Immunogenicity of anti-TNF biologic agents in the treatment of rheumatoid arthritis

Bibliography

• Papers of special note have been highlighted as either of interest (•) or of considerable interest (••) to readers.
   Google Scholar
• National Collaborating Centre for Chronic Conditions. Rheumatoid arthritis: national clinical guideline for management and treatment in adults. London: Royal College of Physicians; 2009.
   Google Scholar
• Smolen JS, Aletaha D, Bijlsma JW, et al. Treating rheumatoid arthritis to target: recommendations of an international task force. Ann Rheum Dis. 2010;69:631–637.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Landewé R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying anti-rheumatic drugs: 2013 update. Ann Rheum Dis. 2014;73:492–509.
   PubMed Web of Science ®Google Scholar
• Singh JA, Furst DE, Bharat A, et al. Update of the 2008 American College of Rheumatology recommendations for the use of disease-modifying anti-rheumatic drugs and biologic agents in the treatment of rheumatoid arthritis. Arthritis Care Res (Hoboken). 2012;2012(64):625–639.
   Web of Science ®Google Scholar
• Jung YO, Kim HA. Recent paradigm shifts in the diagnosis and treatment of rheumatoid arthritis. Korean J Intern Med. 2012;27:378–387.
   PubMed Web of Science ®Google Scholar
• Wu B, Song Y, Leng L, et al. Treatment of moderate rheumatoid arthritis with different strategies in a health resource-limited setting: a cost-effectiveness analysis in the era of biosimilars. Clin Exp Rheumatol. 2015;33:20–26.
   PubMed Web of Science ®Google 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;72:1613–1620.
   PubMed Web of Science ®Google Scholar
• Dörner T, Strand V, Castañeda-Hernández G, et al. The role of biosimilars in the treatment of rheumatic diseases. Ann Rheum Dis. 2013;72:322–328.
   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
• 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
• Vincent FB, Morand EF, Murphy K, et al. Anti-drug antibodies (ADAb) to tumour necrosis factor (TNF)-specific neutralizing agents in chronic inflammatory diseases: a real issue, a clinical perspective. Ann Rheum Dis. 2013;72:165–178.
   PubMed Web of Science ®Google Scholar
• Hwang WY, Foote J. Immunogenicity of engineered antibodies. Methods. 2005;36:3–10.
   PubMed Web of Science ®Google Scholar
• Clarck M. Antibody humanization: a case of the ‘Emperor’s new clothes’? Immunol Today. 2000;8:397–402.
   Google Scholar
• Bartelds GM, Krieckaert CL, Nurmohamed MT, et al. Development of anti-drug 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

•• The first large prospective study on the effect of antidrug antibody on the clinical efficacy of the anti-TNF monoclonal.

• Wolbink GJ, Vis M, Lems W, et al. Development of antiinfliximab antibodies and relationship to clinical response in patients with rheumatoid arthritis. Arthritis Rheum. 2006;54:711–715.
   PubMed Web of Science ®Google Scholar
• Pascual-Salcedo D, Plasencia C, Ramiro S, et al. Influence of immunogenicity on the efficacy of long-term treatment with infliximab in rheumatoid arthritis. Rheumatology. 2011;50:1445–1452.
   PubMed Web of Science ®Google Scholar
• Daïen CI, Daïen V, Parussini E, et al. Etanercept concentration in patients with rheumatoid arthritis and its potential influence on treatment decisions: a pilot study. J Rheumatol. 2012;39:1533–1538.
   PubMed Web of Science ®Google Scholar

• A pilot study on the effect of drug level (etanercept) on clinical efficacy when used in patients with rheumatoid arthritis.

• de Vries MK, van der Horst-Bruinsma IE, Nurmohamed MT, et al. Immunogenicity does not influence treatment with etanercept in patients with ankylosing spondylitis. Ann Rheum Dis. 2009;68:531–535.
   PubMed Web of Science ®Google Scholar
• Dore RK, Mathews S, Schechtman J, et al. The immunogenicity, safety, and efficacy of etanercept liquid administered once weekly in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2007;25:40–46.
   PubMed Web of Science ®Google Scholar
• Garcês 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

• A meta-analysis of 17 studies on the effect of antidrug antibodies on drug response in various immune-mediated inflammatory diseases.

• Kaine J, Gladstein G, Strusberg I, et al. Evaluation of abatacept administered subcutaneously in adults with active rheumatoid arthritis: impact of withdrawal and reintroduction on immunogenicity, efficacy and safety (Phase IIIb ALLOW study). Ann Rheum Dis. 2012;71:38–44.
   PubMed Web of Science ®Google Scholar
• Schiff M. Subcutaneous abatacept for the treatment of rheumatoid arthritis. Rheumatology (Oxford). 2013;52:986–997.
   PubMed Web of Science ®Google Scholar
• Amano K, Matsubara T, Inoue H, et al. Long-term safety and efficacy of treatment with subcutaneous abatacept in Japanese patients with RA who were MTX inadequate responders – 76-week results. Ann Rheum Dis. 2013;72(Suppl. 3):458.
   PubMed Web of Science ®Google Scholar
• Toki H, Momohara S, Tsukahara S, et al. Infusion reaction to infliximab in a patient with rheumatoid arthritis after discontinuation over 1 year and readministration. J Rheumatol. 2008;35:1896–1897.
   PubMed Web of Science ®Google Scholar
• Bartelds GM, Wijbrandts CA, Nurmohamed MT, et al. Anti-infliximab and anti-adalimumab antibodies in relation to response to adalimumab in infliximab switchers and anti-tumour necrosis factor naive patients: a cohort study. Ann Rheum Dis. 2010;69:817–821.
   PubMed Web of Science ®Google Scholar

• Preliminary observation that the chance of antibodies to one anti-TNF agent is higher in patients who have history of antibodies against other anti-TNF agents.

• Schellekens H. The immunogenicity of therapeutic proteins. Discov Med. 2010;9:560–564.
   PubMed Web of Science ®Google Scholar
• Bartelds GM, Wijbrandts CA, Nurmohamed MT, et al. Anti-adalimumab antibodies in rheumatoid arthritis patients are associated with interleukin-10 gene polymorphisms. Arthritis Rheum. 2009;60:2541–2542.
   PubMed Web of Science ®Google Scholar
• Albert D, Dunham J, Khan S, et al. Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythematosus. Ann Rheum Dis. 2008;67:1724–1731.
   PubMed Web of Science ®Google Scholar
• Krieckaert C, Rispens T, Wolbink G. Immunogenicity of biological therapeutics: from assay to patient. Curr Opin Rheumatol. 2012;24:306–311.
   PubMed Web of Science ®Google Scholar
• Krieckaert CLM, Bartelds GM, Lems WF, et al. The effect of immunomodulators on the immunogenicity of TNF-blocking therapeutic monoclonal antibodies: a review. Arthritis Res Ther. 2010;12:217.
   PubMed Web of Science ®Google Scholar
• Jani M, Barton A, Warren RB, et al. The role of DMARDs in reducing the immunogenicity of TNF inhibitors in chronic inflammatory diseases. Rheumatology (Oxford). 2014;53:213–222.
   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
• Krieckaert CL, Nurmohamed MT, Wolbink GJ. Methotrexate reduces immunogenicity in adalimumab treated rheumatoid arthritis patients in a dose dependent manner. Ann Rheum Dis. 2012;71:1914–1915.
   PubMed Web of Science ®Google Scholar
• Krieckaert CLM, Lems WF. Are we ready for therapeutic drug monitoring of biologic therapeutics? Arthritis Res Ther. 2011;13:120.
   PubMed Web of Science ®Google Scholar
• Chen DY, Chen YM, Tsai WC, et al. Significant associations of antidrug antibody levels with serum drug trough levels and clinical effectiveness of adalimumab and etanercept treatment in rheumatoid arthritis. Ann Rheum Dis. 2015;74:e16.
   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 inhibitor infliximab. Arthritis Rheum. 2006;54:3782–3789.
   PubMed Web of Science ®Google Scholar
• Bartelds GM, Wijbrandts CA, Nurmohamed MT, et al. Clinical response to adalimumab: relationship to antiadalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis. Ann Rheum Dis. 2007;66:921–926.
   PubMed Web of Science ®Google Scholar
• Lipsky PE, van der Heijde DM, St Clair EW, et al. On behalf of the Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-tumor necrosis factor trial in rheumatoid arthritis with concomitant therapy study group. N Engl J Med. 2000;343:1594–1602.
   PubMed Web of Science ®Google Scholar
• Maini RN, Breedveld FC, Kalden JR, et al. Therapeutic efficacy of multiple intravenous infusions of anti-tumor necrosis factor alpha monoclonal antibody combined with low-dose weekly methotrexate in rheumatoid arthritis. Arthritis Rheum. 1998;41:1552–1563.
   PubMed Web of Science ®Google Scholar
• Radstake TR, Svenson M, Eijsbouts AM, et al. Formation of antibodies against infliximab and adalimumab strongly correlates with functional drug levels and clinical responses in rheumatoid arthritis. Ann Rheum Dis. 2009;68:1739–1745.
   PubMed Web of Science ®Google Scholar
• Miyasaka N. on behalf of the CHANGE Study Investigators. Clinical investigation in highly disease-affected rheumatoid arthritis patients in Japan with adalimumab applying standard and general evaluation: the CHANGE study. Mod Rheumatol. 2008;18:252–262.
   PubMed Web of Science ®Google Scholar
• Van de Putte LBA, Atkins C, Malaise M, et al. Efficacy and safety of adalimumab as monotherapy in patients with rheumatoid arthritis for whom previous disease modifying anti-rheumatic drug treatment has failed. Ann Rheum Dis. 2004;63:508–516.
   PubMed Web of Science ®Google Scholar
• Baert F, Noman M, Vermeire S, et al. Influence of immunogenicity on the long-term efficacy of infliximab in Crohn’s disease. N Engl J Med. 2003;348:601–608.
   PubMed Web of Science ®Google Scholar
• Hanauer SB, Feagan BG, Lichtenstein GR, et al. on behalf of the ACCENT I Study Group. Maintenance infliximab for Crohn’s disease: the ACCENT I randomised trial. Lancet. 2002;359:1541–1549.
   PubMed Web of Science ®Google Scholar
• Sands BE, Anderson FH, Bernstein CN, et al. Infliximab maintenance therapy for fistulizing Crohn’s disease. N Engl J Med. 2004;350:876–885.
   PubMed Web of Science ®Google Scholar
• Karmiris K, Paintaud G, Noman M, et al. Influence of trough serum levels and immunogenicity on long-term outcome of adalimumab therapy in Crohn’s disease. Gastroenterology. 2009;137:1628–1640.
   PubMed Web of Science ®Google Scholar
• Sandborn WJ, Hanauer SB, Rutgeerts P, et al. Adalimumab for maintenance treatment of Crohn’s disease: results of the CLASSIC II trial. Gut. 2007;56:1232–1239.
   PubMed Web of Science ®Google Scholar
• West RL, Zelinkova Z, Wolbink GJ, et al. Immunogenicity negatively influences the outcome of adalimumab treatment in Crohn’s disease. Aliment Pharmacol Ther. 2008;28:1122–1126.
   PubMed Web of Science ®Google Scholar
• Hanauer SB, Sandborn WJ, Rutgeerts P, et al. Human anti-tumor necrosis factor monoclonal antibody (adalimumab) in Crohn’s disease: the CLASSIC-I trial. Gastroenterology. 2006;130:323–333.
   PubMed Web of Science ®Google Scholar
• Lovell DJ, Ruperto N, Goodman S, et al. On behalf of the Pediatric Rheumatology Collaborative Study Group and the Pediatric Rheumatology International Trials Organisation. Adalimumab with or without methotrexate in juvenile rheumatoid arthritis. N Engl J Med. 2008;359:810–820.
   PubMed Web of Science ®Google Scholar
• De Vries MK, Wolbink GJ, Stapel SO, et al. Decreased clinical response to infliximab in ankylosing spondylitis is correlated with anti-infliximab formation. Ann Rheum Dis. 2007;66:1252–1254.
   PubMed Web of Science ®Google Scholar
• De Vries MK, Brouwer E, van der Horst-Bruinsma IE, et al. Decreased clinical response to adalimumab in ankylosing spondylitis is associated with antibody formation. Ann Rheum Dis. 2009;68:1787–1788.
   PubMed Web of Science ®Google Scholar
• Van Kuijk AW, de Groot M, Stapel SO, et al. Relationship between the clinical response to adalimumab treatment and serum levels of adalimumab and anti-adalimumab antibodies in patients with psoriatic arthritis. Ann Rheum Dis. 2010;69:624–625.
   PubMed Web of Science ®Google Scholar
• Lecluse LL, Driessen RJ, Spuls PI, et al. Extent and clinical consequences of antibody formation against adalimumab in patients with plaque psoriasis. Arch Dermatol. 2010;146:127–132.
   PubMed Web of Science ®Google Scholar
• Smolen J, Landewé RB, Mease P, et al. Efficacy and safety of certolizumab pegol plus methotrexate in active rheumatoid arthritis: the RAPID 2 study. A randomized controlled trial. Ann Rheum Dis. 2009;68:797–804.
   PubMed Web of Science ®Google Scholar
• Bendtzen K. Anti-TNF-α biotherapies: perspectives for evidence-based personalized medicine. Immunotherapy. 2012;4:1167–1179.
   PubMed Web of Science ®Google Scholar
• Tracey D, Klareskog L, Sasso EH, et al. Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacol Ther. 2008;117:244–279.
   PubMed Web of Science ®Google 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
• Svenson M, Geborek P, Saxne T, et al. Monitoring patients treated with anti-TNF-biopharmaceuticals: assessing serum infliximab and anti-infliximab antibodies. Rheumatology. 2007;46:1828–1834.
   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

• A study which shows that different assay methods may affect the incidence and levels of antibodies to the anti-TNF monoclonals.

• Lallemand C, Kavrochorianou A, Steenholdt C, et al. Reporter gene assay for the quantification of the activity and neutralizing antibody response to TNF- antagonists. J Immunol Meth. 2011;373:229–239.
   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
• van der Maas A, van den Bemt BJF, 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
• van den Bemt BJF, den Broeder AA, Wolbink GJ, et al. Anti-infliximab antibodies are already detectable in most patients with rheumatoid arthritis halfway through an infusion cycle: an open-label pharmacokinetic cohort study. BMC Musculoskelet Disord. 2011;12:12.
   PubMedGoogle Scholar
• Mok CC, van der Kleij D, Wolbink GJ. Drug levels, anti-drug antibodies, and clinical efficacy of the anti-TNFα biologics in rheumatic diseases. Clin Rheumatol. 2013;32:1429–1435.
   PubMed Web of Science ®Google Scholar
• Lai CH, Lai MS, Lai KL, et al. Nationwide population-based epidemiologic study of rheumatoid arthritis in Taiwan. Clin Exp Rheumatol. 2012;30:358–363.
   PubMed Web of Science ®Google Scholar
• Yeo KJ, Leong PY, Chen CY, et al. Immunogenicity of adalimumab in ankylosing spondylitis in Taiwan: A registry-based cohort study. [Submitted for publication]
   Google Scholar
• Kneepkens EL, Wei JC, Nurmohamed MT, et al. Immunogenicity, adalimumab levels and clinical response in ankylosing spondylitis patients during 24 weeks of follow-up. Ann Rheum Dis. 2013;72(Suppl. s3):518.
   Google Scholar
• Ducourau E, Mulleman D, Paintaud G, et al. Antibodies toward infliximab are associated with low infliximab concentration at treatment initiation and poor infliximab maintenance in rheumatic diseases. Arthritis Res Ther. 2011;13:R105.
   PubMed Web of Science ®Google Scholar
• REMICADE® (infliximab) Prescribing Information. Janssen Biotech, Inc. 2013. Available from: http://www.remicade.com/shared/product/remicade/prescribing-information.pdf
   Google Scholar
• Van der Laken CJ, Voskuyl AE, Roos JC, et al. Imaging and serum analysis of immune complex formation of radiolabelled infliximab and anti-infliximab in responders and non-responders to therapy for rheumatoid arthritis. Ann Rheum Dis. 2007;66:253–256.
   PubMed Web of Science ®Google Scholar
• Enbrel® (etanercept) Prescribing Information 2013. Amgen. September 2013. Available from: http://pi.amgen.com/united_states/enbrel/derm/enbrel_pi.pdf
   Google Scholar
• Batycka-Baran A, Flaig M, Molin S, et al. Etanercept-induced injection site reactions: potential pathomechanisms and clinical assessment. Expert Opin Drug Saf 77. 2012;11:911–921.
   PubMed Web of Science ®Google Scholar
• Descotes J, Gouraud A. Clinical immunotoxicity of therapeutic proteins. Expert Opin Drug Metab Toxicol. 2008;4:1537–1549.
   PubMed Web of Science ®Google Scholar
• Korswagen LA, Bartelds GM, Krieckaert CL, et al. Venous and arterial thromboembolic events in adalimumab-treated patients with antiadalimumab antibodies: a case series and cohort study. Arthritis Rheum. 2011;63:877–883.
   PubMed Web of Science ®Google Scholar
• Markatseli TE, Alamanos Y, Saougou I, et al. Survival of TNF-alpha antagonists in rheumatoid arthritis: a long-term study. Clin Exp Rheumatol. 2012;30:31–38.
   PubMed Web of Science ®Google Scholar
• Iannone F, Gremese E, Atzeni F, et al. Long term retention of tumor necrosis factor-α inhibitor therapy in a large Italian cohort of patients with rheumatoid arthritis from the GISEA registry: an appraisal of predictors. J Rheumatol. 2012;39:1179–1184.
   PubMed Web of Science ®Google Scholar
• Hetland ML, Christensen IJ, Tarp U, et al. Direct comparison of treatment responses, remission rates, and drug adherence in patients with rheumatoid arthritis treated with adalimumab, etanercept, or infliximab: results from eight years of surveillance of clinical practice in the nationwide Danish DANBIO registry. Arthritis Rheum. 2010;62:22–32.
   PubMed Web of Science ®Google Scholar
• Mok CC, Chan KY, Lee KL, et al on behalf of the Hong Kong Society of Rheumatology. Factors associated with withdrawal of the anti-TNFα biologics in the treatment of rheumatic diseases: data from the Hong Kong Biologics Registry. Int J Rheum Dis. 2014;17(Suppl. 3):1–8.
   Google Scholar
• Maini RN, Breedveld FC, Kalden JR, et al. Sustained improvement over two years in physical function, structural damage, and signs and symptoms among patients with rheumatoid arthritis treated with infliximab and methotrexate. Arthritis Rheum. 2004;50:1051–1065.
   PubMed Web of Science ®Google Scholar
• Haraoui B, Cameron L, Ouellet M, et al. Anti-infliximab antibodies in patients with rheumatoid arthritis who require higher doses of infliximab to achieve or maintain a clinical response. J Rheumatol. 2006;33:31–36.
   PubMed Web of Science ®Google Scholar
• Cohen SB. Efficacy and safety of TNF inhibitors in the treatment of rheumatoid arthritis. Medscape 2007. Available from: http://www.medscape.org/viewarticle/567983
   Google Scholar
• Greenberg JD, Reed G, Decktor D, et al. On behalf of the CORRONA Investigators. A comparative effectiveness study of adalimumab, etanercept and infliximab in biologically naive and switched rheumatoid arthritis patients: results from the US CORRONA registry. Ann Rheum Dis. 2012;71:1134–1142.
   PubMed Web of Science ®Google Scholar
• Emery P. Optimizing outcomes in patients with rheumatoid arthritis and an inadequate response to anti-TNF treatment. Rheumatology (Oxford). 2012;51(Suppl. 5):v22–v30.
   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

• Preliminary observation that the chance of having a clinical response to a second anti-TNF agent is higher in patients who fail the first anti-TNF agent because of anti-drug antibodies.