Anti-TNF-α biotherapies: Perspectives for evidence-based personalized medicine

Immunotherapy

Volumn 4, Issue 11, 2012, Pages 1167-1179

  Bendtzen, Klaus ^a  

^a University of Copenhagen   (Denmark)

Author keywords

anti TNF antibodies; immunogenicity; pharmacodynamics; pharmacokinetics; recombinant protein therapeutics; theranostics

Indexed keywords

ADALIMUMAB; CERTOLIZUMAB PEGOL; ETANERCEPT; GOLIMUMAB; INFLIXIMAB; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

B LYMPHOCYTE; DRUG BIOAVAILABILITY; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; EVIDENCE BASED MEDICINE; GENETIC ENGINEERING; HUMAN; IMMUNOGENICITY; IMMUNOPHARMACOLOGY; NONHUMAN; PERSONALIZED MEDICINE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; TREATMENT FAILURE; TREATMENT RESPONSE;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; AUTOIMMUNE DISEASES; BIOLOGICAL THERAPY; CLINICAL TRIALS AS TOPIC; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNOGLOBULIN G; INDIVIDUALIZED MEDICINE; MONITORING, PHYSIOLOGIC; PROTEIN ENGINEERING; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84870455276     PISSN: 1750743X     EISSN: 17507448     Source Type: Journal    
DOI: 10.2217/imt.12.114     Document Type: Review

References (79)

1. Langford CA. Drug insight: anti-tumor necrosis factor therapies for the vasculitic diseases. Nat. Clin. Pract. Rheumatol. 4, 364-370 (2008).
2. Emery P, Fleischmann RM, Moreland LW et al. Golimumab, a human anti-tumor necrosis factor a monoclonal antibody, injected subcutaneously every four weeks in methotrexate-naive patients with active rheumatoid arthritis: twenty-four-week results of a Phase III, multicenter, randomized, double-blind, placebo-controlled study of golimumab before methotrexate as first-line therapy for early-onset rheumatoid arthritis. Arthritis Rheum. 60, 2272-2283 (2009).
3. 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 4, 355-366 (2010).
4. Handa T, Tsunekawa H, Yoneda M et al. Long-term remission of ocular and extraocular manifestations in Behcet's disease using infliximab. Clin. Exp. Rheumatol. 29, S58-S63 (2011).
5. Furst DE, Keystone EC, Braun J et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2010. Ann. Rheum. Dis. 70(Suppl. 1), I2-I36 (2011).
6. Oxholm A, Oxholm P, Staberg B, Bendtzen K. Immunohistological detection of interleukin 1-like molecules and tumour necrosis factor in human epidermis before and after UVB-irradiation in vivo. Br. J. Dermatol. 118, 369-376 (1988).
7. Deleuran BW, Chu CQ, Field M et al. Localization of tumor necrosis factor receptors in the synovial tissue and cartilage-pannus junction in patients with rheumatoid arthritis: implications for local actions of tumor necrosis factor a. Arthritis Rheum. 35, 1170-1178 (1992).
8. Reinecker HC, Steffen M, Witthoeft T et al. Enhanced secretion of tumour necrosis factor-a, IL-6, and IL-1b by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin. Exp. Immunol. 94, 174-181 (1993).
9. Elliott MJ, Maini RN, Feldmann M et al. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to tumor necrosis factor a. Arthritis Rheum. 36, 1681-1690 (1993).
10. Baert FJ, D'Haens GR, Peeters M et al. Tumor necrosis factor a antibody (infliximab) therapy profoundly down-regulates the inflammation in Crohn's ileocolitis. Gastroenterology 116, 22-28 (1999).
11. McDermott MF, Aksentijevich I, Galon J et al. Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell 97, 133-144 (1999).
12. Lobuglio AF, Wheeler RH, Trang J et al. Mouse/human chimeric monoclonal antibody in man: kinetics and immune response. Proc. Natl Acad. Sci. USA 86, 4220-4224 (1989).
13. van Dullemen HM, van Deventer SJH, Hommes DW et al. Treatment of Crohn's disease with anti-tumor necrosis factor chimeric monoclonal antibody (cA2). Gastroenterology 109, 129-135 (1995).
14. Moreland LW, Baumgartner SW, Schiff MH et al. Treatment of rheumatoid arthritis with a recombinant human tumor necrosis factor receptor (p75)-Fc fusion protein. N. Engl. J. Med. 337, 141-147 (1997).
15. Choy EH, Hazleman B, Smith M et al. Efficacy of a novel PEGylated humanized anti-TNF fragment (CDP870) in patients with rheumatoid arthritis: a Phase II double-blinded, randomized, dose-escalating trial. Rheumatology 41, 1133-1137 (2002).
16. den Broeder A, van de Putte L, Rau R et al. A single dose, placebo controlled study of the fully human anti-tumor necrosis factor-a antibody adalimumab (D2E7) in patients with rheumatoid arthritis. J. Rheumatol. 29, 2288-2298 (2002).
17. Sandborn WJ. Optimizing anti-tumor necrosis factor strategies in inflammatory bowel disease. Curr. Gastroenterol. Rep. 5, 501-505 (2003).
18. Zhou H, Jang H, Fleischmann RM et al. Pharmacokinetics and safety of golimumab, a fully human anti-TNF-a monoclonal antibody, in subjects with rheumatoid arthritis. J. Clin. Pharmacol. 47, 383-396 (2007).
19. Assasi N, Blackhouse G, Xie F et al. Patient outcomes after anti TNF-a drugs for Crohn's disease. Expert Rev. Pharmacoecon. Outcomes Res. 10, 163-175 (2010).
20. Bendtzen K. Immunogenicity of anti-TNF antibodies. In: Immunogenicity of Biopharmaceuticals (Volume VIII). van de Weert M, Møller EH (Eds). Springer, NY, USA, 189-203 (2008).
21. Strand V, Kimberly R, Isaacs JD. Biologic therapies in rheumatology: lessons learned, future directions. Nat. Rev. Drug Discov. 6, 75-92 (2007).
22. Bendtzen K, Ainsworth M, Steenholdt C, Thomsen OO, Brynskov J. Individual medicine in inflammatory bowel disease: monitoring bioavailability, pharmacokinetics and immunogenicity of anti-tumour necrosis factor-a antibodies. Scand. J. Gastroenterol. 44, 774-781 (2009).
23. Krieckaert CL, Bartelds GM, Lems WF, Wolbink GJ. The effect of immunomodulators on the immunogenicity of TNF-blocking therapeutic monoclonal antibodies: a review. Arthritis Res. Ther. 12, 217 (2010).
24. Bendtzen K, Geborek P, Svenson M, Larsson L, Kapetanovic MC, Saxne T. Individualized monitoring of drug bioavailability and immunogenicity in rheumatoid arthritis patients treated with the tumor necrosis factor a inhibitor Infliximab. Arthritis Rheum. 54, 3782-3789 (2006).
25. Ternant D, Aubourg A, Magdelaine-Beuzelin C et al. Infliximab pharmacokinetics in inflammatory bowel disease patients. Ther. Drug Monit. 30, 523-529 (2008).
26. Ainsworth MA, Bendtzen K, Brynskov J. Tumor necrosis factor-a 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. 103, 944-948 (2008).
27. Wijbrandts CA, Dijkgraaf MG, Kraan MC et al. The clinical response to infliximab in rheumatoid arthritis is in part dependent on pretreatment tumour necrosis factor a expression in the synovium. Ann. Rheum. Dis. 67, 1139-1144 (2008).
28. Bendtzen K. Editorial: Is there a need for immunopharmacological guidance of anti-TNF therapies? Arthritis Rheum. 63, 867-870 (2011).
29. Emery P. Optimizing outcomes in patients with rheumatoid arthritis and an inadequate response to anti-TNF treatment. Rheumatology (Oxf.). 51(Suppl. 5), V22-V30 (2012).
30. Kromminga A, Schellekens H. Antibodies against erythropoietin and other protein-based therapeutics: an overview. Ann. N. Y. Acad. Sci. 1050, 257-265 (2005).
31. Shankar G, Shores E, Wagner C, Mire-Sluis A. Scientific and regulatory considerations on the immunogenicity of biologics. Trends Biotechnol. 24, 274-280 (2006).
32. Hartung HP, Polman C, Bertolotto A et al. Neutralising antibodies to interferon b in multiple sclerosis: Expert panel report. J. Neurol. 254, 827-837 (2007).
33. Ehrenforth S, Seremetis S. Case study: Immunogenicity of factor VIII. In: Immunogenicity of Biopharmaceuticals (Volume VIII). van de Weert M, Møller EH (Eds). Springer, NY, USA, 147-171 (2008).
34. Tamilvanan S, Raja NL, Sa B, Basu SK. Clinical concerns of immunogenicity produced at cellular levels by biopharmaceuticals following their parenteral administration into human body. J. Drug Target 18, 489-498 (2010).
35. Richard J, Prang N. The formulation and immunogenicity of therapeutic proteins: product quality as a key factor. IDrugs 13, 550-558 (2010).
36. Nielsen CH, Bendtzen K. Immunoregulation by naturally occurring and disease-associated autoantibodies: binding to cytokines and their role in regulation of T-cell responses. Adv. Exp. Med. Biol. 750, 116-132 (2012).
37. Fefferman DS, Farrell RJ. Immunogenicity of biological agents in inflammatory bowel disease. Inflamm. Bowel Dis. 11, 497-503 (2005).
38. Wolbink GJ, Vis M, Lems W et al. Development of antiinfliximab antibodies and relationship to clinical response in patients with rheumatoid arthritis. Arthritis Rheum. 54, 711-715 (2006).
39. Bartelds GM, Wijbrandts CA, Nurmohamed MT et al. Clinical response to adalimumab: The relationship with anti-adalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis. Ann. Rheum. Dis. 66, 921-926 (2007).
40. Ebert EC, Das KM, Mehta V, Rezac C. Non-response to infliximab may be due to innate neutralizing anti-tumour necrosis factor-a antibodies. Clin. Exp. Immunol. 154, 325-331 (2008).
41. West RL, Zelinkova Z, Wolbink GJ, Kuipers EJ, Stokkers PC, Van der Woude CJ. Immunogenicity negatively influences the outcome of adalimumab treatment in Crohn's disease. Aliment Pharmacol. Ther. 28, 1122-1126 (2008).
42. Ko JM, Gottlieb AB, Kerbleski JF. Induction and exacerbation of psoriasis with TNF-blockade therapy: a review and analysis of 127 cases. J. Dermatolog. Treat. 20, 100-108 (2009).
43. Petitpain N, Gambier N, Wahl D, Chary-Valckenaere I, Loeuille D, Gillet P. Arterial and venous thromboembolic events during anti-TNF therapy: a study of 85 spontaneous reports in the period 2000-2006. Biomed. Mater. Eng. 19, 355-364 (2009).
44. Cassinotti A, Travis S. Incidence and clinical significance of immunogenicity to infliximab in Crohn's disease: a critical systematic review. Inflamm. Bowel Dis. 15, 1264-1275 (2009).
45. Wolbink GJ, Aarden LA, Dijkmans BA. Dealing with immunogenicity of biologicals: assessment and clinical relevance. Curr. Opin. Rheumatol. 21, 211-215 (2009).
46. 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 137, 1628-1640 (2009).
47. Aikawa NE, JF de Carvalho, Silva CA, Bonfa E. Immunogenicity of anti-TNF-a agents in autoimmune diseases. Clin. Rev. Allergy Immunol. 38, 82-89 (2010).
48. 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. 70, 284-288 (2010).
49. Lecluse LL, Driessen RJ, Spuls PI et al. Extent and clinical consequences of antibody formation against adalimumab in patients with plaque psoriasis. Arch. Dermatol. 146, 127-132 (2010).
50. Makol A, Grover M, Guggenheim C, Hassouna H. Etanercept and venous thromboembolism: a case series. J. Med. Case Reports 4, 12 (2010).
51. 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 305, 1460-1468 (2011).
52. 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. 63, 877-883 (2011).
53. Steenholdt C, Svenson M, Bendtzen K, Thomsen O, Brynskov J, Ainsworth MA. Severe infusion reactions to infliximab: aetiology, immunogenicity and risk factors in patients with inflammatory bowel disease. Aliment Pharmacol. Ther. 34, 51-58 (2011).
54. Yanai H, Hanauer SB. Assessing response and loss of response to biological therapies in IBD. Am. J. Gastroenterol. 106, 685-698 (2011).
55. Steenholdt C, Svenson M, Bendtzen K, Thomsen O, Brynskov J, Ainsworth MA. Acute and delayed hypersensitivity reactions to infliximab and adalimumab in a patient with Crohn's disease. J. Crohns Colitis 6, 108-111 (2012).
56. Aarden L, Ruuls SR, Wolbink G. Immunogenicity of anti-tumor necrosis factor antibodies-toward improved methods of anti-antibody measurement. Curr. Opin. Immunol. 20, 431-435 (2008).
57. 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. 64, 704-707 (2005).
58. Descotes J, Gouraud A. Clinical immunotoxicity of therapeutic proteins. Expert Opin. Drug Metab. Toxicol. 4, 1537-1549 (2008).
59. Dubey S, Kerrigan N, Mills K, Scott DG. Bronchospasm associated with anti-TNF treatment. Clin. Rheumatol. 28, 989-992 (2009).
60. Tangri S, Mothe BR, Eisenbraun J et al. Rationally engineered therapeutic proteins with reduced immunogenicity. J. Immunol. 174, 3187-3196 (2005).
61. Hwang WY, Foote J. Immunogenicity of engineered antibodies. Methods 36, 3-10 (2005).
62. Cheifetz A, Mayer L. Monoclonal antibodies, immunogenicity, and associated infusion reactions. Mt Sinai J. Med. 72, 250-256 (2005).
63. De Groot AS, Scott DW. Immunogenicity of protein therapeutics. Trends Immunol. 28, 482-490 (2007).
64. 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. 68, 1739-1745 (2009).
65. Afif W, Loftus EVJ, Faubion WA et al. Clinical utility of measuring infliximab and human anti-chimeric antibody concentrations in patients with inflammatory bowel disease. Am. J. Gastroenterol. 105, 1133-1139 (2010).
66. Jamnitski A, Krieckaert CL, Nurmohamed MT et al. Patients non-responding to etanercept obtain lower etanercept concentrations compared with responding patients. Ann. Rheum. Dis. 71(1), 88-91 (2012).
67. Ginsburg GS, McCarthy JJ. Personalized medicine: revolutionizing drug discovery and patient care. Trends Biotechnol. 19, 491-496 (2001).
68. Maini RN, Breedveld FC, Kalden JR et al. Therapeutic efficacy of multiple intravenous infusions of anti-tumor necrosis factor a monoclonal antibody combined with low-dose weekly methotrexate in rheumatoid arthritis. Arthritis Rheum. 41, 1552-1563 (1998).
69. Candon S, Mosca A, Ruemmele F, Goulet O, Chatenoud L, Cezard JP. Clinical and biological consequences of immunization to infliximab in pediatric Crohn's disease. Clin. Immunol. 118, 11-19 (2006).
70. Steenholdt C, Al-khalaf M, Brynskov J, Bendtzen K, Thomsen O, Ainsworth MA. Clinical implications of variations in anti-infliximab antibody levels in patients with inflammatory bowel disease. Inflamm. Bowel Dis. doi:10.1002/ibd.22910 (2012) (Epub ahead of print).
71. 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 56, 1226-1231 (2007).
72. McDonald TA, Zepeda ML, Tomlinson MJ, Bee WH, Ivens IA. Subcutaneous administration of biotherapeutics: current experience in animal models. Curr. Opin. Mol. Ther. 12, 461-470 (2010).
73. Hart MH, de Vrieze H, Wouters D et al. Differential effect of drug interference in immunogenicity assays. J. Immunol. Methods 372, 196-203 (2011).
74. Bendtzen K, Svenson M. Enzyme immunoassays and radioimmunoassays for quantification of anti-TNF biopharmaceuticals and anti-drug antibodies. In: Detection and Quantification of Antibodies to Biopharmaceuticals. Practical and Applied Considerations. Tovey MG (Ed.). John Wiley & Sons, West Sussex, UK, 83-101 (2011).
75. Steenholdt C, Bendtzen K, Brynskov J, Thomsen OO, Ainsworth MA. Cut-off levels and diagnostic accuracy of infliximab trough levels and anti-infliximab antibodies in Crohn's disease. Scand. J. Gastroenterol. 46, 310-318 (2011).
76. Svenson M, Geborek P, Saxne T, Bendtzen K. Monitoring patients treated with anti-TNF-a biopharmaceuticals-assessing serum infliximab and anti-infliximab antibodies. Rheumatology 46, 1828-1834 (2007).
77. van Schouwenburg PA, Bartelds GM, Hart MH, Aarden L, Wolbink GJ, Wouters D. 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 362, 82-88 (2010).
78. 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. Meth. 373, 229-239 (2011).
79. Cada DJ, Levien TL, Baker DE. Golimumab. Hosp. Pharm. 44, 894-907 (2009).