Assessing the Immunogenicity of Biopharmaceuticals

BioDrugs

Volumn 30, Issue 3, 2016, Pages 195-206

  Pineda, Carlos ^a   Castañeda Hernández, Gilberto ^b,c   Jacobs, Ira A ^d   Alvarez, Daniel F ^d   Carini, Claudio ^d  

^a INSTITUTO NACIONAL DE REHABILITACIÓN   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c Centro Latinoamericano de Pesquisa em Biologicos   (Brazil)

^d PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; BIOSIMILAR AGENT; DRUG ANTIBODY; METHOTREXATE; NEUTRALIZING ANTIBODY; ANTIBODY; BIOLOGICAL PRODUCT;

ANTIBODY SCREENING; DRUG SAFETY; EXPERIMENTAL DESIGN; HUMAN; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOGENICITY; POSTMARKETING SURVEILLANCE; PRACTICE GUIDELINE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; RISK MANAGEMENT; STANDARD; FOOD AND DRUG ADMINISTRATION; IMMUNOLOGY; PHARMACEUTICS; PROCEDURES; STANDARDS; UNITED STATES;

ADALIMUMAB; ANTIBODIES; BIOLOGICAL PRODUCTS; BIOPHARMACEUTICS; BIOSIMILAR PHARMACEUTICALS; HUMANS; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

EID: 84964319034     PISSN: 11738804     EISSN: 1179190X     Source Type: Journal    
DOI: 10.1007/s40259-016-0174-5     Document Type: Review

References (72)

1. Morrow T, Felcone LH. Defining the difference: what makes bologics unique. Biotechnol Healthc. 2004;1(4):24–9.
2. Walsh G. Biopharmaceutical benchmarks 2010. Nat Biotechnol. 2010;28(9):917–24.
3. Wang J, Chow SC. On the regulatory approval pathway of biosimilar products. Pharmaceuticals (Basel). 2012;5(4):353–68. doi:10.3390/ph5040353.
4. Bennett CL, Chen B, Hermanson T, Wyatt MD, Schulz RM, Georgantopoulos P, et al. Regulatory and clinical considerations for biosimilar oncology drugs. Lancet Oncol. 2014;15(13):e594–605. doi:10.1016/S1470-2045(14)70365-1.
5. US Food and Drug Administration. Scientific considerations in demonstrating biosimilarity to a reference product: guidance for industry. SIlver Spring: U.S. Department of Health and Human Services, Center for Drug Evaluation and Research (CDER), Center for Biologics Evaluation and Research (CBER); 2015 (last update Apr 2015). http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM291128.pdf. Accessed 23 Mar 2015.
6. European Medicines Agency, Committee for Medicinal Products for Human Use (CHMP). Guideline on similar biological medicinal products containing biotechnology-derived proteins as active substance: non-clinical and clinical issues. London: EMA; 2013 (last update 3 June 2013). http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2013/06/WC500144124.pdf. Accessed 23 Mar 2015.
7. World Health Organization, Expert Committee on Biological Standardization. Geneva, 19 to 23 October 2009. Guidelines on evaluation of similar biotherapeutic products (SBPs). Geneva: WHO; 2009 (last update 19–23 Oct 2009). http://www.who.int/biologicals/areas/biological_therapeutics/BIOTHERAPEUTICS_FOR_WEB_22APRIL2010.pdf. Accessed 21 Apr 2015.
8. Espinosa Morales R, Diaz Borjon A, Barile Fabris LA, Esquivel Valerio JA, Medrano Ramirez G, Arce Salinas CA, et al. Biosimilar drugs in Mexico: position of the Mexican College of Rheumatology, 2012. Reumatol Clin. 2013;9(2):113–6. doi:10.1016/j.reuma.2012.11.001.
9. American College of Rheumatology. American College of Rheumatology position statement: biosimilars. Atlanta: ACR; 2015. http://www.rheumatology.org/Portals/0/Files/Biosimilars.pdf. Accessed 27 May 2015.
10. Barosi G, Bosi A, Abbracchio MP, Danesi R, Genazzani A, Corradini P, et al. Key concepts and critical issues on epoetin and filgrastim biosimilars. A position paper from the Italian Society of Hematology, Italian Society of Experimental Hematology, and Italian Group for Bone Marrow Transplantation. Haematologica. 2011;96(7):937–42. doi:10.3324/haematol.2011.041210.
11. Fiorino G, Girolomoni G, Lapadula G, Orlando A, Danese S, Olivieri I. The use of biosimilars in immune-mediated disease: a joint Italian Society of Rheumatology (SIR), Italian Society of Dermatology (SIDeMaST), and Italian Group of Inflammatory Bowel Disease (IG-IBD) position paper. Autoimmun Rev. 2014;13(7):751–5. doi:10.1016/j.autrev.2014.02.004.
12. Arguelles-Arias F, Barreiro-de-Acosta M, Carballo F, Hinojosa J, Tejerina T. Joint position statement by “Sociedad Espanola de Patologia Digestiva” (Spanish Society of Gastroenterology) and “Sociedad Espanola de Farmacologia” (Spanish Society of Pharmacology) on biosimilar therapy for inflammatory bowel disease. Rev Esp Enferm Dig. 2013;105(1):37–43.
13. Fonseca JE, Goncalves J, Araujo F, Cordeiro I, Teixeira F, Canhao H, et al. The Portuguese Society of Rheumatology position paper on the use of biosimilars. Acta Reumatol Port. 2014;39(1):60–71.
14. Mularczyk A, Gonciarz M, Bartnik W, Durlik M, Eder P, Gasiorowska A, et al. Biosimilar medicines—their use in the treatment of inflammatory bowel diseases. Position statement of the Working Group of the Polish National Consultant in Gastroenterology. Prz Gastroenterol. 2014;9(1):1–3. doi:10.5114/pg.2014.40842.
15. Bendtzen K. Anti-TNF-alpha biotherapies: perspectives for evidence-based personalized medicine. Immunotherapy. 2012;4(11):1167–79. doi:10.2217/imt.12.114.
16. European Medicines Agency, European Agency for the Evaluation of Medicinal Products, Committee for Proprietary Medicinal Products (CPMP). Development pharmaceutics for biotechnological and biological products (CPMP/BWP/328/99). Annex to note for guidance on development of pharmaceutics (CPMP/QWP/155/96). London: EMA; 1999 (last update Apr 2000). http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500003603.pdf. Accessed 28 May 2015.
17. Pendley C, Schantz A, Wagner C. Immunogenicity of therapeutic monoclonal antibodies. Curr Opin Mol Ther. 2003;5(2):172–9.
18. Schellekens H. Bioequivalence and the immunogenicity of biopharmaceuticals. Nat Rev Drug Discov. 2002;1(6):457–62. doi:10.1038/nrd818.
19. Schellekens H. Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin Ther. 2002;24(11):1720–40 (discussion 19).
20. Shankar G, Pendley C, Stein KE. A risk-based bioanalytical strategy for the assessment of antibody immune responses against biological drugs. Nat Biotechnol. 2007;25(5):555–61. doi:10.1038/nbt1303.
21. Vincent FB, Morand EF, Murphy K, Mackay F, Mariette X, Marcelli C. 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. doi:10.1136/annrheumdis-2012-202545.
22. Casadevall N, Nataf J, Viron B, Kolta A, Kiladjian JJ, Martin-Dupont P, et al. Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin. N Engl J Med. 2002;346(7):469–75. doi:10.1056/NEJMoa011931.
23. Li J, Yang C, Xia Y, Bertino A, Glaspy J, Roberts M, et al. Thrombocytopenia caused by the development of antibodies to thrombopoietin. Blood. 2001;98(12):3241–8.
24. Buttel IC, Chamberlain P, Chowers Y, Ehmann F, Greinacher A, Jefferis R, et al. Taking immunogenicity assessment of therapeutic proteins to the next level. Biologicals. 2011;39(2):100–9. doi:10.1016/j.biologicals.2011.01.006.
25. Jahn EM, Schneider CK. How to systematically evaluate immunogenicity of therapeutic proteins—regulatory considerations. N Biotechnol. 2009;25(5):280–6. doi:10.1016/j.nbt.2009.03.012.
26. Barbosa MD, Kumar S, Loughrey H, Singh SK. Biosimilars and biobetters as tools for understanding and mitigating the immunogenicity of biotherapeutics. Drug Discov Today. 2012;17(23–24):1282–8. doi:10.1016/j.drudis.2012.07.003.
27. Barbosa MD, Celis E. Immunogenicity of protein therapeutics and the interplay between tolerance and antibody responses. Drug Discov Today. 2007;12(15–16):674–81. doi:10.1016/j.drudis.2007.06.005.
28. Liu PM, Zou L, Sadhu C, Shen WD, Nock S. Comparative immunogenicity assessment: a critical consideration for biosimilar development. Bioanalysis. 2015;7(3):373–81. doi:10.4155/bio.14.311.
29. Nechansky A, Kircheis R. Immunogenicity of therapeutics: a matter of efficacy and safety. Expert Opin Drug Discov. 2010;5(11):1067–79. doi:10.1517/17460441.2010.514326.
30. Wadhwa M, Bird C, Dilger P, Gaines-Das R, Thorpe R. Strategies for detection, measurement and characterization of unwanted antibodies induced by therapeutic biologicals. J Immunol Methods. 2003;278(1–2):1–17.
31. Mire-Sluis AR, Barrett YC, Devanarayan V, Koren E, Liu H, Maia M, et al. Recommendations for the design and optimization of immunoassays used in the detection of host antibodies against biotechnology products. J Immunol Methods. 2004;289(1–2):1–16. doi:10.1016/j.jim.2004.06.002.
32. Yin L, Chen X, Vicini P, Rup B, Hickling TP. Therapeutic outcomes, assessments, risk factors and mitigation efforts of immunogenicity of therapeutic protein products. Cell Immunol. 2015;295(2):118–26. doi:10.1016/j.cellimm.2015.03.002.
33. Wadhwa M, Knezevic I, Kang HN, Thorpe R. Immunogenicity assessment of biotherapeutic products: an overview of assays and their utility. Biologicals. 2015;43(5):298–306. doi:10.1016/j.biologicals.2015.06.004.
34. 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(4):431–5. doi:10.1016/j.coi.2008.06.011.
35. Vollmer N, Trombini F, Hely M, Bellon S, Mercier K, Cazeneuve C. Methodology to study polymers interaction by surface plasmon resonance imaging. MethodsX. 2015;2:14–8. doi:10.1016/j.mex.2014.12.001.
36. Wolbink GJ, Aarden LA, Dijkmans BA. Dealing with immunogenicity of biologicals: assessment and clinical relevance. Curr Opin Rheumatol. 2009;21(3):211–5.
37. 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. 2010;362(1–2):82–8. doi:10.1016/j.jim.2010.09.005.
38. Patton A, Mullenix MC, Swanson SJ, Koren E. An acid dissociation bridging ELISA for detection of antibodies directed against therapeutic proteins in the presence of antigen. J Immunol Methods. 2005;304(1–2):189–95. doi:10.1016/j.jim.2005.06.014.
39. Sickert D, Kroeger K, Zickler C, Chokote E, Winkler B, Grenet JM, et al. Improvement of drug tolerance in immunogenicity testing by acid treatment on Biacore. J Immunol Methods. 2008;334(1–2):29–36. doi:10.1016/j.jim.2008.01.010.
40. Bourdage JS, Cook CA, Farrington DL, Chain JS, Konrad RJ. An affinity capture elution (ACE) assay for detection of anti-drug antibody to monoclonal antibody therapeutics in the presence of high levels of drug. J Immunol Methods. 2007;327(1–2):10–7. doi:10.1016/j.jim.2007.07.004.
41. Schmidt E, Hennig K, Mengede C, Zillikens D, Kromminga A. Immunogenicity of rituximab in patients with severe pemphigus. Clin Immunol. 2009;132(3):334–41. doi:10.1016/j.clim.2009.05.007.
42. Wang SL, Ohrmund L, Hauenstein S, Salbato J, Reddy R, Monk P, 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(1–2):177–88. doi:10.1016/j.jim.2012.06.002.
43. Bloem K, van Leeuwen A, Verbeek G, Nurmohamed MT, Wolbink GJ, van der Kleij D, et al. Systematic comparison of drug-tolerant assays for anti-drug antibodies in a cohort of adalimumab-treated rheumatoid arthritis patients. J Immunol Methods. 2015;418:29–38. doi:10.1016/j.jim.2015.01.007.
44. van Schouwenburg PA, Krieckaert CL, Rispens T, Aarden L, Wolbink GJ, Wouters D. Long-term measurement of anti-adalimumab using pH-shift-anti-idiotype antigen binding test shows predictive value and transient antibody formation. Ann Rheum Dis. 2013;72(10):1680–6. doi:10.1136/annrheumdis-2012-202407.
45. Shankar G, Devanarayan V, Amaravadi L, Barrett YC, Bowsher R, Finco-Kent D, et al. Recommendations for the validation of immunoassays used for detection of host antibodies against biotechnology products. J Pharm Biomed Anal. 2008;48(5):1267–81. doi:10.1016/j.jpba.2008.09.020.
46. Koren E, Smith HW, Shores E, Shankar G, Finco-Kent D, Rup B, et al. Recommendations on risk-based strategies for detection and characterization of antibodies against biotechnology products. J Immunol Methods. 2008;333(1–2):1–9. doi:10.1016/j.jim.2008.01.001.
47. Gupta S, Indelicato SR, Jethwa V, Kawabata T, Kelley M, Mire-Sluis AR, et al. Recommendations for the design, optimization, and qualification of cell-based assays used for the detection of neutralizing antibody responses elicited to biological therapeutics. J Immunol Methods. 2007;321(1–2):1–18. doi:10.1016/j.jim.2006.12.004.
48. AbbVie Inc. HUMIRA (adalimumab) prescribing information. North Chicago: AbbVie Inc.; 2014. http://www.rxabbvie.com/pdf/humira.pdf. Accessed 2 June 2015.
49. Weinblatt ME, Keystone EC, Furst DE, Moreland LW, Weisman MH, Birbara CA, 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(1):35–45.
50. Keystone EC, Kavanaugh AF, Sharp JT, Tannenbaum H, Hua Y, Teoh LS, et al. Radiographic, clinical, and functional outcomes of treatment with adalimumab (a human anti-tumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy: a randomized, placebo-controlled, 52-week trial. Arthritis Rheum. 2004;50(5):1400–11.
51. Hart MH, de Vrieze H, Wouters D, Wolbink GJ, Killestein J, de Groot ER, et al. Differential effect of drug interference in immunogenicity assays. J Immunol Methods. 2011;372(1–2):196–203. doi:10.1016/j.jim.2011.07.019.
52. Bartelds GM, de Groot E, Nurmohamed MT, Hart MHL, van Eede PH, Wijbrandts CA, et al. Surprising negative association between IgG1 allotype disparity and anti-adalimumab formation: a cohort study. Arthritis Res Ther. 2010;12(6). doi:10.1186/ar3208.
53. Bartelds GM, Krieckaert CL, Nurmohamed MT, van Schouwenburg PA, Lems WF, Twisk JW, et al. Development of antidrug antibodies against adalimumab and association with disease activity and treatment failure during long-term follow-up. JAMA. 2011;305(14):1460–8. doi:10.1001/jama.2011.406.
54. Bartelds GM, Wijbrandts CA, Nurmohamed MT, Stapel S, Lems WF, Aarden L, et al. Clinical response to adalimumab: relationship to anti-adalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis. Ann Rheum Dis. 2007;66(7):921–6. doi:10.1136/ard.2006.065615.
55. US Food and Drug Administration. Immunogenicity assessment for therapeutic protein products: guidance for industry. Silver Spring: U.S. Department of Health and Human Services, Center for Drug Evaluation and Research (CDER), Center for Biologics Evaluation and Research (CBER); 2014 (last update August 2014). http://www.fda.gov/downloads/drugs/guidancecomplianceregulatoryinformation/guidances/ucm338856.pdf. Accessed 28 May 2015.
56. World Health Organization. Guidelines on the quality, safety, and efficacy of biotherapeutic protein products prepared by recombinant DNA technology. Geneva: WHO; 2013. http://www.who.int/biologicals/biotherapeutics/rDNA_DB_final_19_Nov_2013.pdf. Accessed 28 May 2015.
57. European Medicines Agency, Committee for Medicinal Products for Human Use (CHMP). Guideline on immunogenicity assessment of biotechnology-derived therapeutic proteins. London: EMA; 2008. http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500003946.pdf. Accessed 28 May 2015.
58. European Medicines Agency, Committee for Medicinal Products for Human Use (CHMP). Guideline on immunogenicity assessment of monoclonal antibodies intended for in vivo clinical use. London: European Medicines Agency; 2012 (last update 1 Dec 2012). http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2012/06/WC500128688.pdf. Accessed 25 Nov 2015.
59. Ebbers HC, Crow SA, Vulto AG, Schellekens H. Interchangeability, immunogenicity and biosimilars. Nat Biotechnol. 2012;30(12):1186–90. doi:10.1038/nbt.2438.
60. Pascual-Salcedo D, Plasencia C, Ramiro S, Nuno L, Bonilla G, Nagore D, et al. Influence of immunogenicity on the efficacy of long-term treatment with infliximab in rheumatoid arthritis. Rheumatology (Oxford). 2011;50(8):1445–52. doi:10.1093/rheumatology/ker124.
61. Rosenberg AS. Immunogenicity of biological therapeutics: a hierarchy of concerns. Dev Biol (Basel). 2003;112:15–21.
62. Woodcock J, Griffin J, Behrman R, Cherney B, Crescenzi T, Fraser B, et al. The FDA’s assessment of follow-on protein products: a historical perspective. Nat Rev Drug Discov. 2007;6(6):437–42. doi:10.1038/nrd2307.
63. Chamberlain P. Assessing immunogenicity of biosimilar therapeutic monoclonal antibodies: regulatory and bioanalytical considerations. Bioanalysis. 2013;5(5):561–74. doi:10.4155/bio.13.6.
64. van Herwaarden N, Bouman CA, van der Maas A, van Vollenhoven RF, Bijlsma JW, van den Hoogen FH, et al. Adalimumab and etanercept serum (anti)drug levels are not predictive for successful dose reduction or discontinuation in rheumatoid arthritis. Ann Rheum Dis. 2015;74(12):2260–1. doi:10.1136/annrheumdis-2015-207814.
65. Cai XY, Thomas J, Cullen C, Gouty D. Challenges of developing and validating immunogenicity assays to support comparability studies for biosimilar drug development. Bioanalysis. 2012;4(17):2169–77. doi:10.4155/bio.12.185.
66. Chamberlain P. Multidisciplinary approach to evaluating immunogenicity of biosimilars: lessons learnt and open questions based on 10 years’ experience of the European Union regulatory pathway. Biosimilars. 2014;4:23–43.
67. Scheinberg M, Castaneda-Hernandez G. Anti-tumor necrosis factor patent expiration and the risks of biocopies in clinical practice. Arthritis Res Ther. 2014;16(6):501. doi:10.1186/s13075-014-0501-5.
68. Arredondo-Garza T, Majluf-Cruz A, Vela-Ojeda J, Mariscal-Ramirez I, Solis-Anaya L, Lopez-Gutierrez JR, et al. Peri-infusional adverse reactions to rituximab in patients with non-Hodgkin’s lymphoma. Arch Med Res. 2013;44(7):549–54. doi:10.1016/j.arcmed.2013.09.011.
69. Shankar G, Arkin S, Cocea L, Devanarayan V, Kirshner S, Kromminga A, et al. Assessment and reporting of the clinical immunogenicity of therapeutic proteins and peptides-harmonized terminology and tactical recommendations. AAPS J. 2014;16(4):658–73. doi:10.1208/s12248-014-9599-2.
70. Rup B, Pallardy M, Sikkema D, Albert T, Allez M, Broet P, et al. ABIRISK Consortium. Standardizing terms, definitions and concepts for describing and interpreting unwanted immunogenicity of biopharmaceuticals: recommendations of the Innovative Medicines Initiative ABIRISK consortium. Clin Exp Immunol. 2015;181(3):385–400. doi:10.1111/cei.12652.
71. van de Putte LB, Atkins C, Malaise M, Sany J, Russell AS, van Riel PL, et al. Efficacy and safety of adalimumab as monotherapy in patients with rheumatoid arthritis for whom previous disease modifying antirheumatic drug treatment has failed. Ann Rheum Dis. 2004;63(5):508–16. doi:10.1136/ard.2003.013052.
72. Miyasaka N. Clinical investigation in highly disease-affected rheumatoid arthritis patients in Japan with adalimumab applying standard and general evaluation: the CHANGE study. Mod Rheumatol. 2008;18(3):252–62. doi:10.1007/s10165-008-0045-0.