Review article: Immunogenicity of anti-TNF biologics in IBD - The role of patient, product and prescriber factors

Alimentary Pharmacology and Therapeutics

Volumn 38, Issue 10, 2013, Pages 1188-1197

  Moss, A C ^a   Brinks, V ^b   Carpenter, J F ^c  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 MERCAPTOPURINE DERIVATIVE; ADALIMUMAB; AZATHIOPRINE; BETA INTERFERON; CYTOKINE; DRUG ANTIBODY; ERYTHROPOIETIN; HLA ANTIGEN; IMMUNOGLOBULIN; IMMUNOMODULATING AGENT; INFLIXIMAB; INTERLEUKIN 10; METHOTREXATE; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR INHIBITOR;

AGE; ANTIBODY DETECTION; BIOLOGICAL THERAPY; CROHN DISEASE; DISEASE SEVERITY; DRUG ANTIGENICITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DOSE ESCALATION; DRUG DOSE REGIMEN; DRUG FORMULATION; DRUG PACKAGING; DRUG QUALITY; DRUG RESPONSE; DRUG STABILITY; DRUG STORAGE; ENTERITIS; FREEZE THAWING; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; LIGHT EXPOSURE; LOW DRUG DOSE; MAINTENANCE THERAPY; NONHUMAN; PH; PHARMACOGENETICS; PRESCRIPTION; PREVALENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; TEMPERATURE; ULCERATIVE COLITIS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIBODIES; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; BIOLOGICAL PRODUCTS; HUMANS; IMMUNOLOGIC FACTORS; INFLAMMATORY BOWEL DISEASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84885954199     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.12507     Document Type: Review

References (82)

1. Lichtenstein GR, Hanauer SB, Sandborn WJ,. Management of Crohn's disease in adults. Am J Gastroenterol 2009; 104: 465-83.
2. Regueiro M, Siemanowski B, Kip KE, Plevy S,. Infliximab dose intensification in Crohn's disease. Inflamm Bowel Dis 2007; 13: 1093-9.
3. Gisbert JP, Panes J,. Loss of response and requirement of infliximab dose inten-sification in Crohn's disease: a review. Am J Gastroenterol 2009; 104: 760-7.
4. Rostholder E, Ahmed A, Cheifetz AS, Moss AC,. Outcomes after escalation of infliximab therapy in ambulatory patients with moderately active ulcerative colitis. Aliment Pharmacol Ther 2012; 35: 562-7.
5. Peyrin-Biroulet L,. Anti-TNF therapy in inflammatory bowel diseases: a huge review. Minerva Gastroenterol Dietol 2010; 56: 233-43.
6. 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.
7. Waters H, Vanderpoel J, McKenzie S, et al,. Stability of infliximab dosing in inflammatory bowel disease: results from a multicenter US chart review. J Med Econ 2011; 14: 397-402.
8. Colombel JF, Feagan BG, Sandborn WJ, Van Assche G, Robinson AM,. Therapeutic drug monitoring of biologics for inflammatory bowel disease. Inflamm Bowel Dis 2012; 18: 349-58.
9. Rosenberg AS,. Immunogenicity of biological therapeutics: a hierarchy of concerns. Dev Biol (Basel) 2003; 112: 15-21.
10. Sethu S, Govindappa K, Alhaidari M, Pirmohamed M, Park K, Sathish J,. Immunogenicity to biologics: mechanisms, prediction and reduction. Arch Immunol Ther Exp (Warsz) 2012; 60: 331-44.
11. Baert F, Noman M, Vermeire S, Van Assche G, D' Haens G, Carbonez A, Rutgeerts P,. Influence of immunogenicity on the long-term efficacy of infliximab in Crohn's disease. N Engl J Med. 2003; 348: 601-8.
12. 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.
13. Fasanmade AA, Adedokun OJ, Blank M, Zhou H, Davis HM,. Pharmacokinetic properties of infliximab in children and adults with Crohn's disease: a retrospective analysis of data from 2 phase III clinical trials. Clin Ther 2011; 33: 946-64.
14. van den Bemt BJ, 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.
15. Ordas I, Feagan BG, Sandborn WJ,. Therapeutic drug monitoring of tumor necrosis factor antagonists in inflammatory bowel disease. Clin Gastroenterol Hepatol 2012; 10: 1079-87.
16. Ainsworth MA, Bendtzen K, Brynskov J,. Tumor necrosis factor-alpha binding capacity and anti-infliximab antibodies measured by fluid-phase radioimmunoassays as predictors of clinical efficacy of infliximab in Crohn's disease. Am J Gastroenterol 2008; 103: 944-8.
17. Ben Horin S, Yavzori M, Katz L, et al,. The immunogenic part of infliximab is the F(ab')2, but measuring antibodies to the intact infliximab molecule is more clinically useful. Gut 2011; 60: 41-8.
18. Maser EA, Villela R, Silverberg MS, Greenberg GR,. Association of trough serum infliximab to clinical outcome after scheduled maintenance treatment for Crohn's disease. Clin Gastroenterol Hepatol 2006; 4: 1248-54.
19. Seow CH, Newman A, Irwin SP, Steinhart AH, Silverberg MS, Greenberg GR,. Trough serum infliximab: a predictive factor of clinical outcome for infliximab treatment in acute ulcerative colitis. Gut 2010; 59: 49-54.
20. Seow CH, Panaccione R,. Commentary: detection of infliximab levels and anti-infliximab antibodies. Aliment Pharmacol Ther 2013; 37: 153-4.
21. Vande CN, Buurman DJ, Sturkenboom MG, Kleibeuker JH, Vermeire S, Rispens T, van der KD, Gils A, Dijkstra G,. Detection of infliximab levels and anti-infliximab antibodies: a comparison of three different assays. Aliment Pharmacol Ther. 2012; 36: 765-71.
22. Wang SL, Ohrmund L, Hauenstein S, et al,. Development and validation of a homogeneous mobility shift assay for the measurement of infliximab and antibodies-to-infliximab levels in patient serum. J Immunol Methods 2012; 382: 177-88.
23. Nanda KS, Cheifetz AS, Moss AC,. Impact of antibodies to infliximab on clinical outcomes and serum infliximab levels in patients with inflammatory bowel disease (IBD): a meta-analysis. Am J Gastroenterol 2013; 108: 40-7.
24. Khanna R, Sattin BD, Afif W, et al,. Review article: a clinician's guide for therapeutic drug monitoring of infliximab in inflammatory bowel disease. Aliment Pharmacol Ther 2013; 38: 447-59.
25. Batista FD, Harwood NE,. The who, how and where of antigen presentation to B cells. Nat Rev Immunol 2009; 9: 15-27.
26. Fasanmade AA, Adedokun OJ, Olson A, Strauss R, Davis HM,. Serum albumin concentration: a predictive factor of infliximab pharmacokinetics and clinical response in patients with ulcerative colitis. Int J Clin Pharmacol Ther 2010; 48: 297-308.
27. 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: 704-7.
28. 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: 253-6.
29. Ryff JC,. Clinical investigation of the immunogenicity of interferon-alpha 2a. J Interferon Cytokine Res 1997; 17 (Suppl 1): S29-33.
30. Brandse J, Wildenberg M, de Bruyn J, et al,. Fecal loss of infliximab as a cause of lack of response in severe inflammatory bowel disease. Gastroenterology 2013; 142 (Suppl 1): Abstract 157.
31. Chalmers EA, Brown SA, Keeling D, et al,. Early factor VIII exposure and subsequent inhibitor development in children with severe haemophilia A. Haemophilia 2007; 13: 149-55.
32. Gouw SC, Van Der Bom JG, Marijke vdB,. Treatment-related risk factors of inhibitor development in previously untreated patients with hemophilia A: the CANAL cohort study. Blood 2007; 109: 4648-54.
33. Hamalainen A, Sipponen T, Kolho KL,. Serum infliximab concentrations in pediatric inflammatory bowel disease. Scand J Gastroenterol 2013; 48: 35-41.
34. 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.
35. Deegan PB,. Fabry disease, enzyme replacement therapy and the significance of antibody responses. J Inherit Metab Dis 2012; 35: 227-43.
36. 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: 2541-2.
37. Hoffmann S, Cepok S, Grummel V, et al,. HLA-DRB10401 and HLA-DRB10408 are strongly associated with the development of antibodies against interferon-beta therapy in multiple sclerosis. Am J Hum Genet 2008; 83: 219-27.
38. Praditpornsilpa K, Kupatawintu P, Mongkonsritagoon W, et al,. The association of anti-r-HuEpo-associated pure red cell aplasia with HLA-DRB109-DQB10309. Nephrol Dial Transplant 2009; 24: 1545-9.
39. Magira E, Lind C, Baldassano R, Monos D,. The HLA DRß13 residue is associated with the development of human anti-chimeric antibody in some Crohn's patients treated with infliximab. Human Immunol 2009; 70 [ S1 ]: 131.
40. 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.
41. Magdelaine-Beuzelin C, Vermeire S, Goodall M, et al,. IgG1 heavy chain-coding gene polymorphism (G1 m allotypes) and development of antibodies-to-infliximab. Pharmacogenet Genomics 2009; 19: 383-7.
42. Brinks V, Hawe A, Basmeleh AH, et al,. Quality of original and biosimilar epoetin products. Pharm Res 2011; 28: 386-93.
43. Jiskoot W, Randolph TW, Volkin DB, et al,. Protein instability and immunogenicity: roadblocks to clinical application of injectable protein delivery systems for sustained release. J Pharm Sci 2012; 101: 946-54.
44. Van Beers MM, Bardor M,. Minimizing immunogenicity of biopharmaceuticals by controlling critical quality attributes of proteins. Biotechnol J 2012; 7: 1473-84.
45. Rosenberg AS, Verthelyi D, Cherney BW,. Managing uncertainty: a perspective on risk pertaining to product quality attributes as they bear on immunogenicity of therapeutic proteins. J Pharm Sci 2012; 101: 3560-7.
46. Drane D, Maraskovsky E, Gibson R, et al,. Priming of CD4+ and CD8+ T cell responses using a HCV core ISCOMATRIX vaccine: a phase I study in healthy volunteers. Hum Vaccin 2009; 5: 151-7.
47. Quarmby V,. Nutropin depot and immunogenicity. 2010 Workshop on Protein Aggregation and Immunogenicity Breckenridge, Colorado. 2010.
48. Wang W, Singh SK, Li N, Toler MR, King KR, Nema S,. Immunogenicity of protein aggregates-concerns and realities. Int J Pharm 2012; 431: 1-11.
49. Van Beers MM, Sauerborn M, Gilli F, Brinks V, Schellekens H, Jiskoot W,. Oxidized and aggregated recombinant human interferon beta is immunogenic in human interferon beta transgenic mice. Pharm Res 2011; 28: 2393-402.
50. Liu L, Ammar DA, Ross LA, Mandava N, Kahook MY, Carpenter JF,. Silicone oil microdroplets and protein aggregates in repackaged bevacizumab and ranibizumab: effects of long-term storage and product mishandling. Invest Ophthalmol Vis Sci 2011; 52: 1023-34.
51. Hochuli E,. Interferon immunogenicity: technical evaluation of interferon-alpha 2a. J Interferon Cytokine Res 1997; 17 (Suppl 1): S15-21.
52. Fradkin AH, Carpenter JF, Randolph TW,. Immunogenicity of aggregates of recombinant human growth hormone in mouse models. J Pharm Sci 2009; 98: 3247-64.
53. Scagnolari C, Bellomi F, Turriziani O, et al,. Neutralizing and binding antibodies to IFN-beta: relative frequency in relapsing-remitting multiple sclerosis patients treated with different IFN-beta preparations. J Interferon Cytokine Res 2002; 22: 207-13.
54. Food & Drug Administration. Infliximab label. Bethesda, MD: 1998.
55. van Dullemen HM, van Deventer SJ, Hommes DW, et al,. Treatment of Crohn's disease with anti-tumor necrosis factor chimeric monoclonal antibody (cA2). Gastroenterology 1995; 109: 129-35.
56. Rice GP, Paszner B, Oger J, Lesaux J, Paty D, Ebers G,. The evolution of neutralizing antibodies in multiple sclerosis patients treated with interferon beta-1b. Neurology 1999; 52: 1277-9.
57. Vande CN, Gils A, Singh S, et al,. Antibody response to infliximab and its impact on pharmacokinetics can be transient. Am J Gastroenterol 2013; 108: 962-71.
58. Steenholdt C, Al Khalaf M, Brynskov J, Bendtzen K, Thomsen OO, Ainsworth MA,. Clinical implications of variations in anti-infliximab antibody levels in patients with inflammatory bowel disease. Inflamm Bowel Dis 2012; 18: 2209-17.
59. Ben Horin S, Mazor Y, Yanai H, et al,. The decline of anti-drug antibody titres after discontinuation of anti-TNFs: implications for predicting re-induction outcome in IBD. Aliment Pharmacol Ther 2012; 35: 714-22.
60. Louis E, Mary JY, Vernier-Massouille G, et al,. Maintenance of remission among patients with Crohn's disease on antimetabolite therapy after infliximab therapy is stopped. Gastroenterology 2012; 142: 63-70.
61. Zelinkova Z, van der EC, Bruin KF, et al,. Effects of discontinuing anti-tumor necrosis factor therapy during pregnancy on the course of inflammatory bowel disease and neonatal exposure. Clin Gastroenterol Hepatol 2013; 11: 318-21.
62. Bendtzen K,. Anti-TNF-alpha biotherapies: perspectives for evidence-based personalized medicine. Immunotherapy 2012; 4: 1167-79.
63. Colombel JF, Sandborn WJ, Reinisch W, et al,. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 2010; 362: 1383-95.
64. Lichtenstein GR, Diamond RH, Wagner CL, et al,. Clinical trial: benefits and risks of immunomodulators and maintenance infliximab for IBD-subgroup analyses across four randomized trials. Aliment Pharmacol Ther 2009; 30: 210-26.
65. Ben Horin S, Waterman M, Kopylov U, et al,. Addition of an immunomodulator to infliximab therapy eliminates anti-drug antibodies in serum and restores clinical response of patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2013; 11: 444-7.
66. Plasencia C, Pascual-Salcedo D, Nuno L, et al,. Influence of immunogenicity on the efficacy of longterm treatment of spondyloarthritis with infliximab. Ann Rheum Dis 2012; 71: 1955-60.
67. Feagan BG, MacDonald J, Pannacione R, et al,. Methotrexate for the prevention of antibodies to infliximab in patients with Crohn's disease. Gastroenterology 2010; 138 [ 5 (1) ]: S167-8.
68. Moss AC, Kim KJ, Fernandez-Becker N, Cury D, Cheifetz AS,. Impact of concomitant immunomodulator use on long-term outcomes in patients receiving scheduled maintenance infliximab. Dig Dis Sci 2010; 55: 1413-20.
69. Rutgeerts P, Sandborn WJ, Feagan BG, et al,. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 2005; 353: 2462-76.
70. Vermeire S, Noman M, Van Assche G, Baert F, D'Haens G, Rutgeerts P,. Effectiveness of concomitant immunosuppressive therapy in suppressing the formation of antibodies to infliximab in Crohn's disease. Gut 2007; 56: 1226-31.
71. 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.
72. Mohanan D, Slutter B, Henriksen-Lacey M, et al,. Administration routes affect the quality of immune responses: a cross-sectional evaluation of particulate antigen-delivery systems. J Control Release 2010; 147: 342-9.
73. Perini P, Facchinetti A, Bulian P, et al,. Interferon-beta (INF-beta) antibodies in interferon-beta1a- and interferon-beta1b-treated multiple sclerosis patients. Prevalence, kinetics, cross-reactivity, and factors enhancing interferon-beta immunogenicity in vivo. Eur Cytokine Netw 2001; 12: 56-61.
74. Kijanka G, Jiskoot W, Schellekens H, Brinks V,. Effect of treatment regimen on the immunogenicity of human interferon beta in immune tolerant mice. Pharm Res 2013; 30: 1553-60.
75. Velayos F, Sheibani S, Lockton S, et al,. Prevalence of antibodies to adalimumab (ATA) and correlation between ATA and low serum drug concentration on CRP and clinical symptoms in a prospective sample of IBD patients. Gastroenterology 2013; 144: S-490.
76. Guyatt GH, Oxman AD, Vist GE, et al,. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008; 336: 924-6.
77. 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.
78. Feagan BG,. Novel infliximab (IFX) & antibody to infliximab (ATI) assays are predictive of disease activity in patients with Crohn's disease. Gastroenterology 2012; 142 (Suppl 1): A565.
79. Pariente B, Pineton dC, Krzysiek R, et al,. Trough levels and antibodies to infliximab may not predict response to intensification of infliximab therapy in patients with inflammatory bowel disease. Inflamm Bowel Dis 2012; 18: 1199-206.
80. vande Casteele N, Compernolle G, Ballet V, et al,. Results on the optimisation phase of the prospective controlled trough level adapted infliximab treatment (TAXIT) trial. Gastroenterology 2012; 142 (Suppl 1): S211-2.
81. Vande CN, Ballet V, Van Assche G, Rutgeerts P, Vermeire S, Gils A,. Early serial trough and antidrug antibody level measurements predict clinical outcome of infliximab and adalimumab treatment. Gut 2012; 61: 321.
82. Brinks V, Jiskoot W, Schellekens H,. Immunogenicity of therapeutic proteins: the use of animal models. Pharm Res 2011; 28: 2379-85.