196
Views
0
CrossRef citations to date
0
Altmetric
Review

Patient-Reported Outcomes in Rheumatoid Arthritis: A Key Consideration for Evaluating Biosimilar Uptake?

ORCID Icon
Pages 79-95 | Published online: 30 Mar 2022

References

  • Uhlig T, Moe RH, Kvien TK. The burden of disease in rheumatoid arthritis. Pharmacoeconomics. 2014;32:841–851. doi:10.1007/s40273-014-0174-6
  • Codreanu C, Popescu CC, Mogosan C, et al. Efficacy and safety of original and biosimilar etanercept (SB4) in active rheumatoid arthritis - A comparison in a real-world national cohort. Biologicals. 2019;62:27–32. doi:10.1016/j.biologicals.2019.10.009
  • Elliott MJ, Feldmann M, Maini RN. TNF alpha blockade in rheumatoid arthritis: rationale, clinical outcomes and mechanisms of action. Int J Immunopharmacol. 1995;17:141–145. doi:10.1016/0192-0561(94)00092-3
  • Tanaka Y, Hirata S, Saleem B, Emery P. Discontinuation of biologics in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2013;31:S22–27.
  • Edwards CJ, Galeazzi M, Bellinvia S, Ringer A, Dimitroulas T, Kitas G. Can we wean patients with inflammatory arthritis from biological therapies? Autoimmun Rev. 2019;18:102399. doi:10.1016/j.autrev.2019.102399
  • Boccia R, Jacobs I, Popovian R, de Lima Lopes G. Can biosimilars help achieve the goals of US health care reform? Cancer Manag Res. 2017;9:197–205. doi:10.2147/CMAR.S133442
  • Stebbing J, Mainwaring PN, Curigliano G, et al. Understanding the role of comparative clinical studies in the development of oncology biosimilars. J Clin Oncol. 2020;38:1070–1080. doi:10.1200/JCO.19.02953
  • Cohen HP, Blauvelt A, Rifkin RM, Danese S, Gokhale SB, Woollett G. Switching reference medicines to biosimilars: a systematic literature review of clinical outcomes. Drugs. 2018;78:463–478. doi:10.1007/s40265-018-0881-y
  • Mallam N, Byalakere-Rudraiah CS, Rudraswamy S. Generic drugs: current status and future potential. J Gene Med. 2017;13:1–6.
  • Choy EH, Kingsley GH, Panayi GS. Monoclonal antibody therapy in rheumatoid arthritis. Br J Rheumatol. 1998;37:484–490. doi:10.1093/Rheumatology/37.5.484
  • Rezk MF, Pieper B. Unlocking the value of anti-TNF biosimilars: reducing disease burden and improving outcomes in chronic immune-mediated inflammatory diseases: a narrative review. Adv Ther. 2020;37:3732–3745. doi:10.1007/s12325-020-01437-4
  • O’Callaghan J, Barry SP, Bermingham M, Morris JM, Griffin BT. Regulation of biosimilar medicines and current perspectives on interchangeability and policy. Eur J Clin Pharmacol. 2019;75:1–11. doi:10.1007/s00228-018-2542-1
  • Jin J, Chang Y, Wei W. Clinical application and evaluation of anti-TNF-alpha agents for the treatment of rheumatoid arthritis. Acta Pharmacol Sin. 2010;31:1133–1140. doi:10.1038/aps.2010.134
  • Mehta P, Manson JJ. What is the clinical relevance of TNF inhibitor immunogenicity in the management of patients with rheumatoid arthritis? Front Immunol. 2020;11:589. doi:10.3389/fimmu.2020.00589
  • Ramirez-Herraiz E, Escudero-Vilaplana V, Alanon-Plaza E, et al. Efficiency of Adalimumab, etanercept and infliximab in rheumatoid arthritis patients: dosing patterns and effectiveness in daily clinical practice. Clin Exp Rheumatol. 2013;31:559–565.
  • Kievit W, Fransen J, Adang EM, et al. Long-term effectiveness and safety of TNF-blocking agents in daily clinical practice: results from the Dutch Rheumatoid Arthritis Monitoring register. Rheumatology. 2011;50:196–203. doi:10.1093/rheumatology/keq325
  • Arora A, Mahajan A, Spurden D, Boyd H, Porter D. Long-term drug survival of TNF inhibitor therapy in RA patients: a systematic review of European National Drug Registers. Int J Rheumatol. 2013;2013:764518. doi:10.1155/2013/764518
  • Araujo F, Goncalves J, Fonseca JE. Biosimilar DMARDs: what does the future hold? Drugs. 2016;76:629–637. doi:10.1007/s40265-016-0556-5
  • Moorkens E, Simoens S, Troein P, Declerck P, Vulto AG, Huys I. Different policy measures and practices between Swedish counties influence market dynamics: part 2-biosimilar and originator etanercept in the outpatient setting. BioDrugs. 2019;33:299–306. doi:10.1007/s40259-019-00346-5
  • Chew C, Aguiar M, Bansback N, Law MR, Harrison M. Patient perspectives on the British Columbia Biosimilars Initiative: a qualitative descriptive study. Rheumatol Int. 2021. doi:10.1007/s00296-021-04874-8
  • Castaneda-Hernandez G, Szekanecz Z, Mysler E, et al. Biopharmaceuticals for rheumatic diseases in Latin America, Europe, Russia, and India: innovators, biosimilars, and intended copies. Joint Bone Spine. 2014;81:471–477. doi:10.1016/j.jbspin.2014.03.019
  • Kim TH, Lee SS, Park W, et al. A 5-year retrospective analysis of drug survival, safety, and effectiveness of the infliximab biosimilar CT-P13 in patients with rheumatoid arthritis and ankylosing spondylitis. Clin Drug Investig. 2020;40:541–553. doi:10.1007/s40261-020-00907-5
  • Blackstone EA, Joseph PF. The economics of biosimilars. Am Health Drug Benefits. 2013;6:469–478.
  • Jensen TB, Bartels D, Saedder EA, et al. The Danish model for the quick and safe implementation of infliximab and etanercept biosimilars. Eur J Clin Pharmacol. 2020;76:35–40. doi:10.1007/s00228-019-02765-3
  • Farhat F, Othman A, El Karak F, Kattan J. Review and results of a survey about biosimilars prescription and challenges in the Middle East and North Africa region. Springerplus. 2016;5:2113. doi:10.1186/s40064-016-3779-8
  • Kim H, Alten R, Avedano L, et al. The future of biosimilars: maximizing benefits across immune-mediated inflammatory diseases. Drugs. 2020;80:99–113. doi:10.1007/s40265-020-01256-5
  • Nabhan C, Valley A, Feinberg BA. Barriers to oncology biosimilars uptake in the United States. Oncologist. 2018;23:1261–1265. doi:10.1634/theoncologist.2018-0066
  • Bellinvia S, Cummings JRF, Ardern-Jones MR, Edwards CJ. Adalimumab biosimilars in Europe: an overview of the clinical evidence. BioDrugs. 2019;33:241–253. doi:10.1007/s40259-019-00355-4
  • 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:e000876. doi:10.1136/rmdopen-2018-000876
  • Dutta B, Huys I, Vulto AG, Simoens S. Identifying key benefits in European off-patent biologics and biosimilar markets: it is not only about price! BioDrugs. 2020;34:159–170. doi:10.1007/s40259-019-00395-w
  • Afzali A, Furtner D, Melsheimer R, Molloy PJ. The automatic substitution of biosimilars: definitions of interchangeability are not interchangeable. Adv Ther. 2021;38:2077–2093. doi:10.1007/s12325-021-01688-9
  • Lobo F, Rio-Alvarez I. Barriers to biosimilar prescribing incentives in the context of clinical governance in Spain. Pharmaceuticals. 2021;14:283. doi:10.3390/ph14030283
  • Nabi H, Georgiadis S, Loft AG, et al. Comparative effectiveness of two Adalimumab biosimilars in 1318 real-world patients with inflammatory rheumatic disease mandated to switch from originator Adalimumab: nationwide observational study emulating a randomised clinical trial. Ann Rheum Dis. 2021;80:1400–1409. doi:10.1136/annrheumdis-2021-219951
  • Allocati E, Bertele V, Gerardi C, Garattini S, Banzi R. Clinical evidence supporting the marketing authorization of biosimilars in Europe. Eur J Clin Pharmacol. 2020;76:557–566. doi:10.1007/s00228-019-02805-y
  • El Zorkany B, Al Ani N, Al Emadi S, et al. Biosimilars in rheumatology: recommendations for regulation and use in Middle Eastern countries. Clin Rheumatol. 2018;37:1143–1152. doi:10.1007/s10067-018-3982-9
  • Chau J, Delate T, Ota T, Bhardwaja B. Patient perspectives on switching from infliximab to infliximab-dyyb in patients with rheumatologic diseases in the United States. ACR Open Rheumatol. 2019;1:52–57. doi:10.1002/acr2.1007
  • Bhat S, Limdi JK, Cross RK, Farraye FA. Does similarity breed contempt? A review of the use of biosimilars in inflammatory bowel disease. Dig Dis Sci. 2021;66:2513–2532. doi:10.1007/s10620-021-07114-y
  • Gasteiger C, Lobo M, Dalbeth N, Petrie KJ. Patients’ beliefs and behaviours are associated with perceptions of safety and concerns in a hypothetical biosimilar switch. Rheumatol Int. 2021;41:163–171. doi:10.1007/s00296-020-04576-7
  • Chan SJ, Yeo HY, Stamp LK, Treharne GJ, Marra CA. What are the preferences of patients with rheumatoid arthritis for treatment modification? A scoping review. Patient. 2021;14:505–532. doi:10.1007/s40271-020-00488-7
  • Mercieca-Bebber R, King MT, Calvert MJ, Stockler MR, Friedlander M. The importance of patient-reported outcomes in clinical trials and strategies for future optimization. Patient Relat Outcome Meas. 2018;9:353–367. doi:10.2147/PROM.S156279
  • Kluzek S, Dean B, Wartolowska KA. Patient-reported outcome measures (PROMs) as proof of treatment efficacy. BMJ Evid Based Med. 2021;bmjebm-2020-111573. doi:10.1136/bmjebm-2020-111573
  • Gossec L, Dougados M, Dixon W. Patient-reported outcomes as end points in clinical trials in rheumatoid arthritis. RMD Open. 2015;1:e000019. doi:10.1136/rmdopen-2014-000019
  • LeBlanc TW, Abernethy AP. Patient-reported outcomes in cancer care - hearing the patient voice at greater volume. Nat Rev Clin Oncol. 2017;14:763–772. doi:10.1038/nrclinonc.2017.153
  • Crossnohere NL, Brundage M, Calvert MJ, et al. International guidance on the selection of patient-reported outcome measures in clinical trials: a review. Qual Life Res. 2021;30:21–40. doi:10.1007/s11136-020-02625-z
  • Durand C, Eldoma M, Marshall DA, Bansback N, Hazlewood GS. Patient preferences for disease-modifying antirheumatic drug treatment in rheumatoid arthritis: a systematic review. J Rheumatol. 2020;47:176–187. doi:10.3899/jrheum.181165
  • Bansal D, Bhagat A, Schifano F, Gudala K. Role of patient-reported outcomes and other efficacy endpoints in the drug approval process in Europe (2008–2012). J Epidemiol Glob Health. 2015;5:385–395. doi:10.1016/j.jegh.2015.04.006
  • Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021; 372:n71
  • Horta-Baas G. Validation of a Spanish version of the Health Assessment Questionnaire-II to assess Mexican patients’ physical function with rheumatoid arthritis. Reumatol Clin. 2021. doi:10.1016/j.reumae.2020.11.002
  • 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. 2017;56:2093–2101. doi:10.1093/rheumatology/kex269
  • Jaworski J, Matucci-Cerinic M, Schulze-Koops H, et al. Switch from reference etanercept to SDZ ETN, an etanercept biosimilar, does not impact efficacy, safety, and immunogenicity of etanercept in patients with moderate-to-severe rheumatoid arthritis: 48-week results from the phase III, randomized, double-blind EQUIRA study. Arthritis Res Ther. 2019;21:130. doi:10.1186/s13075-019-1907-x
  • Blauvelt A, Leonardi CL, Gaylis N, et al. Treatment with SDZ-ADL, an adalimumab biosimilar, in patients with rheumatoid arthritis, psoriasis, or psoriatic arthritis: results of patient-reported outcome measures from two phase III studies (ADMYRA and ADACCESS). BioDrugs. 2021;35:229–238. doi:10.1007/s40259-021-00470-1
  • Yoo DH, Prodanovic N, Jaworski J, et al. Efficacy and safety of CT-P13 (biosimilar infliximab) in patients with rheumatoid arthritis: comparison between switching from reference infliximab to CT-P13 and continuing CT-P13 in the PLANETRA extension study. Ann Rheum Dis. 2017;76:355–363. doi:10.1136/annrheumdis-2015-208786
  • Fleischmann RM, Alten R, Pileckyte M, et al. A comparative clinical study of PF-06410293, a candidate Adalimumab biosimilar, and Adalimumab reference product (Humira(R)) in the treatment of active rheumatoid arthritis. Arthritis Res Ther. 2018;20:178. doi:10.1186/s13075-018-1676-y
  • 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:e000757. doi:10.1136/rmdopen-2018-000757
  • Nikiphorou E, Radner H, Chatzidionysiou K, et al. Patient global assessment in measuring disease activity in rheumatoid arthritis: a review of the literature. Arthritis Res Ther. 2016;18:251. doi:10.1186/s13075-016-1151-6
  • 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;72:1613–1620. doi:10.1136/annrheumdis-2012-203090
  • Edwards CJ, Monnet J, Ullmann M, Vlachos P, Chyrok V, Ghori V. Safety of Adalimumab biosimilar MSB11022 (acetate-buffered formulation) in patients with moderately-to-severely active rheumatoid arthritis. Clin Rheumatol. 2019;38:3381–3390. doi:10.1007/s10067-019-04679-y
  • Jorgensen KK, Olsen IC, Goll GL, et al. Switching from originator infliximab to biosimilar CT-P13 compared with maintained treatment with originator infliximab (NOR-SWITCH): a 52-week, randomised, double-blind, non-inferiority trial. Lancet. 2017;389:2304–2316. doi:10.1016/S0140-6736(17)30068-5
  • 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;25:817–824. doi:10.3109/14397595.2015.1022297
  • Tanaka Y, Yamanaka H, Takeuchi T, et al. Safety and efficacy of CT-P13 in Japanese patients with rheumatoid arthritis in an extension phase or after switching from infliximab. Mod Rheumatol. 2017;27:237–245. doi:10.1080/14397595.2016.1206244
  • Goll GL, Jorgensen KK, Sexton J, et al. Long-term efficacy and safety of biosimilar infliximab (CT-P13) after switching from originator infliximab: open-label extension of the NOR-SWITCH trial. J Intern Med. 2019;285:653–669. doi:10.1111/joim.12880
  • Codreanu C, Sirova K, Jarosova K, Batalov A. Assessment of effectiveness and safety of biosimilar infliximab (CT-P13) in a real-life setting for treatment of patients with active rheumatoid arthritis or ankylosing spondylitis. Curr Med Res Opin. 2018;34:1763–1769. doi:10.1080/03007995.2018.1441144
  • Gossec L, Paternotte S, Aanerud GJ, et al. Finalisation and validation of the rheumatoid arthritis impact of disease score, a patient-derived composite measure of impact of rheumatoid arthritis: a EULAR initiative. Ann Rheum Dis. 2011;70:935–942. doi:10.1136/ard.2010.142901
  • Glintborg B, Loft AG, Omerovic E, et al. To switch or not to switch: results of a nationwide guideline of mandatory switching from originator to biosimilar etanercept. One-year treatment outcomes in 2061 patients with inflammatory arthritis from the DANBIO registry. Ann Rheum Dis. 2019;78:192–200. doi:10.1136/annrheumdis-2018-213474
  • Cheon JH, Nah S, Kang HW, et al. Infliximab biosimilar CT-P13 observational studies for rheumatoid arthritis, inflammatory bowel diseases, and ankylosing spondylitis: pooled analysis of long-term safety and effectiveness. Adv Ther. 2021;38:4366–4387. doi:10.1007/s12325-021-01834-3
  • Gron KL, Glintborg B, Norgaard M, et al. Comparative effectiveness of certolizumab pegol, abatacept, and biosimilar infliximab in patients with rheumatoid arthritis treated in routine care: observational data from the Danish DANBIO registry emulating a randomized trial. Arthritis Rheumatol. 2019;71:1997–2004. doi:10.1002/art.41031
  • Glintborg B, Sorensen IJ, Loft AG, et al. A nationwide non-medical switch from originator infliximab to biosimilar CT-P13 in 802 patients with inflammatory arthritis: 1-year clinical outcomes from the DANBIO registry. Ann Rheum Dis. 2017;76:1426–1431. doi:10.1136/annrheumdis-2016-210742
  • Abdalla A, Byrne N, Conway R, et al. Long-term safety and efficacy of biosimilar infliximab among patients with inflammatory arthritis switched from reference product. Open Access Rheumatol. 2017;9:29–35. doi:10.2147/OARRR.S124975
  • Tweehuysen L, van den Bemt BJF, van Ingen IL, et al. Subjective complaints as the main reason for biosimilar discontinuation after open-label transition from reference infliximab to biosimilar infliximab. Arthritis Rheumatol. 2018;70:60–68. doi:10.1002/art.40324
  • Kay J, Jaworski J, Wojciechowski R, et al. Efficacy and safety of biosimilar CT-P17 versus reference Adalimumab in subjects with rheumatoid arthritis: 24-week results from a randomized study. Arthritis Res Ther. 2021;23:51. doi:10.1186/s13075-020-02394-7
  • Furst DE, Jaworski J, Wojciechowski R, et al. Efficacy and safety of switching from reference Adalimumab to CT-P17 (100 mg/mL): 52-week randomised study in rheumatoid arthritis. Rheumatology. 2021. doi:10.1093/rheumatology/keab460
  • Kiltz U, Pudelko JC, Tsiami S, Baraliakos X, Braun J. Non-medical switching from reference to biosimilar etanercept - no evidence for nocebo effect: a retrospective analysis of real-life data. Clin Exp Rheumatol. 2021;39:1345–1351.
  • Maucksch C, Aries PM, Zinke S, Müller-Ladner U. Patient satisfaction with the etanercept biosimilar SB4 device, among rheumatoid arthritis and spondyloarthropathy patients - a German observational study. Open Rheumatol J. 2020;14:7.14. doi:10.2174/1874312902014010007
  • Bruni C, Bitti R, Nacci F, et al. Efficacy and safety of switching from reference Adalimumab to SB5 in a real-life cohort of inflammatory rheumatic joint diseases. Clin Rheumatol. 2021;40:85–91. doi:10.1007/s10067-020-05199-w
  • Colloca L, Panaccione R, Murphy TK. The clinical implications of nocebo effects for biosimilar therapy. Front Pharmacol. 2019;10:1372. doi:10.3389/fphar.2019.01372
  • Odinet JS, Day CE, Cruz JL, Heindel GA. The biosimilar nocebo effect? A systematic review of double-blinded versus open-label studies. J Manag Care Spec Pharm. 2018;24:952–959. doi:10.18553/jmcp.2018.24.10.952
  • Al Tabaa O, Etcheto A, Dumas S, et al. Doctor’s aptitude for switching from innovator etanercept to biosimilar etanercept in inflammatory rheumatic diseases: experience from a single French rheumatology tertiary care center. Eur J Clin Pharmacol. 2021;77:25–33. doi:10.1007/s00228-020-02957-2
  • Ebbers HC, Pieper B, Issa A, Addison J, Freudensprung U, Rezk MF. Real-world evidence on etanercept biosimilar SB4 in etanercept-naive or switching patients: a systematic review. Rheumatol Ther. 2019;6:317–338. doi:10.1007/s40744-019-00169-4
  • Planes S, Villier C, Mallaret M. The nocebo effect of drugs. Pharmacol Res Perspect. 2016;4:e00208. doi:10.1002/prp2.208
  • Petit J, Antignac M, Poilverd RM, et al. Multidisciplinary team intervention to reduce the nocebo effect when switching from the originator infliximab to a biosimilar. RMD Open. 2021;7:e001396. doi:10.1136/rmdopen-2020-001396
  • Piguet V, D’Incau S, Besson M, Desmeules J, Cedraschi C. Prescribing generic medication in chronic musculoskeletal pain patients: an issue of representations, trust, and experience in a Swiss cohort. PLoS One. 2015;10:e0134661. doi:10.1371/journal.pone.0134661
  • Guttier MC, Silveira MPT, Luiza VL, Bertoldi AD. Factors influencing the preference for purchasing generic drugs in a Southern Brazilian city. Rev Saude Publica. 2017;51:59. doi:10.1590/s1518-8787.2017051006786