The minipig as an alternative non-rodent model for immunogenicity testing using the TNFα blockers adalimumab and infliximab

Journal of Immunotoxicology

Volumn 11, Issue 1, 2014, Pages 62-71

  Van Mierlo, Geertje J D ^a   Cnubben, Nicole H P ^a   Wouters, Diana ^b   Wolbink, Gerrit Jan ^b,c   Hart, Margreet H L ^b   Rispens, Theo ^b   Ganderup, Niels Christian ^c   Kuper, C Frieke ^a   Aarden, Lucien ^b   Penninks, André H ^a  

^a TNO   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

^c Ellegaard Göttingen Minipigs ^*  (Denmark)

Author keywords

Adalimumab; Alternative model; Anti drug antibodies; Immunogenicity; Infliximab; Minipig; Pharmacokinetics

Indexed keywords

ADALIMUMAB; DRUG ANTIBODY; INFLIXIMAB; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; AREA UNDER THE CURVE; ARTICLE; BODY WEIGHT; CLINICAL CHEMISTRY; CLINICAL FEATURE; CLINICAL OBSERVATION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG HALF LIFE; DRUG MEGADOSE; FEMALE; HEMATOLOGICAL PARAMETERS; HISTOPATHOLOGY; IMMUNE FUNCTION TEST; IMMUNE SYSTEM; IMMUNOGENICITY; LOW DRUG DOSE; MAXIMUM PLASMA CONCENTRATION; MEAN RESIDENCE TIME; MINIPIG; NONHUMAN; ORGAN WEIGHT; PREDICTIVE VALUE; PRIORITY JOURNAL; TIME TO MAXIMUM PLASMA CONCENTRATION; ANIMAL; ANTIBODY PRODUCTION; DRUG EFFECTS; DRUG SCREENING; FEASIBILITY STUDY; HUMAN; METABOLIC CLEARANCE RATE; METABOLISM; PIG; SUBCUTANEOUS DRUG ADMINISTRATION;

ADALIMUMAB; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY FORMATION; DRUG EVALUATION, PRECLINICAL; FEASIBILITY STUDIES; FEMALE; HUMANS; INFLIXIMAB; INJECTIONS, SUBCUTANEOUS; METABOLIC CLEARANCE RATE; SWINE; SWINE, MINIATURE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84896506812     PISSN: 1547691X     EISSN: None     Source Type: Journal    
DOI: 10.3109/1547691X.2013.796023     Document Type: Article

References (42)

1. Aarden, L., Ruuls, S. R., and Wolbink, G. 2008. Immunogenicity of anti-tumor necrosis factor antibodies-toward improved methods of antiantibody measurement. Curr. Opin. Immunol. 20:431-435.
2. Abbott Laboratories, Limited. 2011. Product Monograph PrHumira. adalimumab, 40 mg in 0.8 ml sterile solution (50 mg/ml), subcutaneous injection. Abbott Laboratories, Quebec, Canada.
3. Baert, F., Noman, M., Vermeire, S., et al. 2003. Influence of immunogenicity on the long-term efficacy of infliximab in Crohn's disease. New Engl. J. Med. 348:601-608.
4. Baker M. P., Reynolds, H. M., Lumicisi, B., and Bryson, C. J. 2010. Immunogenicity of protein therapeutics: Key causes, consequences and challenges. Self Nonself 1, 314-322.
5. Bartelds, G. M., De Groot, E., Nurmohamed, M. T., et al. 2010. Surprising negative association between IgG1 allotype disparity and anti-adalimumab formation: a cohort study. Arthritis Res Ther. 12:R221.
6. Bartelds, G. M., Krieckaert, C. L., Nurmohamed, M. T., et al. 2011. Development of anti-drug antibodies against adalimumab and association with disease activity and treatment failure during long-term follow-up. JAMA 305:1460-1468.
7. Bartelds, G. M., Wijbrandts, C. A., Nurmohamed, M. T., et al. 2007. Clinical response to adalimumab: Relationship to anti-adalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis. Ann. Rheum. Dis. 66:921-926.
8. Bhogal, N. 2010. Immunotoxicity and immunogenicity of biopharmaceuticals: Design concepts and safety assessment. Curr. Drug Saf. 5: 293-307.
9. Bode, G., Clausing, P., Gervais, F., et al. 2010. The utility of the minipig as an animal model in regulatory toxicology. J. Pharmacol. Toxicol. Meth. 62:196-220.
10. Brinks, V., Jiskoot, W., and Schellekens, H. 2011. Immunogenicity of therapeutic proteins: The use of animal models. Pharm. Res. 28: 2379-2385.
11. Bugelski, P. J., and Treacy, G. 2004. Predictive power of pre-clinical studies in animals for the immunogenicity of recombinant therapeutic proteins in humans. Curr. Opin. Mol. Ther. 6:10-16.
12. Büttel, I. C., Chamberlain, P., Chowers, Y., et al. 2011. Taking immunogenicity assessment of therapeutic proteins to the next level. Biologicals 39:100-109.
13. Chapman, K., Pullen, N., Coney, L., et al. 2009. Pre-clinical development of monoclonal antibodies: Considerations for the use of non-human primates. MAbs 1:505-516.
14. Chapman, K., Pullen, N., Graham, M., and Ragan, I. 2007. Preclinical safety testing of monoclonal antibodies: Significance of species relevance. Nat. Rev. Drug Discov. 6:120-126.
15. Chapman, K. L., Pullen, N., Andrews, L., and Ragan, I. 2010. The future of non-human primate use in mAb development. Drug Discov. Today 15:235-242.
16. Descotes, J. 2009. Immunotoxicity of monoclonal antibodies. MAbs 1: 104-111.
17. Descotes, J., and Gouraud, A. 2008. Clinical immunotoxicity of therapeutic proteins. Expert. Opin. Drug Metab. Toxicol. 4:1537-1549.
18. European Medicines Agency. 2002. EMEA Public statement on Infliximab (Remicade), Update on safety concerns. EMEA, London, United Kingdom. Available from: http://www.ema.europa.eu/docs/en-GB/document-library/Public-statement/ 2010/08/WC500095471.pdf
19. European Medicines Agency. 2004. Scientific discussion. EMEA, London, United Kingdom. Available from: http://www.ema.europa.eu/docs/en-GB/document- library/EPAR-Scientific-Discussion/human/000481/WC500050867.pdf. 2004.
20. European Medicines Agency. 2006. Scientific Discussion. EMEA, London, United Kingdom. Available from: http://www.ema.europa.eu/docs/en-GB/document- library/EPAR-Scientific-Discussion-Variation/human/000481/WC500050874.pdf
21. European Medicines Agency. 2005. ICH Guidance for industry. S8 Immunotoxicity Studies for Human Pharmaceuticals EMEA, London, United Kingdom.
22. Food and Drug Administration. 1998. Infliximab Product Approval Information. USFDA, Silver Spring, United States of America. Available from: http://fda.gov
23. Food and Drug Administration. 2002. Adalimumab Product Approval Information 1999-2002). USFDA, Silver Spring, United States of America. Available from: http://fda.gov.
24. Forster, R., Ancian, P., Fredholm, M., et al. 2010a. The minipig as a platform for new technologies in toxicology. J. Pharmacol. Toxicol. Meth. 62:227-235.
25. Forster, R., Bode, G., Ellegaard, L., and van der Laan, J. W. 2010b. The RETHINK project-minipigs as models for the toxicity testing of new medicines and chemicals: An impact assessment. J. Pharmacol. Toxicol. Meth. 62:158-159.
26. Hart, M. H., de Vrieze, H., Wouters, D., et al. 2011. Differential effect of drug interference in immunogenicity assays. J. Immunol. Meth. 372: 196-203.
27. Janssen Biotech, Inc. 2013. Full prescribing information. Janssen Biotech, Inc., Horsham, United States of America. Available from: http://www.remicade.com/hcp/prescribing-information
28. Kromminga, A., and Schellekens, H. 2005. Antibodies against erythropoietin and other protein-based therapeutics: An overview. Ann. N.Y. Acad. Sci. 1050:257-265.
29. Lobo, E. D., Hansen, R. J., and Balthasar, J. P. 2004. Antibody pharmacokinetics and pharmacodynamics. J. Pharm. Sci. 93: 2645-2668.
30. Loyet, K. M., Deng, R. Liang, W. C., et al. 2009. Technologycomparisons for anti-therapeutic antibody and neutralizing antibody assays in the context of an anti-TNF pharmacokinetic study. J. Immunol. Meth. 345:17-28.
31. Paserchia, L. A. (FDA). Clinical Pharmacology Review of BLA 99-0128, Remicade (Supplement). USFDA, Silver Spring, United States of America. 1999. Available from: http://www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/ HowDrugsareDevelopedandApproved/ApprovalApplications/ TherapeuticBiologicApplications/ucm107725. pdf
32. Paserchia, L. A. (FDA). 1999. Available from: http://www.fda.gov/ downloads/Drugs/DevelopmentApprovalProcess/HowDrugsareDeveloped andApproved/ApprovalApplications/TherapeuticBiologicApplications/ucm107725.pdf
33. Penninks, A. H., and van Mierlo, G. J. D. 2012. Immunotoxicity studies in minipigs. In: The Minipig in Biomedical Research (McAnulty, P. A., Dayan, A. D., Ganderup, N. C., and Hastings, K. L., Eds.). New York: CRC Press/Taylor and Francis, pp. 397-411.
34. Ponce, R., Abad, L., Amaravadi, L., et al. 2009. Immunogenicity of biologically-derived therapeutics: Assessment and interpretation of nonclinical safety studies. Regul. Toxicol. Pharmacol. 54:164-182.
35. Ryffel, B. 1997. Safety of human recombinant proteins. Biomed. Environ. Sci. 10:65-72.
36. Sauerborn, M., Brinks, V., Jiskoot, W., and Schellekens, H. 2010. Immunological mechanism underlying the immune response to recombinant human protein therapeutics. Trends Pharmacol. Sci. 31:53-59.
37. van de Putte, L. B., Atkins, C., Malaise, M., et al. 2004. 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. 63:508-516.
38. van der Laan, J. W., Brightwell, J., McAnulty, P., et al. 2010. Regulatory acceptability of the minipig in the development of pharmaceuticals, chemicals, and other products. J. Pharmacol. Toxicol. Meth. 62: 184-195.
39. van Mierlo, G. J. D., Cnubben, N. H. P., Kuper, C. F., et al. 2013. The Göttingen minipig as an alternative non-rodent species for immunogenicity testing: A demonstrator study using the IL-1 receptor antagonist anakinra. J. Immunotoxicol. 10:96-105.
40. van Schouwenburg, P. A., Bartelds, G. M., Hart, M. H., et al. 2010. A novel method for the detection of antibodies to adalimumab in presence of drug reveals "hidden" immunogenicity in rheumatoid arthritis patients. J. Immunol. Meth. 362:82-88.
41. Wierda, D., Smith, H. W., and Zwickl, C. M. 2001. Immunogenicity of biopharmaceuticals in laboratory animals. Toxicology 158:71-74.
42. Wolbink, G. J., Vis, M., Lems, W., et al. 2006. Development of antiinfliximab antibodies and relationship to clinical response in patients with rheumatoid arthritis. Arthritis Rheum. 54:711-715.