Drug-induced liver injury and drug development: Industry perspective

Seminars in Liver Disease

Volumn 34, Issue 2, 2014, Pages 227-239

  Regev, Arie ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

causality assessment; DILI prediction; drug development; Drug induced liver injury; Hy's law

Indexed keywords

PLACEBO; TROGLITAZONE; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; BILIRUBIN; DRUG; PHARMACOLOGICAL BIOMARKER;

ARTICLE; CELL CULTURE; DISEASE SURVEILLANCE; DRUG DEVELOPMENT; GENETIC POLYMORPHISM; HUMAN; METABOLITE; NONHUMAN; PATIENT MONITORING; PRIORITY JOURNAL; RISK MANAGEMENT; TOXIC HEPATITIS; ANIMAL; BLOOD; CLINICAL TRIAL (TOPIC); DRUG INDUSTRY; DRUG SCREENING; DRUG-INDUCED LIVER INJURY; INFORMATION PROCESSING; METABOLISM; POSTMARKETING SURVEILLANCE; RISK ASSESSMENT; STATISTICAL ANALYSIS; TREATMENT WITHDRAWAL;

ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ANIMALS; BILIRUBIN; BIOMARKERS, PHARMACOLOGICAL; CLINICAL TRIALS AS TOPIC; DATA DISPLAY; DATA INTERPRETATION, STATISTICAL; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; DRUG INDUSTRY; DRUG-INDUCED LIVER INJURY; HUMANS; PHARMACEUTICAL PREPARATIONS; PRODUCT SURVEILLANCE, POSTMARKETING; RISK ASSESSMENT; WITHHOLDING TREATMENT;

EID: 84901781625     PISSN: 02728087     EISSN: 10988971     Source Type: Journal    
DOI: 10.1055/s-0034-1375962     Document Type: Article

References (79)

1. Stevens J. L., Baker T. K. The future of drug safety testing: expanding the view and narrowing the focus. Drug Discov Today: 2009; 14 3-4 162 167
2. Watkins P. B., Seligman P. J., Pears J. S., Avigan M. I., Senior J. R. Using controlled clinical trials to learn more about acute drug-induced liver injury. Hepatology: 2008; 48 5 1680 1689
3. FDA Guidance for industry. Drug-induced livery injury: premarketing clinical evaluation. Available at: http://www.fda.gov/downloads/Drugs/ GuidanceComplianceRegulatoryInformation/Guidances/UCM174090.pdf. Accessed December 17, 2013
4. Navarro V. J., Senior J. R. Drug-related hepatotoxicity. N Engl J Med: 2006; 354 7 731 739 (Pubitemid 43247143)
5. Goodman Z. D. Drug hepatotoxicity. Clin Liver Dis: 2002; 6 2 381 397 (Pubitemid 34755898)
6. Lewis J. H., Ahmed M., Shobassy A., Palese C. Drug-induced liver disease. Curr Opin Gastroenterol: 2006; 22 3 223 233 (Pubitemid 44090058)
7. Bhamidimarri K. R., Schiff E. Drug-induced cholestasis. Clin Liver Dis: 2013; 17 4 519 531, vii
8. Patel V., Sanyal A. J. Drug-induced steatohepatitis. Clin Liver Dis: 2013; 17 4 533 546, vii
9. Lewis J. H. Drug-induced liver injury throughout the drug development life cycle: where we have been, where we are now, and where we are headed. Perspectives of a clinical hepatologist. Pharm Med: 2013; 27 165 191
10. Zimmerman H. J. Drug-induced liver disease. In: Hepatotoxicity, The Adverse Effects of Drugs and Other Chemicals on the Liver. 2nd ed. Philadelphia, PA Lippincott Williams & Wilkins: 1999; 428 433
11. Zetzel L., Kaplan H. Liver damage concurrent with iproniazid administration. N Engl J Med: 1958; 258 24 1209 1211
12. Zimmerman H. J., Rosenblum L., Korn R. J., Feldman P. E. Some preliminary clinical and biochemical aspects of liver function in patients receiving iproniazid. Ann N Y Acad Sci: 1959; 80 915 927
13. Manier J. W., Chang W. W., Kirchner J. P., Beltaos E. Hepatotoxicity associated with ticrynafen-a uricosuric diuretic. Am J Gastroenterol: 1982; 77 6 401 404 (Pubitemid 12070613)
14. Zimmerman H. J., Lewis J. H., Ishak K. G., Maddrey W. C. Ticrynafen-associated hepatic injury: analysis of 340 cases. Hepatology: 1984; 4 2 315 323 (Pubitemid 14131442)
15. NIDDK LiverTox, Clinical and research information on drug-induced liver injury. Available at: http://livertox.nlm.nih.gov/Isoniazid.htm. Accessed January 7, 2014
16. Walker R. M., McElligott T. F. Furosemide induced hepatotoxicity. J Pathol: 1981; 135 4 301 314 (Pubitemid 12215921)
17. Taggart H. M., Alderdice J. M. Fatal cholestatic jaundice in elderly patients taking benoxaprofen. Br Med J (Clin Res Ed): 1982; 284 6326 1372
18. Hamdy R. C., Murnane B., Perera N., Woodcock K., Koch I. M. The pharmacokinetics of benoxaprofen in elderly subjects. Eur J Rheumatol Inflamm: 1982; 5 2 69 75 (Pubitemid 12010711)
19. Moses P. L., Schroeder B., Alkhatib O., Ferrentino N., Suppan T., Lidofsky S. D. Severe hepatotoxicity associated with bromfenac sodium. Am J Gastroenterol: 1999; 94 5 1393 1396 (Pubitemid 29214660)
20. Hunter E. B., Johnston P. E., Tanner G., Pinson C. W., Awad J. A. Bromfenac (Duract)-associated hepatic failure requiring liver transplantation. Am J Gastroenterol: 1999; 94 8 2299 2301 (Pubitemid 29374571)
21. Rabkin J. M., Smith M. J., Orloff S. L., Corless C. L., Stenzel P., Olyaei A. J. Fatal fulminant hepatitis associated with bromfenac use. Ann Pharmacother: 1999; 33 9 945 947 (Pubitemid 29420991)
22. Fontana R. J., McCashland T. M., Benner K. G., et al. The Acute Liver Failure Study Group. Acute liver failure associated with prolonged use of bromfenac leading to liver transplantation. Liver Transpl Surg: 1999; 5 6 480 484 (Pubitemid 29517862)
23. Gitlin N., Julie N. L., Spurr C. L., Lim K. N., Juarbe H. M. Two cases of severe clinical and histologic hepatotoxicity associated with troglitazone. Ann Intern Med: 1998; 129 1 36 38 (Pubitemid 28304650)
24. Vella A., de Groen P. C., Dinneen S. F. Fatal hepatotoxicity associated with troglitazone. Ann Intern Med: 1998; 129 12 1080
25. Herrine S. K., Choudhary C. Severe hepatotoxicity associated with troglitazone. Ann Intern Med: 1999; 130 2 163 164
26. Watkins P. B., Whitcomb R. W. Hepatic dysfunction associated with troglitazone. N Engl J Med: 1998; 338 13 916 917
27. Maria V. A., Victorino R. M. Hypersensitivity immune reaction as a mechanism for dilevalol-associated hepatitis. Ann Pharmacother: 1992; 26 7-8 924 926
28. He R. 2004, Clinical Review of Exanta (ximelagatran) Tablets, FDA Cardiovascular and Renal Drugs Advisory Committee Briefing Information. Available at: http://www.fda.gov/ohrms/dockets/ac/04/briefing/2004-4069B1-01- AstraZeneca-Backgrounder.pdf. Accessed January 7, 2014
29. Lee W. M., Larrey D., Olsson R., et al. Hepatic findings in long-term clinical trials of ximelagatran. Drug Saf: 2005; 28 4 351 370 (Pubitemid 40545769)
30. Ainscow E. K., Pilling J. E., Brown N. M., et al. Investigations into the liver effects of ximelagatran using high content screening of primary human hepatocyte cultures. Expert Opin Drug Saf: 2008; 7 4 351 365
31. Kenne K., Skanberg I., Glinghammar B., et al. Prediction of drug-induced liver injury in humans by using in vitro methods: the case of ximelagatran. Toxicol In Vitro: 2008; 22 3 730 746
32. Kramer J. A., Sagartz J. E., Morris D. L. The application of discovery toxicology and pathology towards the design of safer pharmaceutical lead candidates. Nat Rev Drug Discov: 2007; 6 8 636 649 (Pubitemid 47207750)
33. Olson H., Betton G., Robinson D., et al. Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol: 2000; 32 1 56 67
34. Release of Guidance Document Pre-market evaluation of hepatotoxicity in health Products. Available at: http://www.hc-sc.gc.ca/dhp-mps/alt-formats/pdf/ prodpharma/applic-demande/guide-ld/hepatotox-guide-ld-eng.pdf Accessed January 10, 2014
35. Uetrecht J. Idiosyncratic drug reactions: past, present, and future. Chem Res Toxicol: 2008; 21 1 84 92 (Pubitemid 351219710)
36. Horsmans Y., Desager J. P., Harvengt C. Biochemical changes and morphological alterations of the liver in guinea-pigs after administration of simvastatin (HMG CoA reductase-inhibitor). Pharmacol Toxicol: 1990; 67 4 336 339 (Pubitemid 20358741)
37. Kornbrust D. J., MacDonald J. S., Peter C. P., et al. Toxicity of the HMG-coenzyme A reductase inhibitor, lovastatin, to rabbits. J Pharmacol Exp Ther: 1989; 248 2 498 505 (Pubitemid 19090215)
38. Roth R. A., Ganey P. E. Animal models of idiosyncratic drug-induced liver injury-current status. Crit Rev Toxicol: 2011; 41 9 723 739
39. Corsini A., Ganey P., Ju C., et al. Current challenges and controversies in drug-induced liver injury. Drug Saf: 2012; 35 12 1099 1117
40. Katoh M., Matsui T., Nakajima M., et al. Expression of human cytochromes P450 in chimeric mice with humanized liver. Drug Metab Dispos: 2004; 32 12 1402 1410 (Pubitemid 39564560)
41. Antoine D. J., Williams D. P., Park B. K. Understanding the role of reactive metabolites in drug-induced hepatotoxicity: state of the science. Expert Opin Drug Metab Toxicol: 2008; 4 11 1415 1427
42. Kalgutkar A. S., Gardner I., Obach R. S., et al. A comprehensive listing of bioactivation pathways of organic functional groups. Curr Drug Metab: 2005; 6 3 161 225 (Pubitemid 40753853)
43. Williams D. P. Toxicophores: investigations in drug safety. Toxicology: 2006; 226 1 1 11 (Pubitemid 44287158)
44. Iwanaga T., Nakakariya M., Yabuuchi H., Maeda T., Tamai I. Involvement of bile salt export pump in flutamide-induced cholestatic hepatitis. Biol Pharm Bull: 2007; 30 4 739 744 (Pubitemid 46571003)
45. Usui T., Mise M., Hashizume T., Yabuki M., Komuro S. Evaluation of the potential for drug-induced liver injury based on in vitro covalent binding to human liver proteins. Drug Metab Dispos: 2009; 37 12 2383 2392
46. Obach R. S., Kalgutkar A. S., Soglia J. R., Zhao S. X. Can in vitro metabolism-dependent covalent binding data in liver microsomes distinguish hepatotoxic from nonhepatotoxic drugs? An analysis of 18 drugs with consideration of intrinsic clearance and daily dose. Chem Res Toxicol: 2008; 21 9 1814 1822
47. Park B. K., Boobis A., Clarke S., et al. Managing the challenge of chemically reactive metabolites in drug development. Nat Rev Drug Discov: 2011; 10 4 292 306
48. Watkins P. B., Zimmerman H. J., Knapp M. J., Gracon S. I., Lewis K. W. Hepatotoxic effects of tacrine administration in patients with Alzheimer's disease. JAMA: 1994; 271 13 992 998 (Pubitemid 24099919)
49. Liu Z. X., Govindarajan S., Kaplowitz N. Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology: 2004; 127 6 1760 1774 (Pubitemid 39575855)
50. Liu Z. X., Han D., Gunawan B., Kaplowitz N. Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology: 2006; 43 6 1220 1230 (Pubitemid 43980100)
51. Persson M., Loye A. F., Mow T., Hornberg J. J. A high content screening assay to predict human drug-induced liver injury during drug discovery. J Pharmacol Toxicol Methods: 2013; 68 3 302 313
52. Przybylak K. R., Cronin M. T. In silico models for drug-induced liver injury-current status. Expert Opin Drug Metab Toxicol: 2012; 8 2 201 217
53. Zhang M., Chen M., Tong W. Is toxicogenomics a more reliable and sensitive biomarker than conventional indicators from rats to predict drug-induced liver injury in humans? Chem Res Toxicol: 2012; 25 1 122 129
54. Low Y., Uehara T., Minowa Y., et al. Predicting drug-induced hepatotoxicity using QSAR and toxicogenomics approaches. Chem Res Toxicol: 2011; 24 8 1251 1262
55. Corvi R., Ahr H. J., Albertini S., et al. Meeting report: Validation of toxicogenomics-based test systems: ECVAM-ICCVAM/NICEATM considerations for regulatory use. Environ Health Perspect: 2006; 114 3 420 429 (Pubitemid 43338268)
56. Senior John. Lessons from isoniazid. Would it be approved today? Available at: www.fda.gov/downloads/Drugs/ScienceResearch/../ucm076755.pdf. Accessed January 7, 2014
57. Mitchell J. R., Long M. W., Thorgeirsson U. P., Jollow D. J. Acetylation rates and monthly liver function tests during one year of isoniazid preventive therapy. Chest: 1975; 68 2 181 190
58. Nolan C. M., Goldberg S. V., Buskin S. E. Hepatotoxicity associated with isoniazid preventive therapy: a 7-year survey from a public health tuberculosis clinic. JAMA: 1999; 281 11 1014 1018 (Pubitemid 29143893)
59. Harrill A. H., Roach J., Fier I., et al. The effects of heparins on the liver: application of mechanistic serum biomarkers in a randomized study in healthy volunteers. Clin Pharmacol Ther: 2012; 92 2 214 220
60. Cohen D. E., Anania F. A., Chalasani N.; National Lipid Association Statin Safety Task Force Liver Expert Panel. An assessment of statin safety by hepatologists. Am J Cardiol: 2006; 97 8A 77C 81C
61. Olsson R., Korsan-Bengtsen B. M., Korsan-Bengtsen K., Lennartsson J., Waldenström J. Serum aminotransferases after low-dose heparin treatment. Short communication. Acta Med Scand: 1978; 204 3 229 230 (Pubitemid 9024660)
62. Dukes G. E. Jr, Sanders S. W., Russo J. Jr., et al. Transaminase elevations in patients receiving bovine or porcine heparin. Ann Intern Med: 1984; 100 5 646 650 (Pubitemid 14143936)
63. Carlson M. K., Gleason P. P., Sen S. Elevation of hepatic transaminases after enoxaparin use: case report and review of unfractionated and low-molecular-weight heparin-induced hepatotoxicity. Pharmacotherapy: 2001; 21 1 108 113 (Pubitemid 32047579)
64. Lucena M. I., Molokhia M., Shen Y., et al. Spanish DILI Registry; EUDRAGENE; DILIN; DILIGEN; International SAEC. Susceptibility to amoxicillin-clavulanate-induced liver injury is influenced by multiple HLA class I and II alleles. Gastroenterology: 2011; 141 1 338 347
65. Kleiner D. E., Gaffey M. J., Sallie R., et al. Histopathologic changes associated with fialuridine hepatotoxicity. Mod Pathol: 1997; 10 3 192 199 (Pubitemid 27130467)
66. Berends M. AM, Snoek J., de Jong E. M., et al. Liver injury in long-term methotrexate treatment in psoriasis is relatively infrequent. Aliment Pharmacol Ther: 2006; 24 5 805 811
67. Temple R. Hy's law: predicting serious hepatotoxicity. Pharmacoepidemiol Drug Saf: 2006; 15 4 241 243
68. Senior J. R. Regulatory perspectives. In: Kaplowitz N., DeLeve L. D., eds. Drug-Induced Liver Disease. New York, NY Marcel Dekker: 2003; 739 754
69. Björnsson E., Olsson R. Outcome and prognostic markers in severe drug-induced liver disease. Hepatology: 2005; 42 2 481 489 (Pubitemid 41061102)
70. Andrade R. J., Lucena M. I., Fernández M. C., et al. Spanish Group for the Study of Drug-Induced Liver Disease. Drug-induced liver injury: an analysis of 461 incidences submitted to the Spanish registry over a 10-year period. Gastroenterology: 2005; 129 2 512 521 (Pubitemid 41096639)
71. Food and Drug Administration Guidance for clinical trial sponsors on the establishment and operation of clinical trial data monitoring committees. Available at: http://www.fda.gov/downloads/Regulatoryinformation/Guidances/ ucm127073.pdf. Accessed January 7, 2014
72. Slutsky A. S., Lavery J. V. Data safety and monitoring boards. N Engl J Med: 2004; 350 11 1143 1147 (Pubitemid 38298996)
73. Guo T., Gelperin K., Senior J. A tool to help you decide (detect potentially serious liver injury). Available at: http://www.fda.gov/downloads/ Drugs/ScienceResearch/ResearchAreas/ucm076777.pdf. Accessed December 17, 2009
74. Watkins P. B., Desai M., Berkowitz S. D., et al. Evaluation of drug-induced serious hepatotoxicity (eDISH): application of this data organization approach to phase III clinical trials of rivaroxaban after total hip or knee replacement surgery. Drug Saf: 2011; 34 3 243 252
75. Chitturi S., Farrell G. C. Drug induced liver disease. In: Schiff E. R. et al, eds. Schiff's diseases of the liver. 11th ed. Hoboken, NJ Wiley-Blackwell: 2012; 703 782
76. Shapiro M. A., Lewis J. H. Causality assessment of drug-induced hepatotoxicity: promises and pitfalls. Clin Liver Dis: 2007; 11 3 477 505, v (Pubitemid 47302343)
77. Fontana R. J., Watkins P. B., Bonkovsky H. L., et al. DILIN Study Group. Drug-Induced Liver Injury Network (DILIN) prospective study: rationale, design and conduct. Drug Saf: 2009; 32 1 55 68
78. Starkey Lewis P. J., Dear J., Platt V., et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology: 2011; 54 5 1767 1776
79. Locke J. E., Sun Z., Warren D. S., et al. Generation of humanized animal livers using embryoid body-derived stem cell transplant. Ann Surg: 2008; 248 3 487 493