The effect of antidrug antibodies on the sustainable efficacy of biologic therapies in rheumatoid arthritis: Practical consequences

Expert Review of Clinical Immunology

Volumn 10, Issue 8, 2014, Pages 1049-1057

  Keiserman, Mauro ^a   Codreanu, Catalin ^b   Handa, Rohini ^c   Xibillé Friedmann, Daniel ^d   Mysler, Eduardo ^e   Briceño, Francisco ^f   Akar, Servet ^g  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b Center of Rheumatic Diseases   (Romania)

^c INDRAPRASTHA APOLLO HOSPITAL   (India)

^d UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^e Organizacion Medica de Investigacion ^*  (Argentina)

^f INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^g IZMIR KATIP CELEBI UNIVERSITY   (Turkey)

Author keywords

TNF antagonists

Indexed keywords

ABATACEPT; ADALIMUMAB; ANTIDRUG ANTIBODY; CERTOLIZUMAB PEGOL; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; GOLIMUMAB; IMMUNOMODULATING AGENT; INFLIXIMAB; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; RITUXIMAB; TOCILIZUMAB; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; ANTIRHEUMATIC AGENT; BLOCKING ANTIBODY; HYBRID PROTEIN; IMMUNOGLOBULIN G; TNFR-FC FUSION PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR;

ADVERSE DRUG REACTION; ANTIGEN BINDING; BIOLOGICAL ACTIVITY; BIOLOGICAL THERAPY; CONCENTRATION (PARAMETERS); COST EFFECTIVENESS ANALYSIS; DRUG EFFICACY; DRUG SAFETY; HUMAN; IMMUNOGENICITY; REVIEW; RHEUMATOID ARTHRITIS; TREATMENT RESPONSE; ANIMAL; ARTHRITIS, RHEUMATOID; DRUG SUBSTITUTION; ECONOMICS; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; TREATMENT WITHDRAWAL;

ANIMALS; ANTIBODIES, BLOCKING; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; DRUG SUBSTITUTION; HUMANS; IMMUNOGLOBULIN G; IMMUNOTHERAPY; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT FUSION PROTEINS; WITHHOLDING TREATMENT;

EID: 84904338095     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2014.926219     Document Type: Review

References (66)

1. Saag KG, Teng GG, Patkar NM, et al. on behalf of the American College of Rheumatology. American College of Rheumatology 2008 recommendations for the use of nonbiologic and biologic disease-modifying antirheumatic drugs in rheumatoid arthritis. Arthritis Rheum 2008; 59(6):762-84
2. Smolen JS, Landewe R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs. Ann Rheum Dis 2010; 69(6):964-75
3. Smolen JS, Landewe R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis 2014;73(3):492-509
4. Wolbink GJ, Aarden LA, Dijkmans BA. Dealing with immunogenicity of biologicals: assessment and clinical relevance. Curr Opin Rheumatol 2009;21(3):211-15
5. Krieckaert CLM, Lems WF. Are we ready for therapeutic drug monitoring of biologic therapeutics? Arthritis Res Ther 2011;13(4): 120
6. Schroff RW, Foon KA, Braty SM, et al. Human autoimmune immunoglobulin responses in patients receiving monoclonal antibody therapy. Cancer Res 1985;45: 879-85
7. Courtney Luck N, Epenetos AA, Moore R. Development of primary and secondary immune response to mouse monoclonal antibodies used in the diagnosis and therapy of malignant neoplasms. Cancer Res 1986;46:6489-91
8. Clarck M. Antibody humanization: a case of the Emperors new clothes? Immunol Today 2000;8:397-402
9. Krieckaert CLM, Bartelds GM, Lems WF, Wolbink GJ. The effect of immunomodulators on the immunogenicity of TNF-blocking therapeutic monoclonal antibodies: a review. Arthritis Res Ther 2010;12(5):217
10. Hwang WY, Foote J. Immunogenecity of engineered antibodies. Methods 2005;36(1): 3-10
11. Jung YO, Kim HA. Recent paradigm shifts in the diagnosis and treatment of rheumatoid arthritis. Korean J Intern Med 2012;27(4):378-87
12. Miltenburger C, Munkombwe M, Lekander I. A Survey of Barriers to Treatment Access in Rheumatoid Arthritis in Major Latin American Countries -Argentina, Brazil and Mexico. March 2010. Available from: www. comparatorreports.se/LA%20RA%20barrier%20report-FINAL. pdf [Last accessed 25 April 2013]
13. 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
14. 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(2):165-78
15. Hoshino M, Yoshio T, Onishi S, Minota S. Influence of antibodies against infliximab and etanercept on the treatment effectiveness of these agents in Japanese patients with rheumatoid arthritis. Mod Rheumatol 2012;22(4):532-40
16. 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(4): 531-5
17. Haraoui B, Pelletier J-P, Martel-Pelletier J. Immunogenicity of biologic agents: a new concern for the practicing rheumatologist? Curr Rheumatol Rep 2007;9(4):265-7
18. Rituxan Prescribing Information. Biogen Idec Inc. and Genentech Inc. February 2010. Available from: www.accessdata.fda. gov/drugsatfda-docs/label/ 2010/103705s5311lbl.pdf [Last accessed 30 May 2013]
19. Levi M, Grange S, Frey N. Exposure-response relationship of tocilizumab, an anti-IL-6 receptor monoclonal antibody, in a large population of patients with rheumatoid arthritis. J Clin Pharmacol 2013;53(2):151-9
20. Genovese MC, Schiff M, Luggen M, et al. Long term safety and efficacy of abatacept through 5 years of treatment in patients with rheumatoid arthritis and an inadequate response to tumor necrosis factor inhibitor therapy. J Rheumatol 2012;39(8):1546-154
21. Schiff M. Subcutaneous abatacept for the treatment of rheumatoid arthritis. Rheumatology (Oxford) 2013;52(6):986-97
22. Weinblatt ME, Keystone EC, Furst D.E., et al. Adalimumab, a fully human anti-tumor necrosis factor a monoclonal antibody, for the treatment of rheumatoid arthritis in patients taking concomitant methotrexate: the ARM.A.DA trial. Arthritis Rheum 2003;48(1):35-45
23. 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. JAM.A. 2011;305(14):1460-8
24. Bendtzen K. Anti-TNF-a biotherapies: perspectives for evidence-based personalized medicine. Immunotherapy 2012;4(11): 1167-79. Available from: www.medscape.com/viewarticle/778245 [Last accessed 20 Nov 2013]
25. Vennegoor A, Rispens T, Strijbis EM, et al. Clinical relevance of serum natalizumab concentration and anti-natalizumab antibodies in multiple sclerosis. Mult Scler 2013;19(5):593-600
26. Aarden L, Ruuls S.R., Wolbink G. Immunogenicity of anti-tumor necrosis factor antibodies -toward improved methods of anti-antibody measurement. Curr Opin Immunol 2008;20(4):431-5
27. Bendtzen K. Immunogenicity of anti-TNF antibodies. In: van de Weert M, Möller EH, editors. Immunogenicity of Biopharmaceuticals. Berlin; Springer: 2008. p189-203
28. Svenson M, Geborek P, Saxne T, Bendtzen K. Monitoring patients treated with anti-TNF-a biopharmaceuticals: assessing serum infliximab and anti-infliximab antibodies. Rheumatology 2007;46(12):1828-34
29. Hart MH, de Vrieze H, Wouters D, et al. Differential effect of drug interference in immunogenicity assays. J Immunol Methods 2011;372(1-2):196-203
30. Lallemand C, Kavrochorianou A, Steenholdt C, et al. Reporter gene assay for the quantification of the activity and neutralizing antibody response to TNFa antagonists. J Immunol Methods 2011; 373(1-2):229-39
31. 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(12): 3782-9
32. 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(12):1947-55
33. 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(3):711-15
34. 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(11): 1739-45
35. 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 (Oxford) 2011;50(8): 1445-52
36. 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(7): 921-6
37. 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(5):817-21
38. 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): 1613-20
39. 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(2):353-63
40. 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(1):40-6
41. Klareskog L, Gaubitz M, Rodriguez-Valverde V, on behalf of the Etanercept Study 301 Investigators. Assessment of long-term safety and efficacy of etanercept in a 5-year extension study in patients with rheumatoid arthritis. Clin Exp Rheumatol 2011;29(2):238-47
42. Jamnitski A, Krieckaert CL, Nurmohamed MT, et al. Patients non-responding to etanercept obtain lower etanercept concentrations compared with responding patients. Ann Rheum Dis 2012; 71(1):88-91
43. Singh SK, Cousens LP, Alvarez D, Mahajan PB. Determinants of immunogenic response to protein therapeutics. Biologicals 2012;40(5):364-8
44. 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(12):3850-5
45. Iannone F, Gremese E, Atzeni F, et al. on behalf of the Gruppo Italiano di Studio sulle Early Arthritides (GISEA). Longterm retention of tumor necrosis factor-a inhibitor therapy in a large Italian cohort of patients with rheumatoid arthritis from the GISEA registry: an appraisal of predictors. J Rheumatol 2012;39(6): 1179-84
46. Hetland ML, Christensen IJ, Tarp U, et al. on behalf of all Departments of Rheumatology in Denmark. 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(1):22-32
47. 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(1):31-8
48. de Punder YM, Fransen J, Kievit W, et al. The prevalence of clinical remission in RA patients treated with anti-TNF: results from the Dutch Rheumatoid Arthritis Monitoring (DREAM) registry. Rheumatology (Oxford) 2012;51(9): 1610-17
49. Kvien TK, Heiberg MS, Lie E, et al. A Norwegian DM.A.RD register: prescriptions of DM.A.RDs and biological agents to patients with inflammatory rheumatic diseases. Clin Exp Rheumatol 2005;23(Suppl 39):S188-94
50. 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
51. 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
52. Haraoui B, Cameron L, Ouellet M, White B. 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(1):31-6
53. 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(3):R105. Available from: www.arthritis-research.com/content/13/3/R105
54. Toki H, Momohara S, Tsukahara S, Ikari K. Infusion reaction to infliximab in a patient with rheumatoid arthritis after discontinuation over 1 year and readministration. J Rheumatol 2008;35(9): 1896-7
55. Descotes J, Gouraud A. Clinical immunotoxicity of therapeutic proteins. Expert Opin Drug Metab Toxicol 2008;4: 1537-49
56. Dubey S, Kerrigan N, Mills K, Scott DG. Bronchospasm associated with anti-TNF treatment. Clin Rheumatol 2009;28:989-92
57. 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(4): 877-83
58. 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(7):1134-42
59. Emery P. Optimizing outcomes in patients with rheumatoid arthritis and an inadequate response to anti-TNF treatment. Rheumatology (Oxford) 2012;51(Suppl 5): v22-30
60. 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(2):284-8
61. Emery P, Keystone E, Tony HP, et al. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis 2008;67(11):1516-23
62. Genovese MC, Becker JC, Schiff M, et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005;353(11):1114-23
63. Emery P, Fleischmann R, Filipowicz-Sosnowska A, et al. on behalf of the DANCER Study Group. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum 2006;54(5):1390-400
64. Solau-Gervais E, Laxenaire N, Cortet B, et al. Lack of efficacy of a third tumour necrosis factor alpha antagonist after failure of a soluble receptor and a monoclonal antibody. Rheumatology (Oxford) 2006; 45(9):1121-4
65. Blom M, Kievit W, Fransen J, et al. The reason for discontinuation of the first tumor necrosis factor (TNF) blocking agent does not influence the effect of a second TNF blocking agent in patients with rheumatoid arthritis. J Rheumatol 2009;36(10):2171-7
66. Garcês 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(6):1138-43