Biological anti-TNF drugs: immunogenicity underlying treatment failure and adverse events

References

• Vincent FB, Morand EF, Murphy K, et al. Antidrug antibodies (ADAb) to tumour necrosis factor (TNF)-specific neutralising agents in chronic inflammatory diseases: a real issue, a clinical perspective. Ann Rheum Dis. 2013;72:165–178.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Personalized medicine: theranostics (therapeutics diagnostics) essential for rational use of tumor necrosis factor-alpha antagonists. Discov Med. 2013;15:201–211.
   PubMed Web of Science ®Google Scholar
• Malviya G, Salemi S, Lagana B, et al. Biological therapies for rheumatoid arthritis: progress to date. BioDrugs. 2013;27:329–345.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Anti-TNF-alpha biotherapies: perspectives for evidence-based personalized medicine. Immunotherapy. 2012;4:1167–1179.
   PubMed Web of Science ®Google Scholar
• Garces S, Demengeot J, Benito-Garcia E. The immunogenicity of anti-TNF therapy in immune-mediated inflammatory diseases: a systematic review of the literature with a meta-analysis. Ann Rheum Dis. 2013;72:1947–1955.
   PubMed Web of Science ®Google Scholar
• Atzeni F, Talotta R, Salaffi F, et al. Immunogenicity and autoimmunity during anti-TNF therapy. Autoimmun Rev. 2013;12:703–708.
   PubMed Web of Science ®Google Scholar
• Van Schouwenburg PA, Rispens T, Wolbink GJ. Immunogenicity of anti-TNF biologic therapies for rheumatoid arthritis. Nat Rev Rheumatol. 2013;9:164–172.
   PubMed Web of Science ®Google Scholar
• Maneiro JR, Salgado E, Gomez-Reino JJ. Immunogenicity of monoclonal antibodies against tumor necrosis factor used in chronic immune-mediated inflammatory conditions: systematic review and meta-analysis. JAMA Intern Med. 2013;173:1416–1428.
   PubMed Web of Science ®Google Scholar
• Takeuchi T. Revolutionary change in rheumatoid arthritis management with biological therapy. Keio J Med. 2011;60:75–81.
   PubMedGoogle Scholar
• Kohler G, Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975;256:495–497.
   PubMed Web of Science ®Google Scholar
• Brekke OH, Sandlie I. Therapeutic antibodies for human diseases at the dawn of the twenty-first century. Nat Rev Drug Discov. 2003;2:52–62.
   PubMed Web of Science ®Google Scholar
• Morrison SL, Johnson MJ, Herzenberg LA, et al. Chimeric human antibody molecules: mouse antigen-binding domains with human constant region domains. Proc Natl Acad Sci U S A. 1984;81:6851–6855.
   PubMed Web of Science ®Google Scholar
• Jones PT, Dear PH, Foote J, et al. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature. 1986;321:522–525.
   PubMed Web of Science ®Google Scholar
• Chapman AP. PEGylated antibodies and antibody fragments for improved therapy: a review. Adv Drug Deliv Rev. 2002;54:531–545.
   PubMed Web of Science ®Google Scholar
• Da Mota LM, Cruz BA, Brenol CV, et al. 2012 Brazilian Society of Rheumatology Consensus for the treatment of rheumatoid arthritis. Rev Bras Reumatol. 2012;52:152–174.
   PubMed Web of Science ®Google Scholar
• Borchers AT, Leibushor N, Cheema GS, et al. Immune-mediated adverse effects of biologicals used in the treatment of rheumatic diseases. J Autoimmun. 2011;37:273–288.
   PubMed Web of Science ®Google Scholar
• Elliott MJ, Maini RN, Feldmann M, et al. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to tumor necrosis factor alpha. Arthritis Rheum. 1993;36:1681–1690.
   PubMed Web of Science ®Google Scholar
• 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;68:789–796.
   PubMed Web of Science ®Google Scholar
• Ghezzi P, Cerami A. Tumor necrosis factor as a pharmacological target. Mol Biotechnol. 2005;31:239–244.
   PubMed Web of Science ®Google Scholar
• Spinelli FR, Valesini G. Immunogenicity of anti-tumour necrosis factor drugs in rheumatic diseases. Clin Exp Rheumatol. 2013;31:954–963.
   PubMed Web of Science ®Google Scholar
• Rau R. Adalimumab (a fully human anti-tumour necrosis factor alpha monoclonal antibody) in the treatment of active rheumatoid arthritis: the initial results of five trials. Ann Rheum Dis. 2002;61(Suppl 2):ii70–ii73.
   PubMedGoogle Scholar
• Meier FM, Frerix M, Hermann W, et al. Current immunotherapy in rheumatoid arthritis. Immunotherapy. 2013;5:955–974.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency EMA. Guideline on immunogenicity assessment of biotechnology-derived therapeutic proteins 2007. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500003946.pdf
   Google Scholar
• Federal Drug Administration FDA. Guidance for industry. Assay development for immunogenicity testing of therapeutic proteins 2009. Available from: http://www.fda.gov/downloads/Drugs/./Guidances/UCM192750.pdf
   Google Scholar
• Keystone EC, Schiff MH, Kremer JM, et al. Once-weekly administration of 50 mg etanercept in patients with active rheumatoid arthritis: results of a multicenter, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2004;50:353–363.
   PubMed Web of Science ®Google Scholar
• Emi Aikawa N, De Carvalho JF, Artur Almeida Silva C, et al. Immunogenicity of anti-TNF-alpha agents in autoimmune diseases. Clin Rev Allergy Immunol. 2010;38:82–89.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Immunogenicity of anti-TNF-alpha biotherapies: II. Clinical relevance of methods used for anti-drug antibody detection. Front Immunol. 2015;6:109.
   PubMed Web of Science ®Google Scholar
• Jamnitski A, Bartelds GM, Nurmohamed MT, et al. The presence or absence of antibodies to infliximab or adalimumab determines the outcome of switching to etanercept. Ann Rheum Dis. 2011;70:284–288.
   PubMed Web of Science ®Google Scholar
• Krieckaert CL, Jamnitski A, Nurmohamed MT, et al. Comparison of long-term clinical outcome with etanercept treatment and adalimumab treatment of rheumatoid arthritis with respect to immunogenicity. Arthritis Rheum. 2012;64:3850–3855.
   PubMed Web of Science ®Google Scholar
• Vande Casteele N, Therapeutic Drug KR. Monitoring of golimumab in the treatment of ulcerative colitis. Pharm Res. 2017.
   PubMed Web of Science ®Google Scholar
• Xue L, Rup B. Evaluation of pre-existing antibody presence as a risk factor for posttreatment anti-drug antibody induction: analysis of human clinical study data for multiple biotherapeutics. Aaps J. 2013;15:893–896.
   PubMed Web of Science ®Google Scholar
• Furst DE, Keystone EC, So AK, et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2012. Ann Rheum Dis. 2013;72(Suppl 2):ii2–ii34.
   PubMed Web of Science ®Google Scholar
• Allez M, Karmiris K, Louis E, et al. Report of the ECCO pathogenesis workshop on anti-TNF therapy failures in inflammatory bowel diseases: definitions, frequency and pharmacological aspects. J Crohns Colitis. 2010;4:355–366.
   PubMed Web of Science ®Google Scholar
• Emery P. Optimizing outcomes in patients with rheumatoid arthritis and an inadequate response to anti-TNF treatment. Rheumatology. 2012;51(Suppl 5):v22–v30.
   PubMed Web of Science ®Google Scholar
• Hausmann OV, Seitz M, Villiger PM, et al. The complex clinical picture of side effects to biologicals. Med Clin North Am. 2010;94:791-804, xi-ii.
   PubMed Web of Science ®Google Scholar
• Schellekens H. Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin Ther. 2002;24:1720-1740; discussion 19.
   PubMed Web of Science ®Google Scholar
• Van Der Maas A, Van Den Bemt BJ, Wolbink G, et al. Low infliximab serum trough levels and anti-infliximab antibodies are prevalent in rheumatoid arthritis patients treated with infliximab in daily clinical practice: results of an observational cohort study. BMC Musculoskelet Disord. 2012;13:184.
   PubMed Web of Science ®Google Scholar
• Genovese MC, Covarrubias A, Leon G, et al. Subcutaneous abatacept versus intravenous abatacept: a phase IIIb noninferiority study in patients with an inadequate response to methotrexate. Arthritis Rheum. 2011;63:2854–2864.
   PubMed Web of Science ®Google Scholar
• Schellekens H. Factors influencing the immunogenicity of therapeutic proteins. Nephrol Dial Transplant. 2005;20(Suppl 6):vi3–vi9.
   PubMedGoogle Scholar
• Porter S. Human immune response to recombinant human proteins. J Pharm Sci. 2001;90:1–11.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Is there a need for immunopharmacologic guidance of anti-tumor necrosis factor therapies? Arthritis Rheum. 2011;63:867–870.
   PubMed Web of Science ®Google Scholar
• Colombel JF, Sandborn WJ, Reinisch W, et al. Infliximab, azathioprine, or combination therapy for Crohn’s disease. N Engl J Med. 2010;362:1383–1395.
   PubMed Web of Science ®Google Scholar
• Farrell RJ, Alsahli M, Jeen YT, et al. Intravenous hydrocortisone premedication reduces antibodies to infliximab in Crohn’s disease: a randomized controlled trial. Gastroenterology. 2003;124:917–924.
   PubMed Web of Science ®Google Scholar
• Vermeire S, Noman M, Van Assche G, et al. Effectiveness of concomitant immunosuppressive therapy in suppressing the formation of antibodies to infliximab in Crohn’s disease. Gut. 2007;56:1226–1231.
   PubMed Web of Science ®Google Scholar
• Wolbink GJ, Aarden LA, Dijkmans BA. Dealing with immunogenicity of biologicals: assessment and clinical relevance. Curr Opin Rheumatol. 2009;21:211–215.
   PubMed Web of Science ®Google Scholar
• Gupta S, Indelicato SR, Jethwa V, et al. Recommendations for the design, optimization, and qualification of cell-based assays used for the detection of neutralizing antibody responses elicited to biological therapeutics. J Immunol Methods. 2007;321:1–18.
   PubMed Web of Science ®Google Scholar
• Bendtzen K, Geborek P, Svenson M, et al. Individualized monitoring of drug bioavailability and immunogenicity in rheumatoid arthritis patients treated with the tumor necrosis factor alpha inhibitor infliximab. Arthritis Rheum. 2006;54:3782–3789.
   PubMed Web of Science ®Google Scholar
• Bartelds GM, Krieckaert CL, Nurmohamed MT, et al. Development of antidrug antibodies against adalimumab and association with disease activity and treatment failure during long-term follow-up. JAMA. 2011;305:1460–1468.
   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;64:704–707.
   PubMed Web of Science ®Google Scholar
• Kim MS, Lee SH, Song MY, et al. Comparative analyses of complex formation and binding sites between human tumor necrosis factor-alpha and its three antagonists elucidate their different neutralizing mechanisms. J Mol Biol. 2007;374:1374–1388.
   PubMed Web of Science ®Google Scholar
• Kohno T, Tam LT, Stevens SR, et al. Binding characteristics of tumor necrosis factor receptor-Fc fusion proteins vs anti-tumor necrosis factor mAbs. J Investig Dermatol Symp Proc. 2007;12:5–8.
   PubMedGoogle Scholar
• Aarden L, Ruuls SR, Wolbink G. Immunogenicity of anti-tumor necrosis factor antibodies-toward improved methods of anti-antibody measurement. Curr Opin Immunol. 2008;20:431–435.
   PubMed Web of Science ®Google Scholar
• Hart MH, De Vrieze H, Wouters D, et al. Differential effect of drug interference in immunogenicity assays. J Immunol Methods. 2011;372:196–203.
   PubMed Web of Science ®Google Scholar
• Tatarewicz S, Miller JM, Swanson SJ, et al. Rheumatoid factor interference in immunogenicity assays for human monoclonal antibody therapeutics. J Immunol Methods. 2010;357:10–16.
   PubMed Web of Science ®Google Scholar
• Van Schouwenburg PA, Bartelds GM, Hart MH, et al. A novel method for the detection of antibodies to adalimumab in the presence of drug reveals “hidden” immunogenicity in rheumatoid arthritis patients. J Immunol Methods. 2010;362:82–88.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Immunogenicity of Anti-TNF-alpha biotherapies: I. Individualized medicine based on immunopharmacological evidence. Front Immunol. 2015;6:152.
   PubMed Web of Science ®Google Scholar
• Steenholdt C, Ainsworth MA, Tovey M, et al. Comparison of techniques for monitoring infliximab and antibodies against infliximab in Crohn’s disease. Ther Drug Monit. 2013;35:530–538.
   PubMed Web of Science ®Google Scholar
• Lallemand C, Kavrochorianou N, Steenholdt C, et al. Reporter gene assay for the quantification of the activity and neutralizing antibody response to TNFalpha antagonists. J Immunol Methods. 2011;373:229–239.
   PubMed Web of Science ®Google Scholar
• Garces S, Antunes M, Benito-Garcia E, et al. A preliminary algorithm introducing immunogenicity assessment in the management of patients with RA receiving tumour necrosis factor inhibitor therapies. Ann Rheum Dis. 2014;73:1138–1143.
   PubMed Web of Science ®Google Scholar
• Steenholdt C, Brynskov J, Thomsen OO, et al. Individualised therapy is more cost-effective than dose intensification in patients with Crohn’s disease who lose response to anti-TNF treatment: a randomised, controlled trial. Gut. 2014;63:919–927.
   PubMed Web of Science ®Google Scholar
• Bendtzen K, Ainsworth M, Steenholdt C, et al. Individual medicine in inflammatory bowel disease: monitoring bioavailability, pharmacokinetics and immunogenicity of anti-tumour necrosis factor-alpha antibodies. Scand J Gastroenterol. 2009;44:774–781.
   PubMed Web of Science ®Google Scholar