The immunogenicity of anti-TNF therapy in immune-mediated inflammatory diseases: A systematic review of the literature with a meta-analysis

Annals of the Rheumatic Diseases

Volumn 72, Issue 12, 2013, Pages 1947-1955

  Garcês, Sandra ^a,b,c   Demengeot, Jocelyne ^b   Benito Garcia, Elizabeth ^d  

^a HOSPITAL GARCIA DE ORTA   (Portugal)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c Gulbenkian Programme for Advanced Medical Education   (Portugal)

^d BioEPI Clinical and Translational Research Center   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; AZATHIOPRINE; DRUG ANTIBODY; ETANERCEPT; INFLIXIMAB; MERCAPTOPURINE; METHOTREXATE; TUMOR NECROSIS FACTOR INHIBITOR;

ANTIBODY DETECTION; ANTIBODY RESPONSE; ARTICLE; CROHN DISEASE; DOSE RESPONSE; DRUG EFFICACY; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; IMMUNOGENICITY; IMMUNOPATHOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATORY DISEASE; META ANALYSIS; PRIORITY JOURNAL; PSORIASIS; RADIOIMMUNOASSAY; RHEUMATOID ARTHRITIS; SINGLE DRUG DOSE; SPONDYLARTHRITIS; SYSTEMATIC REVIEW; TREATMENT OUTCOME; ULCERATIVE COLITIS;

ANTI-TNF; AUTOIMMUNE DISEASES; METHOTREXATE;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY FORMATION; ANTIRHEUMATIC AGENTS; ARTHRITIS; AUTOIMMUNE DISEASES; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATORY BOWEL DISEASES; METHOTREXATE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84887489815     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2012-202220     Document Type: Article

References (62)

1. Atzeni F, Sarzi-Puttini P, Gorla R, et al. Switching rheumatoid arthritis treatments: an update. Autoimmun Rev 2011;10:397-403.
2. 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;305:1460-8.
3. 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;66:1252-4.
4. 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;348:601-8.
5. Harding FA, Stickler MM, Razo J, et al. The immunogenicity of humanized and fully human antibodies: residual immunogenicity resides in the CDR regions. MAbs 2010;2:256-65.
6. Aarden L, Ruuls SR, Wolbink G. Immunogenicity of anti-tumor necrosis factor antibodies-toward improved methods of anti-antibody measurement. Curr Opin Immunol 2008;20:431-5.
7. 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.
8. Persselin JE, Stevens RH. Anti-Fab antibodies in humans. Predominance of minor immunoglobulin G subclasses in rheumatoid arthritis. J Clin Invest 1985;76:723-30.
9. Hennig C, Rink L, Fagin U, et al. The influence of naturally occurring heterophilic anti-immunoglobulin antibodies on direct measurement of serum proteins using sandwich ELISAs. J Immunol Methods 2000;235:71-80.
10. Hart MH, De Vrieze H, Wouters D, et al. Differential effect of drug interference in immunogenicity assays. J Immunol Methods 2011;372:196-203.
11. Svenson M, Geborek P, Saxne T, et al. Monitoring patients treated with anti-TNF-alpha biopharmaceuticals: assessing serum infliximab and anti-infliximab antibodies. Rheumatology (Oxford). 2007;46:1828-34.
12. 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;54:711-15.
13. 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;362:82-8.
14. 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;50:1445-52.
15. Rispens T, De Vrieze H, De Groot E, et al. Antibodies to constant domains of therapeutic monoclonal antibodies: anti-hinge antibodies in immunogenicity testing. J Immunol Methods 2012;375:93-9.
16. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008-12.
17. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 2009;62:e1-34.
18. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-88.
19. 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;68:1739-45.
20. Bartelds GM, Wijbrandts CA, Nurmohamed MT, et al. Clinical response to adalimumab: relationship to anti-adalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis. Ann Rheum Dis 2007;66:921-6.
21. Bender NK, Heilig CE, Droll B, et al. Immunogenicity, efficacy and adverse events of adalimumab in RA patients. Rheumatol Int 2007;27:269-74.
22. West RL, Zelinkova Z, Wolbink GJ, et al. Immunogenicity negatively influences the outcome of adalimumab treatment in Crohn's disease. Aliment Pharmacol Ther 2008;28:1122-6.
23. Steenholdt C, Bendtzen K, Brynskov J, et al. Cut-off levels and diagnostic accuracy of infliximab trough levels and anti-infliximab antibodies in Crohn's disease. Scand J Gastroenterol 2011;46:310-18.
24. Plasencia C, Pascual-Salcedo D, Nuno L, et al. Influence of immunogenicity on the efficacy of long-term treatment of spondylarthritis with infliximab. Ann Rheum Dis 2012;71:1955-60.
25. 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;146:127-32.
26. Hoffmann JH, Hartmann M, Enk AH, et al. Autoantibodies in psoriasis as predictors for loss of response and anti-infliximab antibody induction. Br J Dermatol 2011;165:1355-8.
27. 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;68:531-5.
28. 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;69:624-5.
29. 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;71:88-91.
30. Hoshino M, Yoshio T, Onishi S, et al. Influence of antibodies against infliximab and etanercept on the treatment effectiveness of these agents in Japanese patients with rheumatoid arthritis. Mod Rheumatol 2012;22:532-40.
31. Adisen E, Aral A, Aybay C, et al. Anti-infliximab antibody status and its relation to clinical response in psoriatic patients: a pilot study. J Dermatol 2010;37:708-13.
32. 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;56:1226-31.
33. Afif W, Loftus EV Jr, Faubion WA, et al. Clinical utility of measuring infliximab and human anti-chimeric antibody concentrations in patients with inflammatory bowel disease. Am J Gastroenterol 2010;105:1133-9.
34. 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;69:817-21.
35. 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;41:1552-63.
36. 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;354:1932-9.
37. Sandborn WJ, Hanauer SB, Rutgeerts P, et al. Adalimumab for maintenance treatment of Crohn's disease: results of the CLASSIC II trial. Gut 2007;56:1232-9.
38. Hanauer SB, Feagan BG, Lichtenstein GR, et al. Maintenance infliximab for Crohn's disease: the ACCENT I randomised trial. Lancet 2002;359:1541-9.
39. Weinblatt ME, Keystone EC, Furst DE, et al. Adalimumab, a fully human anti-tumor necrosis factor alpha monoclonal antibody, for the treatment of rheumatoid arthritis in patients taking concomitant methotrexate: the ARMADA trial. Arthritis Rheum 2003;48:35-45.
40. Magdelaine-Beuzelin C, Vermeire S, Goodall M, et al. IgG1 heavy chain-coding gene polymorphism (G1m allotypes) and development of antibodies-to-infliximab. Pharmacogenet Genomics 2009;19:383-7.
41. Ben-Horin S, Yavzori M, Katz L, et al. The immunogenic part of infliximab is the F (ab0) 2, but measuring antibodies to the intact inflix+imab molecule is more clinically useful. Gut 2011;60:41-8.
42. Bartelds GM, De Groot E, Nurmohamed MT, et al. Surprising negative association between IgG1 allotype disparity and anti-adalimumab formation: a cohort study. Arthritis Res Ther 2010;12:R221.
43. Van Der Neut Kolfschoten M, Schuurman J, Losen M, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 2007;317:1554-7.
44. 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;25:40-6.
45. Weinblatt ME, Kremer JM, Bankhurst AD, et al. A trial of etanercept, a recombinant tumor necrosis factor receptor:Fc fusion protein, in patients with rheumatoid arthritis receiving methotrexate. N Engl J Med 1999;340:253-9.
46. Moreland LW, Schiff MH, Baumgartner SW, et al. Etanercept therapy in rheumatoid arthritis. A randomized, controlled trial. Ann Intern Med 1999;130:478-86.
47. 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;343:1586-93.
48. Kim HJ, Kammertoens T, Janke M, et al. Establishment of early lymphoid organ infrastructure in transplanted tumors mediated by local production of lymphotoxin alpha and in the combined absence of functional B and T cells. J Immunol 2004;172:4037-47.
49. 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.
50. Noiles K, Vender R. Biologic survival. J Drugs Dermatol 2009;8:329-33.
51. Punzi L, Matucci Cerinic M, Cantini F, et al. Treatment patterns of anti-TNF agents in Italy: an observational study. Reumatismo 2011;63:18-28.
52. Krieckaert CL, Nurmohamed MT, Wolbink GJ. Methotrexate reduces immunogenicity in adalimumab treated rheumatoid arthritis patients in a dose dependent manner. Ann Rheum Dis 2012;71:1914-5.
53. 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;54:3782-9.
54. Mulleman D, Lauferon F, Wendling D, et al. Infliximab in ankylosing spondylitis: alone or in combination with methotrexate? A pharmacokinetic comparative study. Arthritis Res Ther 2011;13:R82.
55. 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;137:1628-40.
56. 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;63:877-83.
57. Rutgeerts P, Feagan BG, Lichtenstein GR, et al. Comparison of scheduled and episodic treatment strategies of infliximab in Crohn's disease. Gastroenterology 2004;126:402-13.
58. Hanauer SB, Wagner CL, Bala M, et al. Incidence and importance of antibody responses to infliximab after maintenance or episodic treatment in Crohn's disease. Clin Gastroenterol Hepatol 2004;2:542-53.
59. Van Gestel AM, Anderson JJ, Van Riel PL, et al. ACR and EULAR improvement criteria have comparable validity in rheumatoid arthritis trials. American College of Rheumatology European League of Associations for Rheumatology. J Rheumatol 1999;26:705-11.
60. Braun J, Pham T, Sieper J, et al. International ASAS consensus statement for the use of anti-tumour necrosis factor agents in patients with ankylosing spondylitis. Ann Rheum Dis 2003;62:817-24.
61. Van Der Heijde D, Lie E, Kvien TK, et al. ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis. Ann Rheum Dis 2009;68:1811-18.
62. Ashcroft DM, Wan Po AL, Williams HC, et al. Clinical measures of disease severity and outcome in psoriasis: a critical appraisal of their quality. Br J Dermatol 1999;141:185-91.