13,850
Views
10
CrossRef citations to date
0
Altmetric
Review Articles

Challenges for biosimilars: focus on rheumatoid arthritis

ORCID Icon, , ORCID Icon, , , ORCID Icon, & ORCID Icon show all
Pages 121-153 | Received 24 Dec 2019, Accepted 30 Aug 2020, Published online: 11 Oct 2020

References

  • Carillo S, Mittermayr S, Farrell A, et al. Glycosylation analysis of therapeutic glycoproteins produced in CHO cells. Methods Mol Biol. 2017;1603:227–241.
  • Research AM. World biosimilars/follow on biologics market – opportunities and forecasts. 2014.
  • Levine HL, Cooney BR. The development of therapeutic monoclonal antibody products. Waltham (MA): BioProcess Technology Consultants, Inc; 2017.
  • Emily Capra JS, Guang Y. Gene therapy coming of age: opportunities and challenges to getting ahead. Pharmaceuticals and Medical Products Practice. 2019.
  • Hanna, C., Uccello, C. Prescription drug spending in the U.S. Healthcare System. Am Academy of Actuaries 2018. 1-12. Available from: www.actuary.org.
  • Isaacs J, Gonçalves J, Strohal R, et al. The biosimilar approval process: how different is it? Considerations Med. 2017;1(1):3–6.
  • Kogan LA. US biologics price competition and innovation Act of 2009 triggers public debates, regulatory/policy risks, and international trade concerns. Global Trade & Cust J. 2011;(6):513.
  • Kirchhoff CF, Wang XM, Conlon HD, et al. Biosimilars: key regulatory considerations and similarity assessment tools. Biotechnol Bioeng. 2017;114(12):2696–2705.
  • Reusch D, Haberger M, Falck D, et al. Comparison of methods for the analysis of therapeutic immunoglobulin G Fc-glycosylation profiles-Part 2: mass spectrometric methods. MAbs. 2015;7(4):732–742.
  • Christl L. FDA’s overview of the regulatory guidance for the development and approval of biosimilar products in the US. USA: US Food and Drug Administration. 2016.
  • Olech E. Biosimilars: rationale and current regulatory landscape. Semin Arthritis Rheum. 45(5 Suppl):S1–S10.
  • Alten R, Cronstein BN. Clinical trial development for biosimilars. Semin Arthritis Rheum. 44(6 Suppl):S2–S8.
  • Laimer J, Hofer H, Fritz M, et al. MAESTRO-multi agent stability prediction upon point mutations. BMC Bioinformatics. 2015;16(1):116.
  • Weise M, Bielsky M-C, De Smet K, et al. Biosimilars—why terminology matters. Nat Biotechnol. 2011;29(8):690–693.
  • Hamm M, Wang Y, Rustandi RR. Characterization of N-linked glycosylation in a monoclonal antibody produced in NS0 cells using capillary electrophoresis with laser-induced fluorescence detection. Pharmaceuticals. 2013;6(3):393–406.
  • Schiestl M, Stangler T, Torella C, et al. Acceptable changes in quality attributes of glycosylated biopharmaceuticals. Nat Biotechnol. 2011;29(4):310–312.
  • Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol. 2003;21(3):255–261.
  • Beck A, Sanglier-Cianférani S, Van Dorsselaer A. Biosimilar, biobetter, and next generation antibody characterization by mass spectrometry. Anal Chem. 2012;84(11):4637–4646.
  • Food U, Administration D. Guidance for industry: scientific considerations in demonstrating biosimilarity to a reference product. Rockville (MD), US Food and Drug Administration; 2012.
  • Sha S, Agarabi C, Brorson K, et al. N-Glycosylation design and control of therapeutic monoclonal antibodies. Trends Biotechnol. 2016;34(10):835–846.
  • Shinkawa T, Nakamura K, Yamane N, et al. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J Biol Chem. 2003;278(5):3466–3473.
  • St Amand MM, Tran K, Radhakrishnan D, et al. Controllability analysis of protein glycosylation in CHO cells. PLoS One. 2014;9(2):e87973.
  • Wooding KM, Peng W, Mechref Y. Characterization of pharmaceutical IgG and biosimilars using miniaturized platforms and LC-MS/MS. Curr Pharm Biotechnol. 2016;17(9):788–801.
  • Hong J, Lee Y, Lee C. et al. Physicochemical and biological characterization of SB2, a biosimilar of Remicade®(infliximab). MAbs. 2017;9(2):364–382.
  • Cho IH, Lee N, Song D. et al. Evaluation of the structural, physicochemical, and biological characteristics of SB4, a biosimilar of etanercept. MAbs. 2016;8(6):1136–1155.
  • Kozlowski S, Swann P. Current and future issues in the manufacturing and development of monoclonal antibodies. Adv Drug Deliv Rev. 2006;58(5–6):707–722.
  • Dumont J, Euwart D, Mei B, et al. Human cell lines for biopharmaceutical manufacturing: history, status, and future perspectives. Crit Rev Biotechnol. 2016;36(6):1110–1122.
  • Lam SK, Ng TB. Lectins: production and practical applications. Appl Microbiol Biotechnol. 2011;89(1):45–55.
  • Dobson CL, Devine PW, Phillips JJ, et al. Engineering the surface properties of a human monoclonal antibody prevents self-association and rapid clearance in vivo. Sci Rep. 2016;6:38644.
  • Wouters OJ, McKee M, Luyten J. Estimated research and development investment needed to bring a new medicine to market, 2009–2018. JAMA. 2020;323(9):844–853.
  • Farid SS, Baron M, Stamatis C, et al. Benchmarking biopharmaceutical process development and manufacturing cost contributions to R&D. Mabs. 2020;12(1):1754999.
  • Burchiel SW, Aspbury R, Munday J. The search for biosimilars and biobetters. Drug Discov Today. 2019;24(5):1087–1091.
  • Dan N, Setua S, Kashyap VK, et al. Antibody-drug conjugates for cancer therapy: chemistry to clinical implications. Pharmaceuticals. 2018;11(2):32.
  • European Medicines Agency. (2005). ICH Topic Q5E, comparability of Biotechnological/Biological products. Step 5, CPMP/ICH/5721/03, 1–13.
  • Neubauer S, Cifaldi M, Mittendorf T, et al. Biologic TNF inhibiting agents for treatment of rheumatoid arthritis: persistence and dosing patterns in Germany. Health Econ Rev. 2014;4(1):32.
  • Smolen JS, Aletaha D, Koeller M, et al. New therapies for treatment of rheumatoid arthritis. Lancet. 2007;370(9602):1861–1874.
  • Malemud CJ, Blumenthal DE. Protein kinase small molecule inhibitors for rheumatoid arthritis: Medicinal chemistry/clinical perspectives. World J Orthop. 2014;5(4):496–503.
  • Pesu M, Laurence A, Kishore N, et al. Therapeutic targeting of Janus kinases. Immunol Rev. 2008;223:132–142.
  • Ozminkowski RJ, Burton WN, Goetzel RZ, et al. The impact of rheumatoid arthritis on medical expenditures, absenteeism, and short-term disability benefits. J Occup Environ Med. 2006;48(2):135–148.
  • Albers JM, Kuper HH, van Riel PL, et al. Socio-economic consequences of rheumatoid arthritis in the first years of the disease. Rheumatology. 1999;38(5):423–430.
  • Birnbaum H, Pike C, Kaufman R, et al. Societal cost of rheumatoid arthritis patients in the US. Curr Med Res Opin. 2010;26(1):77–90.
  • Zhang W, Anis AH. The economic burden of rheumatoid arthritis: beyond health care costs. Clin Rheumatol. 2011;30(S1):25–32.
  • Boonen A, Severens JL. The burden of illness of rheumatoid arthritis. Clin Rheumatol. 2011;30(S1):3–8.
  • Cooper NJ. Economic burden of rheumatoid arthritis: a systematic review. Rheumatology. 2000;39(1):28–33.
  • Yoon SJ, Bae SC, Lee SI, et al. Measuring the burden of disease in Korea. J Korean Med Sci. 2007;22(3):518–523.
  • Koenders MI, van den Berg WB. Novel therapeutic targets in rheumatoid arthritis. Trends Pharmacol Sci. 2015;36(4):189–195.
  • Foundation A. Arthritis By The Numbers Atlanta, USA. 2018; [cited 2019 Dec 22]. Available from: https://www.arthritis.org/Documents/Sections/About-Arthritis/arthritis-facts-stats-figures.pdf.
  • Aj LB. The first description of rheumatoid arthritis. Unabridged text of the doctoral dissertation presented in 1800. Joint Bone Spine. 2001;68(2):130–143.
  • Fauci A. Harrison’s principle of internal medicine. 18 ed. United States: McGraw Hill; 2011.
  • Silman AJ, Hochberg MC. Epidemiology of the rheumatic diseases. 2nd ed. New York: Oxford University Press; 2001.
  • McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365(23):2205–2219.
  • Smolen JS, Steiner G. Therapeutic strategies for rheumatoid arthritis. Nat Rev Drug Discov. 2003;2(6):473–488.
  • Duke O, Panayi GS. The pathogenesis of rheumatoid arthritis. In Vivo. 1988;2(1):95–103.
  • Jimenez-Boj E, Redlich K, Türk B, et al. Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol. 2005;175(4):2579–2588.
  • McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007;7(6):429–442.
  • Maini RN, Taylor PC. Anti-cytokine therapy for rheumatoid arthritis. Annu Rev Med. 2000;51:207–229.
  • McInnes IB, Liew FY. Cytokine networks–towards new therapies for rheumatoid arthritis. Nat Clin Pract Rheumatol. 2005;1(1):31–39.
  • Gaujoux-Viala C, Nam J, Ramiro S, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2019 update. Ann Rheum Dis. 2014;73(3):510–515.
  • Smolen JS, Landewe R, Bijlsma J, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis. 2017;76(6):960–977.
  • Emery P, Breedveld FC, Hall S, et al. Comparison of methotrexate monotherapy with a combination of methotrexate and etanercept in active, early, moderate to severe rheumatoid arthritis (COMET): a randomised, double-blind, parallel treatment trial. Lancet. 2008;372(9636):375–382.
  • 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.
  • 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.
  • Gottenberg JE, Morel J, Perrodeau E, et al. Comparative effectiveness of rituximab, abatacept, and tocilizumab in adults with rheumatoid arthritis and inadequate response to TNF inhibitors: prospective cohort study. BMJ. 2019;364:l67.
  • 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.
  • Teitsma XM, Marijnissen AK, Bijlsma JW, et al. Tocilizumab as monotherapy or combination therapy for treating active rheumatoid arthritis: a meta-analysis of efficacy and safety reported in randomized controlled trials. Arthritis Res Ther. 2016;18(1):211.
  • Emery P, Burmester GR, Bykerk VP, et al. Evaluating drug-free remission with abatacept in early rheumatoid arthritis: results from the phase 3b, multicentre, randomised, active-controlled AVERT study of 24 months, with a 12-month, double-blind treatment period. Ann Rheum Dis. 2015;74(1):19–26.
  • Klareskog L, van der Heijde D, de Jager JP, et al. Therapeutic effect of the combination of etanercept and methotrexate compared with each treatment alone in patients with rheumatoid arthritis: double-blind randomised controlled trial. Lancet. 2004;363(9410):675–681.
  • 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.
  • Jansen JP, Buckley F, Dejonckheere F, et al. Comparative efficacy of biologics as monotherapy and in combination with methotrexate on patient reported outcomes (PROs) in rheumatoid arthritis patients with an inadequate response to conventional DMARDs–a systematic review and network meta-analysis. Health Qual Life Outcomes. 2014;12(1):102.
  • Kalliolias GD, Liossis SN. The future of the IL-1 receptor antagonist anakinra: from rheumatoid arthritis to adult-onset Still’s disease and systemic-onset juvenile idiopathic arthritis. Expert Opin Invest Drugs. 2008;17(3):349–359.
  • 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.
  • Cabral VP, Andrade CA, Passos SR, et al. Severe infection in patients with rheumatoid arthritis taking anakinra, rituximab, or abatacept: a systematic review of observational studies. Rev Bras Reumatol Engl Ed. 2016;56(6):543–550.
  • Salliot C, Dougados M, Gossec L. Risk of serious infections during rituximab, abatacept and anakinra treatments for rheumatoid arthritis: meta-analyses of randomised placebo-controlled trials. Ann Rheum Dis. 2009;68(1):25–32.
  • Fleischmann RM, Genovese MC, Enejosa JV, et al. Safety and effectiveness of upadacitinib or adalimumab plus methotrexate in patients with rheumatoid arthritis over 48 weeks with switch to alternate therapy in patients with insufficient response. Ann Rheum Dis. 2019;78(11):1454–1462.
  • Vinson D, Molet-Benhamou L, Degboe Y, et al. Impact of tapering targeted therapies (bDMARDs or JAKis) on the risk of serious infections and adverse events of special interest in patients with rheumatoid arthritis or spondyloarthritis: a systematic analysis of the literature and meta-analysis. Arthritis Res Ther. 2020;22(1):97.
  • Ramiro S, Sepriano A, Chatzidionysiou K, et al. Safety of synthetic and biological DMARDs: a systematic literature review informing the 2016 update of the EULAR recommendations for management of rheumatoid arthritis. Ann Rheum Dis. 2017;76(6):1101–1136.
  • Dreyer L, Cordtz RL, Hansen IMJ, et al. Risk of second malignant neoplasm and mortality in patients with rheumatoid arthritis treated with biological DMARDs: a Danish population-based cohort study. Ann Rheum Dis. 2018;77(4):510–514.
  • Burmester GR, Pope JE. Novel treatment strategies in rheumatoid arthritis. Lancet. 2017;389(10086):2338–2348.
  • Verden A, Dimbil M, Kyle R, et al. Analysis of spontaneous postmarket case reports submitted to the FDA regarding thromboembolic adverse events and JAK inhibitors. Drug Saf. 2018;41(4):357–361.
  • Kaufman MB. Pharmaceutical approval update. P T. 2018;43(9):528–530.
  • EMA. Xeljanz 2019. [updated 5-7-2019; cited 2020 Oct 15]. Available from: https://www.ema.europa.eu/en/medicines/human/EPAR/xeljanz.
  • FDA. FDA approves Boxed Warning about increased risk of blood clots and death with higher dose of arthritis and ulcerative colitis medicine tofacitinib (Xeljanz, Xeljanz XR). 2019; [updated 28-8-2019; cited 2019 Oct 15]. Available from: https://www.fda.gov/drugs/drug-safety-and-availability/fda-approves-boxed-warning-about-increased-risk-blood-clots-and-death-higher-dose-arthritis-and
  • Becede M, Alasti F, Gessl I, et al. Risk profiling for a refractory course of rheumatoid arthritis. Semin Arthritis Rheum. 2019;49(2):211–217.
  • Tracey D, Klareskog L, Sasso EH, et al. Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacol Ther. 2008;117(2):244–279.
  • Azevedo VF, Galli N, Kleinfelder A, et al. Etanercept biosimilars. Rheumatol Int. 2015;35(2):197–209.
  • Hess A, Axmann R, Rech J, et al. Blockade of TNF-alpha rapidly inhibits pain responses in the central nervous system. Proc Natl Acad Sci USA. 2011;108(9):3731–3736.
  • Feldmann M, Brennan FM, Maini RN. Rheumatoid arthritis. Cell. 1996;85(3):307–310.
  • Vervoordeldonk MJ, Tak PP. Cytokines in rheumatoid arthritis. Curr Rheumatol Rep. 2002;4(3):208–217.
  • Feldmann M, Brennan FM, Maini RN. Role of cytokines in rheumatoid arthritis. Annu Rev Immunol. 1996;14:397–440.
  • Zhang JM, An J. Cytokines, inflammation, and pain. Int Anesthesiol Clin. 2007;45(2):27–37.
  • Raza K, Falciani F, Curnow SJ, et al. Early rheumatoid arthritis is characterized by a distinct and transient synovial fluid cytokine profile of T cell and stromal cell origin. Arthritis Res Ther. 2005;7(4):R784–R795.
  • Feldmann M, Brennan F, Bondeson J, et al. Analysis of cytokine expression in rheumatoid synovium has provided new insights into the pathogenesis of rheumatoid arthritis and new therapeutic opportunities. Transplant Proc. 2001;33(3):2085–2086.
  • Rossi JF, Lu ZY, Jourdan M, et al. Interleukin-6 as a therapeutic target. Clin Cancer Res. 2015;21(6):1248–1257.
  • Feldmann M, Maini RN, Bondeson J, et al. Cytokine blockade in rheumatoid arthritis. Adv Exp Med Biol. 2001;490:119–127.
  • Feldmann M, Maini RN. Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu Rev Immunol. 2001;19(1):163–196.
  • Taylor PC, Peters AM, Paleolog E, et al. Reduction of chemokine levels and leukocyte traffic to joints by tumor necrosis factor alpha blockade in patients with rheumatoid arthritis. Arthritis Rheum. 2000;43(1):38–47.
  • Toussirot E, Wendling D. The use of TNF-alpha blocking agents in rheumatoid arthritis: an overview. Expert Opin Pharmacother. 2004;5(3):581–594.
  • Raychaudhuri SP, Nguyen CT, Raychaudhuri SK, et al. Incidence and nature of infectious disease in patients treated with anti-TNF agents. Autoimmun Rev. 2009;9(2):67–81.
  • Saklatvala J. Tumour necrosis factor alpha stimulates resorption and inhibits synthesis of proteoglycan in cartilage. Nature. 1986;322(6079):547–549.
  • Bathon JM, Martin RW, Fleischmann RM, et al. A comparison of etanercept and methotrexate in patients with early rheumatoid arthritis. N Engl J Med. 2000;343(22):1586–1593.
  • Maini R, St Clair EW, Breedveld F, et al. Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. ATTRACT Study Group. Lancet. 1999;354(9194):1932–1939.
  • Maini RN, Elliott M, Brennan FM, et al. TNF blockade in rheumatoid arthritis: implications for therapy and pathogenesis. APMIS. 1997;105(4):257–263.
  • Bhatnagar R, Penfornis H, Mauviel A, et al. Interleukin-1 inhibits the synthesis of collagen by fibroblasts. Biochem Int. 1986;13(4):709–720.
  • Smolen JS, Weinblatt ME. When patients with rheumatoid arthritis fail tumour necrosis factor inhibitors: what is the next step? Ann Rheum Dis. 2008;67(11):1497–1498.
  • Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Allaart CF, et al. Clinical and radiographic outcomes of four different treatment strategies in patients with early rheumatoid arthritis (the BeSt study): a randomized, controlled trial. Arthritis Rheum. 2005;52(11):3381–3390.
  • Gerlag DM, Tak PP. Novel approaches for the treatment of rheumatoid arthritis: lessons from the evaluation of synovial biomarkers in clinical trials. Best Pract Res Clin Rheumatol. 2008;22(2):311–323.
  • Brennan FM, Chantry D, Jackson A, et al. Inhibitory effect of TNF alpha antibodies on synovial cell interleukin-1 production in rheumatoid arthritis. Lancet. 1989;334(8657):244–247.
  • Bystrom J, Clanchy FI, Taher TE, et al. Response to treatment with TNFalpha inhibitors in rheumatoid arthritis is associated with high levels of GM-CSF and GM-CSF(+) T lymphocytes. Clin Rev Allergy Immunol. 2017;53(2):265–276.
  • Polzer K, Baeten D, Soleiman A, et al. Tumour necrosis factor blockade increases lymphangiogenesis in murine and human arthritic joints. Ann Rheum Dis. 2008;67(11):1610–1616.
  • Szekanecz Z, Pakozdi A, Szentpetery A, et al. Chemokines and angiogenesis in rheumatoid arthritis. Front Biosci. 2009;1:44–51.
  • Bradfield PF, Amft N, Vernon-Wilson E, et al. Rheumatoid fibroblast-like synoviocytes overexpress the chemokine stromal cell-derived factor 1 (CXCL12), which supports distinct patterns and rates of CD4+ and CD8+ T cell migration within synovial tissue. Arthritis Rheum. 2003;48(9):2472–2482.
  • Maini RN, Feldmann M. How does infliximab work in rheumatoid arthritis? Arthritis Res. 2002;4 (Suppl 2):S22–S28.
  • Lim H, Lee SH, Lee HT, et al. Structural biology of the TNFalpha antagonists used in the treatment of rheumatoid arthritis. Int J Mol Sci. 2018;19(3):768.
  • Chen X, DuBois DC, Almon RR, et al. Interrelationships between Infliximab and recombinant tumor necrosis factor-alpha in plasma using minimal physiologically based pharmacokinetic models. Drug Metab Dispos. 2017;45(7):790–797.
  • Frenzel A, Schirrmann T, Hust M. Phage display-derived human antibodies in clinical development and therapy. MAbs. 2016;8(7):1177–1194.
  • Jespers LS, Roberts A, Mahler SM, et al. Guiding the selection of human antibodies from phage display repertoires to a single epitope of an antigen. Nat Biotechnol. 1994;12(9):899–903.
  • Grazio S. [Adalimumab (Humira)-efficacy in rheumatoid arthritis treatment with particular reference to working ability]. Reumatizam. 2008;55(2):62–67.
  • Guo Q, Wang Y, Xu D, et al. Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone Res. 2018;6:15.
  • Keystone E, Haraoui B. Adalimumab therapy in rheumatoid arthritis. Rheum Dis Clin North Am. 2004;30(2):349–364.
  • Goel N, Stephens S. Certolizumab pegol. MAbs. 2010;2(2):137–147.
  • Veronese FM, Pasut G. PEGylation, successful approach to drug delivery. Drug Discov Today. 2005;10(21):1451–1458.
  • Chapman AP. PEGylated antibodies and antibody fragments for improved therapy: a review. Adv Drug Deliv Rev. 2002;54(4):531–545.
  • Chapman AP, Antoniw P, Spitali M, et al. Therapeutic antibody fragments with prolonged in vivo half-lives. Nat Biotechnol. 1999;17(8):780–783.
  • Nesbitt A, Fossati G, Bergin M, et al. Mechanism of action of certolizumab pegol (CDP870): in vitro comparison with other anti-tumor necrosis factor alpha agents. Inflamm Bowel Dis. 2007;13(11):1323–1332.
  • Keystone E, Heijde D, Mason D, Jr, 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.
  • Smolen J, Landewe RB, Mease P, et al. Efficacy and safety of certolizumab pegol plus methotrexate in active rheumatoid arthritis: the RAPID 2 study. A randomised controlled trial. Ann Rheum Dis. 2009;68(6):797–804.
  • Palframan R, Airey M, Moore A, et al. Use of biofluorescence imaging to compare the distribution of certolizumab pegol, adalimumab, and infliximab in the inflamed paws of mice with collagen-induced arthritis. J Immunol Methods. 2009;348(1–2):36–41.
  • Mease PJ, Armstrong AW. Managing patients with psoriatic disease: the diagnosis and pharmacologic treatment of psoriatic arthritis in patients with psoriasis. Drugs. 2014;74(4):423–441.
  • Bykerk VP, Cush J, Winthrop K, et al. Update on the safety profile of certolizumab pegol in rheumatoid arthritis: an integrated analysis from clinical trials. Ann Rheum Dis. 2015;74(1):96–103.
  • Inman RD, Davis JC, Jr., Heijde D, et al. Efficacy and safety of golimumab in patients with ankylosing spondylitis: results of a randomized, double-blind, placebo-controlled, phase III trial. Arthritis Rheum. 2008;58(11):3402–3412.
  • Kavanaugh A, McInnes I, Mease P, et al. Golimumab, a new human tumor necrosis factor alpha antibody, administered every four weeks as a subcutaneous injection in psoriatic arthritis: Twenty-four-week efficacy and safety results of a randomized, placebo-controlled study. Arthritis Rheum. 2009;60(4):976–986.
  • Hutas G. Golimumab, a fully human monoclonal antibody against TNFalpha. Curr Opin Mol Ther. 2008;10(4):393–406.
  • Emery P, Fleischmann RM, Strusberg I, et al. Efficacy and safety of subcutaneous golimumab in methotrexate-naive patients with rheumatoid arthritis: five-year results of a randomized clinical trial. Arthritis Care Res. 2016;68(6):744–752.
  • Xu Z, Vu T, Lee H, et al. Population pharmacokinetics of golimumab, an anti-tumor necrosis factor-alpha human monoclonal antibody, in patients with psoriatic arthritis. J Clin Pharmacol. 2009;49(9):1056–1070.
  • Caporali R, Caprioli M, Bobbio-Pallavicini F, et al. DMARDS and infections in rheumatoid arthritis. Autoimmun Rev. 2008;8(2):139–143.
  • Zidi I, Mestiri S, Bartegi A, et al. TNF-alpha and its inhibitors in cancer. Med Oncol. 2010;27(2):185–198.
  • Keystone EC, Genovese MC, 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.
  • Emery P, Fleischmann RM, Moreland LW, et al. Golimumab, a human anti-tumor necrosis factor alpha monoclonal antibody, injected subcutaneously every four weeks in methotrexate-naive patients with active rheumatoid arthritis: twenty-four-week results of a phase III, multicenter, randomized, double-blind, placebo-controlled study of golimumab before methotrexate as first-line therapy for early-onset rheumatoid arthritis. Arthritis Rheum. 2009;60(8):2272–2283.
  • Acevedo-Vasquez E, Ponce de Leon D, Gamboa-Cardenas R. Latent infection and tuberculosis disease in rheumatoid arthritis patients. Rheum Dis Clin North Am. 2009;35(1):163–181.
  • Dumitru RB, Horton S, Hodgson R, et al. A prospective, single-centre, randomised study evaluating the clinical, imaging and immunological depth of remission achieved by very early versus delayed Etanercept in patients with Rheumatoid Arthritis (VEDERA). BMC Musculoskelet Disord. 2016;17:61.
  • Moreland LW, Schiff MH, Baumgartner SW, et al. Etanercept therapy in rheumatoid arthritis. A randomized, controlled trial. Ann Intern Med. 1999;130(6):478–486.
  • Madhusudan S, Muthuramalingam SR, Braybrooke JP, et al. Study of etanercept, a tumor necrosis factor-alpha inhibitor, in recurrent ovarian cancer. J Clin Oncol. 2005;23(25):5950–5959.
  • Mears JB, Huynh-Duc L, Fiechtner JJ. A patient with rheumatoid arthritis on methotrexate and etanercept who developed Pasteurella multocida Bacteremia. J Clin Rheumatol. 2015;21(8):457. Dec
  • Neovius M, Arkema EV, Olsson H, et al. Drug survival on TNF inhibitors in patients with rheumatoid arthritis comparison of adalimumab, etanercept and infliximab. Ann Rheum Dis. 2015;74(2):354–360.
  • McCamish M, Woollett G. The state of the art in the development of biosimilars. Clin Pharmacol Ther. 2012;91(3):405–417.
  • Kay J, Smolen JS. Biosimilars to treat inflammatory arthritis: the challenge of proving identity. Ann Rheum Dis. 2013;72(10):1589–1593.
  • Beck A, Reichert JM. Approval of the first biosimilar antibodies in Europe: a major landmark for the biopharmaceutical industry. MAbs. 2013;5(5):621–623.
  • Rinaudo-Gaujous M, Paul S, Tedesco ED, et al. Review article: biosimilars are the next generation of drugs for liver and gastrointestinal diseases. Aliment Pharmacol Ther. 2013;38(8):914–924.
  • Hlavaty T, Letkovsky J. Biosimilars in the therapy of inflammatory bowel diseases. Eur J Gastroenterol Hepatol. 2014;26(6):581–587.
  • Genazzani A, Altomare G, Balato N, et al. Biosimilar infliximab: an expert view. G Ital Dermatol Venereol. 2015;150(4):449–459.
  • FDA. FDA approves first biosimilar product Zarxio: FDA; 2015; [cited 2016 Feb 16]. Available from: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm436648.htm.
  • Ledford H. Biosimilar’ drugs poised to penetrate market. Nature. 2010;468(7320):18–19.
  • Jung SK, Lee KH, Jeon JW, et al. Physicochemical characterization of Remsima. MAbs. 2014;6(5):1163–1177.
  • Tang H, Hsueh P, Kletter D, et al. The detection and discovery of glycan motifs in biological samples using lectins and antibodies: new methods and opportunities. Adv Cancer Res. 2015;126:167–202.
  • Zhang P, Woen S, Wang T, et al. Challenges of glycosylation analysis and control: an integrated approach to producing optimal and consistent therapeutic drugs. Drug Discov Today. 2016;21(5):740–765.
  • Ahmadi S, Davami F, Davoudi N, et al. Monoclonal antibodies expression improvement in CHO cells by PiggyBac transposition regarding vectors ratios and design. PLoS One. 2017;12(6):e0179902.
  • Krambeck FJ, Bennun SV, Andersen MR, et al. Model-based analysis of N-glycosylation in Chinese hamster ovary cells. PLoS One. 2017;12(5):e0175376.
  • Magnelli PE, Bielik AM, Guthrie EP. Identification and characterization of protein glycosylation using specific endo- and exoglycosidases. J Vis Exp. 2011;26(58):e3749.
  • Jefferis R. Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends Pharmacol Sci. 2009;30(7):356–362.
  • Cao M, De Mel N, Shannon A, et al. Charge variants characterization and release assay development for co-formulated antibodies as a combination therapy. MAbs. 2019;11(3):489–499.
  • Duivelshof BL, Fekete S, Guillarme D, et al. A generic workflow for the characterization of therapeutic monoclonal antibodies-application to daratumumab. Anal Bioanal Chem. 2019;411(19):4615–4627.
  • Gomes RA, Almeida C, Correia C, et al. Exploring the analytical power of the QTOF MS platform to assess monoclonal antibodies quality attributes. PLoS One. 2019;14(7):e0219156.
  • Lee JH, Paek K, Moon JH, et al. Biological characterization of SB3, a trastuzumab biosimilar, and the influence of changes in reference product characteristics on the similarity assessment. BioDrugs. 2019;33(4):411–422.
  • Lippold S, Nicolardi S, Dominguez-Vega E, et al. Glycoform-resolved FcRIIIa affinity chromatography-mass spectrometry. MAbs. 2019;11(7):1191–1196.
  • FDA. FDA approves Inflectra, a biosimilar to Remicade: FDA; 2016; [cited 2016 Jun 28]. Available from: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm494227.htm.
  • Blair HA, Deeks ED. Infliximab biosimilar (CT-P13; Infliximab-dyyb): a review in autoimmune inflammatory diseases. BioDrugs. 2016;30(5):469–480.
  • Jung YS, Park DI, Kim YH, et al. Efficacy and safety of CT-P13, a biosimilar of infliximab, in patients with inflammatory bowel disease: a retrospective multicenter study. J Gastroenterol Hepatol. 2015;30(12):1705–1712.
  • Park W, Hrycaj P, Jeka S, et al. A randomised, double-blind, multicentre, parallel-group, prospective study comparing the pharmacokinetics, safety, and efficacy of CT-P13 and innovator infliximab in patients with ankylosing spondylitis: the PLANETAS study. Ann Rheum Dis. 2013;72(10):1605–1612.
  • Ahrweiler S. ACR Response Criteria: PhuseWiki; 2012; [cited 2020 Oct 03]. Available from: https://www.phusewiki.org/wiki/index.php?title=ACR_Response_Criteria.
  • 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.
  • 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.
  • 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.
  • 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(6):471–477.
  • EMA. FLIXABI: EUROPEAN MEDICINE AGENCY; 2016; [cited 2016 Jun 26]. Available from: http://www.ema.europa.eu/ema/index.jsp?curl=pages/medicines/human/medicines/004020/human_med_001980.jsp&mid=WC0b01ac058001d124.
  • 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.
  • EMA. Benepali: EUROPEAN MEDICINES AGENCY; 2016; [cited 2016 June 18]. Available from: http://www.ema.europa.eu/ema/index.jsp?curl=pages/medicines/human/medicines/004007/human_med_001944.jsp&mid=WC0b01ac058001d124.
  • Chadwick L, Zhao S, Mysler E, et al. Review of biosimilar trials and data on etanercept in rheumatoid arthritis. Curr Rheumatol Rep. 2018;20(12):84.
  • Schneider CK. Biosimilars in rheumatology: the wind of change. Ann Rheum Dis. 2013;72(3):315–318.
  • Castaneda-Hernandez G, Gonzalez-Ramirez R, Kay J, et al. Biosimilars in rheumatology: what the clinician should know. RMD Open. 2015;1(1):e000010–e000010.
  • Zhao S, Chadwick L, Mysler E, et al. Review of biosimilar trials and data on adalimumab in rheumatoid arthritis. Curr Rheumatol Rep. 2018;20(10):57.
  • Papp K, Bachelez H, Costanzo A, et al. Clinical similarity of the biosimilar ABP 501 compared with adalimumab after single transition: long‐term results from a randomized controlled, double‐blind, 52‐week, phase III trial in patients with moderate‐to‐severe plaque psoriasis. Br J Dermatol. 2017;177(6):1562–1574.
  • Markus R, McBride HJ, Ramchandani M, et al. A review of the totality of evidence supporting the development of the first adalimumab biosimilar ABP 501. Adv Ther. 2019;36(8):1818–1833.
  • Dorner T, Kay J. Biosimilars in rheumatology: current perspectives and lessons learnt. Nat Rev Rheumatol. 2015;11(12):713–724.
  • Papamichael K, Van Stappen T, Jairath V, et al. Review article: pharmacological aspects of anti-TNF biosimilars in inflammatory bowel diseases. Aliment Pharmacol Ther. 2015;42(10):1158–1169.
  • Geiler J, Buch M, McDermott MF. Anti-TNF treatment in rheumatoid arthritis. Curr Pharm Des. 2011;17(29):3141–3154.
  • Lai Z, La Noce A. Key design considerations on comparative clinical efficacy studies for biosimilars: adalimumab as an example. RMD Open. 2016;2(1):e000154.
  • Jayaraman K. India’s Cipla sets sights on avastin, herceptin and enbrel. Nat Biotechnol. 2010;28(9):883–884.
  • Roy PS, John S, Karankal S, et al. Comparison of the efficacy and safety of Rituximab (Mabthera™) and its biosimilar (Reditux™) in diffuse large B-cell lymphoma patients treated with chemo-immunotherapy: a retrospective analysis. Indian J Med Paediatr Oncol. 2013;34(4):292.
  • Midha V, Mahajan R, Mehta V, et al. Efficacy and safety of the adalimumab biosimilar Exemptia as induction therapy in moderate-to-severe ulcerative colitis. Intest Res. 2018;16(1):83–89.
  • Statista. Top 10 pharmaceutical products by sales worldwide in 2015 (in billion U.S. dollars): The Statistics Portal; 2016. [cited 2016 Jun 26]. Available from: http://www.statista.com/statistics/258022/top-10-pharmaceutical-products-by-global-sales-2011/.
  • Meier FM, McInnes IB. Small-molecule therapeutics in rheumatoid arthritis: scientific rationale, efficacy and safety. Best Pract Res Clin Rheumatol. 2014;28(4):605–624.
  • Simmons DL. Targeting kinases: a new approach to treating inflammatory rheumatic diseases. Curr Opin Pharmacol. 2013;13(3):426–434.
  • Cohen MD, Keystone EC. JAK inhibitors for rheumatoid arthritis. Curr Treat Options in Rheum. 2015;1(4):305–319.
  • Kavanaugh A, Smolen JS, Emery P, et al. Effect of certolizumab pegol with methotrexate on home and work place productivity and social activities in patients with active rheumatoid arthritis. Arthritis Rheum. 2009;61(11):1592–1600.
  • Scheinberg MA, Azevedo VF. Biosimilars in rheumatology: perspective and concerns. Rheumatology. 2014;53(3):389–390.
  • Expensive treatments for genetic disorders are arriving. But who should foot the bill? Nature Editorial. 2019:576:7–8.