and safety of CT-P13 and innovator infliximab in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2015;25(6):817–824.
   PubMed Web of Science ®Google Scholar
• Kim J, Ryu H, Yoo DH, et al. A clinical trial and extension study of infliximab in Korean patients with active rheumatoid arthritis despite methotrexate treatment. J Korean Med Sci. 2013;28(12):1716–1722.
   PubMed Web of Science ®Google Scholar
• Takeuchi T, Miyasaka N, Inoue K, et al. Impact of trough serum level on radiographic and clinical response to infliximab plus methotrexate in patients with rheumatoid arthritis: results from the RISING study. Mod Rheumatol. 2009;19(5):478–487.
   Web of Science ®Google Scholar
• Weinblatt ME, Baranauskaite A, Niebrzydowski J, et al. Phase III randomized study of SB5, an adalimumab biosimilar, versus reference adalimumab in patients with moderate-to-severe rheumatoid arthritis. Arthritis Rheumatol. 2018;70(1):40–48.
   PubMed Web of Science ®Google Scholar
• Cohen SB, Alonso-Ruiz A, Klimiuk PA, et al. Similar efficacy, safety and immunogenicity of adalimumab biosimilar BI 695501 and Humira reference product in patients with moderately to severely active rheumatoid arthritis: results from the phase III randomised VOLTAIRE-RA equivalence study. Ann Rheum Dis. 2018;77(6):914–921.
   PubMed Web of Science ®Google Scholar
• Edwards CJ, Monnet J, Ullmann M, et al. Safety of adalimumab biosimilar MSB11022 (acetate-buffered formulation) in patients with moderately-to-severely active rheumatoid arthritis. Clin Rheumatol. 2019;38(12):3381–3390.
   PubMed Web of Science ®Google Scholar
• Taylor PC, Keystone EC, van der Heijde D, et al. Baricitinib versus placebo or adalimumab in rheumatoid arthritis. N Engl J Med. 2017;376(7):652–662.
   PubMed Web of Science ®Google Scholar
• Emery P, Vencovsky J, Sylwestrzak A, et al. 52-week results of the phase 3 randomized study comparing SB4 with reference etanercept in patients with active rheumatoid arthritis. Rheumatology (Oxford). 2017;56(12):2093–2101.
   PubMed Web of Science ®Google Scholar
• Matsuno H, Tomomitsu M, Hagino A, et al. Phase III, multicentre, double-blind, randomised, parallel-group study to evaluate the similarities between LBEC0101 and etanercept reference product in terms of efficacy and safety in patients with active rheumatoid arthritis inadequately responding to methotrexate. Ann Rheum Dis. 2018;77(4):488–494.
   PubMed Web of Science ®Google Scholar
• Bae SC, Kim J, Choe JY, et al. A phase III, multicentre, randomised, double-blind, active-controlled, parallel-group trial comparing safety and efficacy of HD203, with innovator etanercept, in combination with methotrexate, in patients with rheumatoid arthritis: the HERA study. Ann Rheum Dis. 2017;76(1):65–71.
   PubMed Web of Science ®Google Scholar
• Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988;31(3):315–324.
   PubMed Web of Science ®Google Scholar
• Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62(9):2569–2581.
   PubMed Web of Science ®Google Scholar
• Graudal N, Kaas-Hansen BS, Guski L, et al. Different original and biosimilar TNF inhibitors similarly reduce joint destruction in rheumatoid arthritis–A network meta-analysis of 36 randomized controlled trials. Int J Mol Sci. 2019;20(18):4350.
   Web of Science ®Google Scholar
• Aaltonen KJ, Virkki LM, Malmivaara A, et al. Systematic review and meta-analysis of the efficacy and safety of existing TNF blocking agents in treatment of rheumatoid arthritis. PLoS One. 2012;7(1):e30275.
   PubMed Web of Science ®Google Scholar
• Wolbink GJ, Voskuyl AE, Lems WF, et al. Relationship between serum trough infliximab levels, pretreatment C reactive protein levels, and clinical response to infliximab treatment in patients with rheumatoid arthritis. Ann Rheum Dis. 2005;64(5):704–707.
   Google Scholar
• Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions, version 6.0 [Internet]. 2019 cited 2020 May 26. Available from: https://training.cochrane.org/cochrane-handbook-systematic-reviews-interventions.
   Google Scholar
• Kravvariti E, Kitas GD, Mitsikostas DD, et al. Nocebos in rheumatology: emerging concepts and their implications for clinical practice. Nat Rev Rheumatol. 2018;14(12):727–740.
   PubMed Web of Science ®Google Scholar