Drug-induced hepatotoxicity

New England Journal of Medicine

Volumn 349, Issue 5, 2003, Pages 474-485

  Lee, William M ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; AMIODARONE; BROMFENAC; COCAINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; METHOTREXATE; NICOTINIC ACID; ORAL CONTRACEPTIVE AGENT; PARACETAMOL; PHENCYCLIDINE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; BENZOPHENONE DERIVATIVE; BROMOBENZENE; CHROMAN DERIVATIVE; DRUG; NONSTEROID ANTIINFLAMMATORY AGENT; THIAZOLE DERIVATIVE; TROGLITAZONE;

BIOTRANSFORMATION; CHOLESTASIS; DOSE RESPONSE; DRUG HYPERSENSITIVITY; DRUG INDUCED DISEASE; FATTY LIVER; HUMAN; LIVER ADENOMA; LIVER FAILURE; LIVER INJURY; LIVER NECROSIS; LIVER TOXICITY; PRIORITY JOURNAL; REVIEW; CHEMICALLY INDUCED DISORDER; DRUG APPROVAL; DRUG EFFECT; LIVER; LIVER CIRRHOSIS; LIVER DISEASE; LIVER FUNCTION TEST; METABOLISM; PATHOLOGY; PHARMACOLOGY;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BENZOPHENONES; BROMOBENZENES; CHROMANS; DRUG APPROVAL; HUMANS; HYPOGLYCEMIC AGENTS; LIVER; LIVER CIRRHOSIS; LIVER DISEASES; LIVER FUNCTION TESTS; PHARMACEUTICAL PREPARATIONS; PHARMACOLOGY; THIAZOLES; THIAZOLIDINEDIONES;

EID: 0041342015     PISSN: 00284793     EISSN: None     Source Type: Journal    
DOI: 10.1056/NEJMra021844     Document Type: Review

References (104)

1. Lazarou J, Pomeranz BH, Corey PN. Incidence of adverse drug reactions in hospitalized patients. JAMA 1998;279:1200-5.
2. Ostapowicz G, Fontana KI, Schiødt FV, et al. Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med 2002;137: 947-54.
3. Bissell DM, Gores GJ, Laskin DL, Hoofnagle JH. Drug-induced liver injury: mechanisms and test systems. Hepatology 2001; 33:1009-13.
4. Center for Drug Evaluation and Research. Drug-induced liver toxicity. (Accessed July 8, 2003, at http://www.fda.gov/cder/livertox/default.htm.)
5. Weinshilboum R. Inheritance and drug response. N Engl J Med 2003;348:529-37.
6. Guengerich FP. Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 2001;14:611-50.
7. Hunt CM, Westerkam WR, Stave GM. Effect of age and gender on the activity of human hepatic GYP3A. Biochem Pharmacol 1992;44:275-83.
8. Ikemoto S, Imaoka S, Hayahara N, Maekawa M, Funae Y. Expression of hepatic microsomal cytochrome P450s as altered by uremia. Biochem Pharmacol 1992;43:2407-12.
9. Moss AJ. The QT interval and torsades de pointes. Drug Saf 1999;21:Suppl 1:5-10.
10. Thummel KE, Slattery JT, Ro H, et al. Ethanol and production of the hepatotoxic metabolite of acetaminophen in healthy adults. Clin Pharmacol Ther 2000;67:591-9.
11. Trauner M, Meier PJ, Boyer J. Molecular pathogenesis of cholestasis. N Engl J Med 1998;339:1217-27.
12. Robin M-A, Le Roy M, Descatoire V, Pessayre D. Plasma membrane cytochromes P450 as neoantigens and autoimmune targets in drug-induced hepatitis. J Hepatol 1997;26:Suppl 1:23-30.
13. Reed JC. Apoptosis-regulating proteins as targets for drug discovery. Trends Mol Med 2001;7:314-9.
14. Pessayre D, Berson A, Fromenty B, Mansouri A. Mitochondria in steatohepatitis. Semin Liver Dis 2001;21:57-69.
15. Yun CH, Okerholm RA, Guengerich FP. Oxidation of the antihistamine drug terfenadine in human liver microsomes: role of cytochrome P-450 3A(4) in N-dealkylation and C-hydroxylation. Drug Metab Dispos 1993; 21:403-9.
16. Beaune P, Dansette PM, Mansuy D, et al. Human anti-endoplasmic reticulum autoantibodies appearing in a drug-induced hepatitis are directed against a human liver cytochrome P-450 that hydroxylates the drug. Proc Natl Acad Sci U S A 1987;84:551-5.
17. Jaeschke H, Gores GJ, Cederbaum AI, Hinson JA, Pessayre D, Lemasters JJ. Mechanisms of hepatotoxicity. Toxicol Sci 2002;66: 166-76.
18. Jonsson JR, Edwards-Smith GJ, Catania SC, et al. Expression of cytokines and factors modulating apoptosis by human sinusoidal lymphocytes. J Hepatol 2000;32:392-8.
19. DeLeve LD, Shulman H, McDonald GB. Toxic injury to hepatic sinusoids: sinusoidal obstruction syndrome (veno-occlusive disease). Semin Liver Dis 2002;22:27-42.
20. Brosens I, Johannisson E, Baulieu E-E, et al. Oral contraceptives and hepatocellular carcinoma. Br Med J 1986;292:1667-8.
21. Huang Y-S, Chern H-D, Su W-J, et al. Polymorphism of the N-acetyltransferase 2 gene as a susceptibility risk factor for antituberculosis drug-induced hepatitis. Hepatology 2002;35:883-9.
22. Watkins PB. Drug metabolism by cytochromes P450 in the liver and small bowel. Gastroenterol Clin North Am 1992;21:511-26.
23. Hautekeete ML, Horsmans Y, Van Waeyenberge C, et al. HLA association of amoxicillin-clavulanate-induced hepatitis. Gastroenterology 1999;117:1181-6.
24. Cai H, Guengerich FP. Reaction of trichlorethylene oxide with proteins and DNA: instability of adducts and modulation of functions. Chem Res Toxicol 2001;14:54-61.
25. Aithal GP, Daly AK, Leathart J, Yuanneng CP, Day CP. Promoter polymorphisms of interleukin-10 (IL-10) and interleukin-4 (IL-4) predict the risk of diclofenac-induced hepatotoxicity. Gastroenterology 2000;118:Suppl 2:A977. abstract.
26. Bernal W, Donaldson P, Underhill J, Wendon J, Williams R. Tumor necrosis genomic polymorphisms and outcome of acetaminophen (paracetamol)-induced acute liver failure. J Hepatol 1998;29:53-9.
27. Zhang J, Huang W, Chua SS, Wei P, Moore DD. Modulation of acetaminophen-induced hepatotoxicity by the xenobiotic receptor CAR. Science 2002;298:422-4.
28. Phillips KA, Veenstra DL, Oren E, Lee JK, Sadee W. Potential role of pharmacogenomics in reducing adverse drug reactions: a systematic review. JAMA 2001;286:2270-9.
29. Kleckner H, Yakulis V, Heller P. Severe hypersensitivity to diphenylhydantoin with circulating antibodies to the drug. Ann Intern Med 1975;83:522-3.
30. Kenna JG. Immunoallergic drug-induced hepatitis: lessons from halothene. J Hepatol 1997;26:Suppl 1:5-12.
31. Chitturi S, Farrell GC. Drug-induced cholestasis. Semin Gastrointest Dis 2001;12: 113-24.
32. Schiødt FV, Rochling FJ, Casey DL, Lee WM. Acetaminophen toxicity in an urban county hospital. N Engl J Med 1997;337: 1112-7.
33. Schmidt LE, Dalhoff K, Poulsen HE. Acute versus chronic alcohol consumption in acetaminophen-induced hepatotoxicity. Hepatology 2002;35:876-82.
34. Whitcomb DC, Block GD. Association of acetaminophen hepatotoxicity with fasting and ethanol use. JAMA 1994;272:1845-50.
35. Wang K, Huang YS, Deng JF, et al. Characteristics and risk factors of acetaminophen-induced hepatitis in Taiwan. Zhonghua Yi Xue Za Zhi (Taipei) 1999;62:369-75.
36. Heubi J, Barbacci MB, Zimmerman HJ. Therapeutic misadventures with acetaminophen hepatotoxicity after multiple doses in children. J Pediatr 1998;132:22-7.
37. Moynihan R. FDA fails to reduce accessibility of paracetamol despite 450 deaths a year. BMJ 2002;325:678.
38. Chitturi S, Farrell GC. Herbal hepatoxicity: an expanding but poorly defined problem. J Gastroenterol Hepatol 2000;10:1093-9.
39. Stedman C. Herbal hepatotoxicity. Semin Liver Dis 2002;22:195-206.
40. Favreau JT, Ryu ML, Braunstein G, et al. Severe hepatotoxicity associated with the dietary supplement LipoKinetix. Ann Intern Med 2002;136:590-5.
41. Danan G, Benichou C. Causality assessment of adverse reactions to drugs. I. A novel method based on the conclusions of international consensus meetings: application to drug-induced liver injuries. J Clin Epidemiol 1993;46:1323-30.
42. Benichou C, Danan G, Flahault A. Causality assessment of adverse reactions to drugs. II. An original model for validation of drug causality assessment methods: case reports with positive rechallenge. J Clin Epidemiol 1993;46:1331-6.
43. Lucena MI, Camargo R, Andrade RJ, Perez-Sanchez CJ, Sanchez De La Cuesta F. Comparison of two clinical scales for causality assessment in hepatotoxicity. Hepatology 2001;33:123-30.
44. Kaplowitz N. Causality assessment versus guilt-by-association in drug hepatotoxicity. Hepatology 2001;33:308-10.
45. George J, Murray K, Byth K, Farrell GC. Differential alterations of cytochrome P450 proteins in livers from patients with severe chronic liver disease. Hepatology 1995;21: 120-8.
46. Adedoyin A, Arns PA, Richards WO, Wilkinson GR, Branch RA. Selective effect of liver disease on the activities of specific metabolizing enzymes: investigation of cytochromes P450 2C19 and 2D6. Clin Pharmacol Ther 1998;64:8-17.
47. Weltman MD, Farrell GC, Hall P, Ingelman-Sundberg M, Liddle C. Hepatic cytochrome P450 ZE1 is increased in patients with nonalcoholic steatohepatitis. Hepatology 1998;27:128-33.
48. Burckart GJ, Frye RF, Kelly P, et al. Induction of CYPZE1 activity in liver transplant patients as measured by chlorzoxazone 6-hydroxylation. Clin Pharmacol Ther 1998; 63:296-302.
49. Froomes PRA, Morgan DJ, Smallwood RA, Angus PW. Comparative effects of oxygen supplementation on theophylline and acetaminophen clearance in human cirrhosis. Gastroenterology 1999;116:915-20.
50. Strasser SI, Myerson D, Spurgeon CL, et al. Hepatitis C virus infection and bone marrow transplantation: a cohort study with 10-year follow-up. Hepatology 1999;29:1893-9.
51. Clark CJ, Creighton S, Portmann B, Taylor C, Wendon JA, Cramp ME. Acute liver failure associated with antiretroviral treatment for HIV: a report of six cases. J Hepatol 2002; 36:295-301.
52. Pol S, Vallet-Pichard A, Fontaine H. Hepatitis C and human immune deficiency coinfection at the era of highly active antiretroviral therapy. J Viral Hepat 2002;9:1-8.
53. Schenker S, Martin RR, Hoyumpa AM. Antecedent liver disease and drug toxicity. J Hepatol 1999;31:1098-105.
54. Zimmerman HJ. Hepatotoxicity: the adverse effects of drugs and other chemicals on the liver. New York: Appleton-Century-Crofts, 1978.
55. Code of federal regulations. 21. Good clinical practices. Princeton, NJ.: Bristol-Myers Squibb, 1996.
56. Lasser KE, Allen PD, Woolhandler SJ, Himmelstein DU, Wolfe SM, Bor DH. Timing of new black box warnings and withdrawals for prescription medications. JAMA 2002; 287:2215-26.
57. Sgro C, Clinard F, Ouazir K, et al. Incidence of drug-induced hepatic injuries: a French population-based study. Hepatology 2002;36:451-5.
58. Meadows M. Serious liver injury: leading reason for drug removals, restrictions. FDA Consum 2001;35:8-9.
59. Carrillo-Jimenez R, Nurnberger M. Celecoxib-induced acute pancreatitis and hepatitis: a case report. Arch Intern Med 2000;160: 553-4.
60. Banks AT, Zimmerman HJ, Ishak KG, Harter JG. Diclofenac-associated hepatotoxicity: analysis of 180 cases reported to the Food and Drug Administration as adverse reactions. Hepatology 1995;22:820-7.
61. Chitturi S, George J. Hepatotoxicity of commonly used drugs: nonsteroidal antiinflammatory drugs, antihypertensives, antidiabetic agents, anticonvulsants, lipid-lowering agents, psychotropic drugs. Semin Liver Dis 2002;22:169-83.
62. Fontana RJ, McCashland TM, Benner KG, et al. Acute liver failure associated with prolonged use of bromfenac leading to liver transplantation. Liver Transpl Surg 1999;5: 480-4.
63. Gitlin N, Julie NL, Spurr CL, Lim KN, Juarbe HM. Two cases of severe clinical and histologic hepatotoxicity associated with troglitazone. Ann Intern Med 1998;129:36-8.
64. Neuschwander-Tetri BA, Isley WL, Oki JC, et al. Troglitazone-induced hepatic failure leading to liver transplantation: a case report. Ann Intern Med 1998;129:38-41.
65. Murphy EJ, Davern TJ, Shakil OA, et al. Troglitazone-induced fulminant hepatic failure. Dig Dis Sci 2000;45:549-53.
66. Malik AH, Prasad P, Saboorian MH, Thiele DH, Malet PF. Hepatic injury due to troglitazone. Dig Dis Sci 2000;45:210-4.
67. Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ. Role of quinones in toxicology. Chem Res Toxicol 2000;13:135-40.
68. Al-Salman J, Arjomand H, Kemp DG, Mittal M. Hepatocellular injury in a patient receiving rosiglitazone: a case report. Ann Intern Med 2000;132:121-4.
69. Forman LM, Simmons DA, Diamond RH. Hepatic failure in a patient taking rosiglitazone. Ann Intern Med 2000;132:118-21.
70. May LD, Lefkowitch JH, Kram MT, Rubin DE. Mixed hepatocellular-cholestatic liver injury after pioglitazone therapy. Ann Intern Med 2002;136:449-52.
71. Garibaldi RA, Drusin U, Ferebee SH, Gregg MB. Isoniazid associated hepatitis: report of an outbreak. Am Rev Respir Dis 1972;106:357-65.
72. Nolan CM, Goldberg SV, Buskin SE. Hepatotoxicity associated with isoniazid preventive therapy: a 7-year survey from a public health tuberculosis clinic. JAMA 1999;281: 1014-8.
73. Sreenarasinahaiah J, Shiels P, Lisker-Melman M. Multiorgan failure induced by atorvastatin. Am J Med 2002;113:348-9.
74. Kaufman KR. Carbamazepine, hepatotoxicity, organic solvents, and paints. Seizure 1999;8:250-2.
75. Baylor P, Williams K. Interstitial nephritis, thrombocytopenia, hepatitis, and elevated serum amylase levels in a patient receiving clarithromycin therapy. Clin Infect Dis 1999;29:1350-1.
76. Gonzalez de la Puenta MA, Calderon E, Espinosa R, Rincon M, Varela JM. Fatal hepatotoxicity associated with enalapril. Ann Pharmacother 2001;35:1492.
77. Capella D, Bruguera M, Fugueras A, Laporte J. Fluoxetine-induced hepatitis: why is postmarketing surveillance needed? Eur J Clin Pharmacol 1999;55:545-6.
78. Kraus I, Vitezic D, Oguic R. Flutamide-associated acute hepatitis in advanced prostate cancer patients. Int J Clin Pharm Ther 2001;39:395-9.
79. Lasso-de-la-Vega MC, Zapater P, Such J, Perez-Mateo M, Horga JF. Gabapentin-induced hepatotoxicity. Am J Gastroenterol 2001;96:3460-2.
80. Vergis E, Paterson DL, Singh N. Indinavir-associated hepatitis in patients with advanced HIV infection. Int J STD AIDS 1998; 9:53.
81. Sphar L, Rubbia-Brandt L, Marinescu O, Armenian B, Hadengue A. Acute fatal hepatitis related to levofloxacin. J Hepatol 2001; 35:308-9.
82. Bosch X. Losartan-induced hepatotoxicity. JAMA 1997;278:1572.
83. Hwang I, Daniels AM, Holtzmuller KC. "Ecstasy"-induced hepatitis in an active duty soldier. Mil Med 2002;167:155-6.
84. Deltenre P, Berson A, Marcellin P, Degott C, Biour M, Pessayre D. Mesalazine (5-aminosalicylic acid) induced chronic hepatitis. Gut 1999;44:886-8.
85. Babich MM, Pike I, Shiffman ML. Metformin-induced acute hepatitis. Am J Med 1998;104:490-2.
86. Piliero PJ, Purdy B. Nevirapine-induced hepatitis: a case series and review of the literature. AIDS Read 2001;11:379-82.
87. Aranda-Michel J, Koehler A, Bejarano PA, et al. Nefazodone-induced liver failure: report of three cases. Ann Intern Med 1999; 130;285-8.
88. Romero-Gomez M, Suarez Garcia E, Fernandez MC. Norfloxacin-induced acute cholestatic hepatitis in a patient with alcoholic liver cirrhosis. Am J Gastroenterol 1999; 94:2324-5.
89. Benbow SJ, Gill G. Paroxetine and hepatotoxicity. BMJ 1997;314:1387.
90. Rosh JR, Dellert SF, Narkewicz M, Birnbaum A, Whitington G. Four cases of severe hepatotoxicity associated with pemoline: possible autoimmune pathogenesis. Pediatrics 1998;101:921-3.
91. Hartleb M, Rymarczyk G, Januszewski K. Acute cholestatic hepatitis associated with pravastatin. Am J Gastroenterol 1999;94: 1388-90.
92. Ribeiro JM, Lucas M, Baptista A, Victorino RM. Fatal hepatitis with ranitidine. Am J Gastroenterol 2000;95:559-60.
93. Benazzi F. Risperidone-induced hepatotoxicity. Pharmacopsychiatry 1998;31:241.
94. Gupta AK, del Rosso JQ, Lynde CW. Brown GH, Shear NH. Hepatitis associated with terbinafine therapy: three case reports and a review of the literature. Clin Exp Dermatol 1998;23:64-7.
95. Iqbal M, Geonka P, Young MF, Thomas E, Borthwick TR. Ticlopidine-induced cholestatic hepatitis: report of three cases and review of the literature. Dig Dis Sci 1998;43: 2223-6.
96. Olanow CW. Tolcapone and hepatotoxic effects. Arch Neurol 2000;57:263-7.
97. Fernandes NF, Martin RR, Schenker S. Trazodone-induced hepatotoxicity: a case report with comments on drug-induced hepatotoxicity. Am J Gastroenterol 2000;95: 532-5.
98. Lucena MI, Andrade RJ, Rodrigo L, et al. Trovafloxacin-induced acute hepatitis. Clin Infect Dis 2000;30:400-1.
99. Konig SA, Schenk M, Sick C, et al. Fatal liver failure associated with valproate therapy in a patient with Friedreich's ataxia: review of valproate hepatotoxicity in adults. Epilepsia 1999;40:1036-40.
100. Cardona X, Avila A, Castellanos P. Venlaxafine-associated hepatitis. Ann Intern Med 2000;132:417.
101. Benninger J, Schneider HT, Schuppan D, Kirchner T, Hahn EG. Acute hepatitis induced by greater celandine (Chelidonium majus). Gastroenterology 1999;117:1234-7.
102. Campo JV, McNabb M, Perel JM, Mazariegos GV, Hasegawa SI, Reyes J. Kava-induced fulminant hepatic failure. J Am Acad Child Adolescent Psych 2002;41:631-2.
103. Angell M, Kassirer JP. Alternative medicine - the risks of the untested and unregulated remedies. N Engl J Med 1998;339: 839-41.
104. Graham DJ, Green L, Senior JR. Hyperacute liver failure induced by troglitazone: what did we learn and what do we need to learn? Hepatology 2002;36:168A. abstract.