Drug-Induced Cholestasis

Clinics in Liver Disease

Volumn 17, Issue 2, 2013, Pages 191-209

  Bjornsson, Einar S ^a   Jonasson, Jon Gunnlaugur ^a  

^a LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

Author keywords

Cholestasis; Drug induced liver injury; Drugs; Liver disease; Pathology

Indexed keywords

AMIODARONE; AMOXICILLIN; AMOXICILLIN PLUS CLAVULANIC ACID; ANABOLIC AGENT; BOSENTAN; CARBAMAZEPINE; CHLORPROMAZINE; CLARITHROMYCIN; CLOXACILLIN; DICLOXACILLIN; ERYTHROMYCIN; FLUCLOXACILLIN; GLIBENCLAMIDE; IBUPROFEN; ORAL CONTRACEPTIVE AGENT; OXACILLIN; PENICILLIN G; PROCHLORPERAZINE; PROTON PUMP INHIBITOR; PSYCHOTROPIC AGENT; RIFAMPICIN; SULINDAC; TEMAFLOXACIN; TERBINAFINE; TIABENDAZOLE; TROGLITAZONE; TROVAFLOXACIN; UNINDEXED DRUG; WARFARIN; ZONISAMIDE;

AGE; CHOLESTASIS; GENE LINKAGE DISEQUILIBRIUM; HAPLOTYPE; HEREDITY; HUMAN; LIVER CIRRHOSIS; LIVER FAILURE; MORTALITY; PATHOPHYSIOLOGY; PROGNOSIS; PRURITUS; REVIEW; RISK ASSESSMENT; TOXIC HEPATITIS;

ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; ANTI-RETROVIRAL AGENTS; ANTIFUNGAL AGENTS; CHOLESTASIS; CHRONIC DISEASE; DRUG-INDUCED LIVER INJURY; HUMANS; PROGNOSIS; PSYCHOTROPIC DRUGS; RISK FACTORS;

EID: 84875588861     PISSN: 10893261     EISSN: 15578224     Source Type: Journal    
DOI: 10.1016/j.cld.2012.11.002     Document Type: Review

References (119)

1. 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, 46:1331-1336.
2. 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, 46:1323-1330.
3. Kleiner D.E. The pathology of drug-induced liver injury. Semin Liver Dis 2009, 29:364-372.
4. Zimmerman H. Hepatotoxicity: the adverse effects of drugs and other chemicals on the liver 1999, Lippincott Williams & Wilkins, Philadelphia.
5. Bjornsson E., Olsson R. Outcome and prognostic markers in severe drug-induced liver disease. Hepatology 2005, 42:481-489.
6. Moradpour D., Altorfer J., Flury R., et al. Chlorpromazine-induced vanishing bile duct syndrome leading to biliary cirrhosis. Hepatology 1994, 20:1437-1441.
7. Rochon J., Protiva P., Seeff L.B., et al. Reliability of the Roussel Uclaf Causality Assessment Method for assessing causality in drug-induced liver injury. Hepatology 2008, 48:1175-1183.
8. Rockey D.C., Seeff L.B., Rochon J., et al. Causality assessment in drug-induced liver injury using a structured expert opinion process: comparison to the Roussel-Uclaf causality assessment method. Hepatology 2010, 51:2117-2126.
9. Hayashi P.H. Causality assessment in drug-induced liver injury. Semin Liver Dis 2009, 29:348-356.
10. Maggio M.C., Liotta A., Cardella F., et al. Stevens-Johnson syndrome and cholestatic hepatitis induced by acute Epstein-Barr virus infection. Eur J Gastroenterol Hepatol 2011, 23:289.
11. Ratnayake E.C., Shivanthan C., Wijesiriwardena B.C. Cholestatic hepatitis in a patient with typhoid fever - a case report. Ann Clin Microbiol Antimicrob 2011, 10:35.
12. Choi H.C., Lee S.H., Kim J., et al. A case of acute q Fever with severe acute cholestatic hepatitis. Gut Liver 2009, 3:141-144.
13. Breidert M., Offensperger S., Blum H.E., et al. Weight loss and severe jaundice in a patient with hyperthyroidism. Z Gastroenterol 2011, 49:1267-1269.
14. Sgro C., Clinard F., Ouazir K., et al. Incidence of drug-induced hepatic injuries: a French population-based study. Hepatology 2002, 36:451-455.
15. Lucena M.I., Andrade R.J., Rodrigo L., et al. Trovafloxacin-induced acute hepatitis. Clin Infect Dis 2000, 30:400-401.
16. Lammert C., Einarsson S., Niklasson A., et al. Relationship between daily dose of oral medications and idiosyncratic drug-induced liver injury (DILI). Search for signals. Hepatology 2008, 47:2003-2009.
17. Lucena M.I., Andrade R.J., Kaplowitz N., et al. Phenotypic characterization of idiosyncratic drug-induced liver injury: the influence of age and gender. Hepatology 2009, 49:2001-2009.
18. Lammert C., Bjornsson E., Niklasson A., et al. Oral medications with significant hepatic metabolism at higher risk for hepatic adverse events. Hepatology 2010, 51:615-620.
19. Lucena M.I., Kaplowitz N., Hallal H., et al. Recurrent drug-induced liver injury (DILI) with different drugs in the Spanish Registry: the dilemma of the relationship to autoimmune hepatitis. J Hepatol 2011, 55:820-827.
20. Andrade R.J., Lucena M.I., Fernandez M.C., et al. Drug-induced liver injury: an analysis of 461 incidences submitted to the Spanish Registry over a 10-year period. Gastroenterology 2005, 129:512-521.
21. Meier Y., Pauli-Magnus C., Zanger U.M., et al. Interindividual variability of canalicular ATP-binding-cassette (ABC)-transporter expression in human liver. Hepatology 2006, 44:62-74.
22. Leevy C.B., Koneru B., Klein K.M. Recurrent familial prolonged intrahepatic cholestasis of pregnancy associated with chronic liver disease. Gastroenterology 1997, 113:966-972.
23. Lindberg M.C. Hepatobiliary complications of oral contraceptives. J Gen Intern Med 1992, 7:199-209.
24. Bachs L., Pares A., Elena M., et al. Effects of long-term rifampicin administration in primary biliary cirrhosis. Gastroenterology 1992, 102:2077-2080.
25. Prince M.I., Burt A.D., Jones D.E. Hepatitis and liver dysfunction with rifampicin therapy for pruritus in primary biliary cirrhosis. Gut 2002, 50:436-439.
26. Hautekeete M.L., Horsmans Y., Van Waeyenberge C., et al. HLA association of amoxicillin-clavulanate-induced hepatitis. Gastroenterology 1999, 117:1181-1186.
27. O'Donohue J., Oien K.A., Donaldson P., et al. Co-amoxiclav jaundice: clinical and histological features and HLA class II association. Gut 2000, 47:717-720.
28. Andrade R.J., Lucena M.I., Alonso A., et al. HLA class II genotype influences the type of liver injury in drug-induced idiosyncratic liver disease. Hepatology 2004, 39:1603-1612.
29. Daly A.K., Donaldson P.T., Bhatnagar P., et al. HLA-B*5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin. Nat Genet 2009, 41:816-821.
30. Meier Y., Zodan T., Lang C., et al. Increased susceptibility for intrahepatic cholestasis of pregnancy and contraceptive-induced cholestasis in carriers of the 1331T>C polymorphism in the bile salt export pump. World J Gastroenterol 2008, 14:38-45.
31. Brown P.J., Lesna M., Hamlyn A.M., et al. Primary biliary cirrhosis after long-term practolol administration. Br Med J 1978, 1(6127):1591.
32. Ludwig J. Idiopathic adulthood ductopenia: an update. Mayo Clin Proc 1998, 73:193-199.
33. Degott C., Feldmann G., Larrey D., et al. Drug-induced prolonged cholestasis in adults: a histological semiquantitative study demonstrating progressive ductopenia. Hepatology 1992, 15:244-251.
34. Olsson R., Wiholm B.E., Sand C., et al. Liver damage from flucloxacillin, cloxacillin and dicloxacillin. J Hepatol 1992, 15:154-161.
35. Desmet V. Vanishing bile duct syndrome in drug-induced liver disease. J Hepatol 1997, 26:31-35.
36. Davies M.H., Harrison R.F., Elias E., et al. Antibiotic-associated acute vanishing bile duct syndrome: a pattern associated with severe, prolonged, intrahepatic cholestasis. J Hepatol 1994, 20:112-116.
37. Forbes G.M., Jeffrey G.P., Shilkin K.B., et al. Carbamazepine hepatotoxicity: another cause of the vanishing bile duct syndrome. Gastroenterology 1992, 102:1385-1388.
38. Ramos A.M., Gayotto L.C., Clemente C.M., et al. Reversible vanishing bile duct syndrome induced by carbamazepine. Eur J Gastroenterol Hepatol 2002, 14:1019-1022.
39. Padda M.S., Sanchez M., Akhtar A.J., et al. Drug-induced cholestasis. Hepatology 2011, 53:1377-1387.
40. Gregory D.H., Zaki G.F., Sarcosi G.A., et al. Chronic cholestasis following prolonged tolbutamide administration. Arch Pathol 1967, 84:194-201.
41. Glober G.A., Wilkenson J.A. Biliary cirrhosis following administration of methyltestosterone. JAMA 1968, 204:170-173.
42. Ishii M., Miyazaki Y., Yamamoto T., et al. A case of drug-induced ductopenia resulting in fatal biliary cirrhosis. Liver 1993, 13:227-231.
43. Eckstein R.P., Dowsett J.F., Lunzer M.R. Flucloxacillin induced liver disease: histopathological findings at biopsy and autopsy. Pathology 1993, 25:223-238.
44. Vuppalanchi R., Chalasani N., Saxena R. Restoration of bile ducts in drug-induced vanishing bile duct syndrome due to zonisamide. Am J Surg Pathol 2006, 30:1619-1623.
45. Alpini G., Lenzi R., Sarkozi L., et al. Biliary physiology in rats with bile ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J Clin Invest 1988, 81:569-578.
46. Anderson J. On hemorrhage from the umbilicus after the separation of the fetus. Boston Med Surg J 1850, 41:440-442.
47. Crawford J.M. Basic mechanisms in hepatopathology. MacSween's pathology of the liver 2007, 75-117. Churchill Livingstone Elsevier, Philadelphia. 5th edition. A.D. Burt, B.C. Portmann, L.D. Ferrell (Eds.).
48. Trauner M., Boyer J.L. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 2003, 83:633-671.
49. Biopsy interpretation of the liver 2009, Lippincott Williams & Wilkins, Philadelphia. 2nd edition. S.A. Geller, L.M. Petrovic (Eds.).
50. Friis H., Andreasen P.B. Drug induced hepatic injury: an analysis of 1100 cases reported to the Danish Committee on adverse drug reactions between 1978 and 1987. J Intern Med 1992, 232:133-138.
51. Björnsson E., Kalaitzakis E., Olsson R. The impact of eosinophilia and hepatic necrosis on prognosis in patients with drug-induced liver injury. Aliment Pharmacol Ther 2007, 25:1411-1421.
52. Ramanchandran R., Kakar S. Histological patterns in drug-induced liver disease. J Clin Pathol 2009, 62:481-492.
53. Larrey D., Vial T., Micaleff A., et al. Hepatitis associated with amoxicillin-clavulanic acid combination: report of 15 cases. Gut 1992, 33:368-371.
54. Chang C.C., Petrelli M., Thomashefski J.F., et al. Severe intrahepatic cholestasis caused by amiodarone toxicity after withdrawal of the drug: a case report and review of the literature. Arch Pathol Lab Med 1999, 123:251-256.
55. Gibson G.G., Skett P. Introduction to drug metabolism 2001, Nelson Thornes, Cheltenham (United Kingdom). 3rd edition.
56. Ho R.H., Kim R.B. Transporters and drug therapy: implications for drug disposition and disease. Clin Pharmacol Ther 2005, 78:260-277.
57. Pauli-Magnus C., Meier P.J. Hepatobiliary transporters and drug-induced cholestasis. Hepatology 2006, 44:778-787.
58. Pauli-Magnus C., Stieger B., Meier Y., et al. Enterohepatic transport of bile salts and genetics of cholestasis. J Hepatol 2005, 43:342-357.
59. Vavricka S.R., Van Montfoort J., Ha H.R., et al. Interactions of rifamycin SV and rifampicin with organic anion uptake systems of human liver. Hepatology 2002, 36:164-172.
60. Lakehal F., Dansette P.M., Becquemont L., et al. Indirect cytotoxicity of flucloxacillin toward human biliary epithelium via metabolite formation in hepatocytes. Chem Res Toxicol 2001, 14:694-701.
61. Iverson S.L., Uetrecht J.P. Identification of a reactive metabolite of terbinafine: insights into terbinafine-induced hepatotoxicity. Chem Res Toxicol 2001, 14:175-181.
62. Bolder U., Trang N.V., Hagey L.R., et al. Sulindac is excreted into bile by a canalicular bile salt pump and undergoes a cholehepatic circulation in rats. Gastroenterology 1999, 117:962-971.
63. Fattinger K., Funk C., Pantze M., et al. The endothelin antagonist bosentan inhibits the canalicular bile salt export pump: a potential mechanism for hepatic adverse reactions. Clin Pharmacol Ther 2001, 69:223-231.
64. +-dependent taurocholate cotransporting polypeptide (NTCP/SLC10A1) by bosentan: a mechanism for species differences in hepatotoxicity. J Pharmacol Exp Ther 2007, 321:1170-1178.
65. Lang C., Meier Y., Stieger B., et al. Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug-induced liver injury. Pharmacogenet Genomics 2007, 17:47-60.
66. Trauner M., Meier P.J., Boyer J.L. Molecular pathogenesis of cholestasis. N Engl J Med 1998, 339:1217-1227.
67. Biour M., Ben Salem C., Chazouilleres O., et al. Drug-induced liver injury; fourteenth updated edition of the bibliographic database of liver injuries and related drugs. Gastroenterol Clin Biol 2004, 28:720-759.
68. Chalasani N., Fontana R.J., Bonkovsky H.L., et al. Causes, clinical features, and outcomes from a prospective study of drug-induced liver injury in the United States. Gastroenterology 2008, 135:1924-1934. 1934.e1-4.
69. Björnsson E., Jerlstad P., Bergqvist A., et al. Fulminant drug-induced hepatic failure leading to death or liver transplantation in Sweden. Scand J Gastroenterol 2005, 40:1095-1101.
70. De Valle M.B., Av Klinteberg V., Alem N., et al. Drug-induced liver injury in a Swedish University hospital out-patient hepatology clinic. Aliment Pharmacol Ther 2006, 24:1187-1195.
71. Hussaini S.H., O'Brien C.S., Despott E.J., et al. Antibiotic therapy: a major cause of drug-induced jaundice in southwest England. Eur J Gastroenterol Hepatol 2007, 19:15-20.
72. Lucena M.I., Andrade R.J., Fernández M.C., et al. Determinants of the clinical expression of amoxicillin-clavulanate hepatotoxicity: a prospective series from Spain. Hepatology 2006, 44:850-856.
73. García Rodríguez L.A., Stricker B.H., Zimmerman H.J. Risk of acute liver injury associated with the combination of amoxicillin and clavulanic acid. Arch Intern Med 1996, 156:1327-1332.
74. Fontana R.J., Shakil A.O., Greenson J.K., et al. Acute liver failure due to amoxicillin and amoxicillin/clavulanate. Dig Dis Sci 2005, 50:1785-1790.
75. Turner I.B., Eckstein R.P., Riley J.W., et al. Prolonged hepatic cholestasis after flucloxacillin therapy. Med J Aust 1989, 151:701-705.
76. Fairley C.K., McNeil J.J., Desmond P., et al. Risk factors for development of flucloxacillin associated jaundice. BMJ 1993, 306:233-235.
77. Polson J.E. Hepatotoxicity due to antibiotics. Clin Liver Dis 2007, 11:549-561.
78. Andrade R.J., Guilarte J., Salmerón F.J., et al. Benzylpenicillin-induced prolonged cholestasis. Ann Pharmacother 2001, 35:783-784.
79. Brown B.A., Wallace R.J., Griffith D.E., et al. Clarithromycin-induced hepatotoxicity. Clin Infect Dis 1995, 20:1073-1074.
80. Lockwood A.M., Cole S., Rabinovich M. Azithromycin-induced liver injury. Am J Health Syst Pharm 2010, 67:810-814.
81. Mainra R.R., Card S.E. Trimethoprim-sulfamethoxazole-associated hepatotoxicity - part of a hypersensitivity syndrome. Can J Clin Pharmacol 2003, 10:175-178.
82. Anon Tetracycline hepatotoxicity. Br Med J 1964, 2(5424):1545-1546.
83. Björnsson E., Lindberg J., Olsson R. Liver reactions to oral low-dose tetracyclines. Scand J Gastroenterol 1997, 32:390-395.
84. Heaton P.C., Fenwick S.R., Brewer D.E. Association between tetracycline or doxycycline and hepatotoxicity: a population based case-control study. J Clin Pharm Ther 2007, 32:483-487.
85. Zapata Garrido A.J., Romo A.C., Padilla F.B. Terbinafine hepatotoxicity. A case report and review of literature. Ann Hepatol 2003, 2:47-51.
86. Agarwal K., Manas D.M., Hudson M. Terbinafine and fulminant hepatic failure. N Engl J Med 1999, 340:1292-1293.
87. Hautekeete M.L., Kockx M.M., Naegels S., et al. Cholestatic hepatitis related to quinolones: a report of two cases. J Hepatol 1995, 23:759-760.
88. Bataille L., Rahier J., Geubel A. Delayed and prolonged cholestatic hepatitis with ductopenia after long-term ciprofloxacin therapy for Crohn's disease. J Hepatol 2002, 37:696-699.
89. Skoog S.M., Smyrk T.C., Talwalkar J.A. Cephalexin-induced cholestatic hepatitis. J Clin Gastroenterol 2004, 38:833.
90. Alqahtani S., Hoofnagle J.H., Ghabril M., et al. Cephalosporin induced liver injury: clinical and biochemical features. Hepatology 2011, 54:516A.
91. Krebs S., Dormann H., Muth-Selbach U., et al. Risperidone-induced cholestatic hepatitis. Eur J Gastroenterol Hepatol 2001, 13:67-69.
92. Wright T.M., Vandenberg A.M. Risperidone- and quetiapine-induced cholestasis. Ann Pharmacother 2007, 41:1518-1523.
93. Vuppalanchi R., Hayashi P.H., Chalasani N., et al. Duloxetine hepatotoxicity: a case-series from the drug-induced liver injury network. Aliment Pharmacol Ther 2010, 32:1174-1183.
94. Romagnuolo J., Sadowski D.C., Lalor E., et al. Cholestatic hepatocellular injury with azathioprine: a case report and review of the mechanisms of hepatotoxicity. Can J Gastroenterol 1998, 12:479-483.
95. Ben Salem C., Ben Salah L., Belajouza C., et al. Azathioprine-induced severe cholestatic hepatitis in patient carrying TPMT*3C polymorphism. Pharm World Sci 2010, 32:701-703.
96. Roda G., Caponi A., Belluzzi A., et al. Severe cholestatic acute hepatitis following azathioprine therapy in a patient with ulcerative pancolitis. Dig Liver Dis 2009, 41:914-915.
97. Bastida G., Nos P., Aguas M., et al. Incidence, risk factors and clinical course of thiopurine-induced liver injury in patients with inflammatory bowel disease. Aliment Pharmacol Ther 2005, 22:775-782.
98. Gisbert J.P., González-Lama Y., Maté J. Thiopurine-induced liver injury in patients with inflammatory bowel disease: a systematic review. Am J Gastroenterol 2007, 102:1518-1527.
99. Aithal G.P. Diclofenac-induced liver injury: a paradigm of idiosyncratic drug toxicity. Expert Opin Drug Saf 2004, 3:519-523.
100. Watanabe N., Takashimizu S., Kojima S., et al. Clinical and pathological features of a prolonged type of acute intrahepatic cholestasis. Hepatol Res 2007, 37:598-607.
101. Hackstein H., Mohl W., Püschel W., et al. Z Gastroenterol 1998, 36:385-389. [in German].
102. Srivastava M., Perez-Atayde A., Jonas M.M. Drug-associated acute-onset vanishing bile duct and Stevens-Johnson syndromes in a child. Gastroenterology 1998, 115:743-746.
103. Levy C., Lindor K.D. Drug-induced cholestasis. Clin Liver Dis 2003, 7:311-330.
104. Servoss J.C., Kitch D.W., Andersen J.W., et al. Predictors of antiretroviral-related hepatotoxicity in the adult AIDS Clinical Trial Group (1989-1999). J Acquir Immune Defic Syndr 2006, 43:320-323.
105. Akhtar A.J., Shaheen M. Jaundice in African-American and Hispanic patients with AIDS. J Natl Med Assoc 2007, 99:825-829.
106. Björnsson E., Olsson R. Suspected drug-induced liver fatalities reported to the WHO database. Dig Liver Dis 2006, 38:33-38.
107. Schiano T.D., Kotler D.P., Ferran E., et al. Hepatoportal sclerosis as a cause of noncirrhotic portal hypertension in patients with HIV. Am J Gastroenterol 2007, 102:2536-2540.
108. Saifee S., Joelson D., Braude J., et al. Noncirrhotic portal hypertension in patients with human immunodeficiency virus-1 infection. Clin Gastroenterol Hepatol 2008, 6:1167-1169.
109. Kovari H., Ledergerber B., Peter U., et al. Association of noncirrhotic portal hypertension in HIV-infected persons and antiretroviral therapy with didanosine: a nested case-control study. Clin Infect Dis 2009, 49:626-635.
110. Cachay E.R., Peterson M.R., Goicoechea M., et al. Didanosine exposure and noncirrhotic portal hypertension in a HIV Clinic in North America: a follow-up study. Br J Med Med Res 2011, 1:346-355.
111. Dourakis S.P., Tolis G. Sex hormonal preparations and the liver. Eur J Contracept Reprod Health Care 1998, 3:7-16.
112. Lindgren A., Olsson R. Liver damage from low-dose oral contraceptives. J Intern Med 1993, 234:287-292.
113. Erlinger S. Drug-induced cholestasis. J Hepatol 1997, 26(Suppl 1):1-4.
114. Kafrouni M.I., Anders R.A., Verma S. Hepatotoxicity associated with dietary supplements containing anabolic steroids. Clin Gastroenterol Hepatol 2007, 5:809-812.
115. Navarro V.J. Herbal and dietary supplement hepatotoxicity. Semin Liver Dis 2009, 29:373-382.
116. Ibáñez L., Pérez E., Vidal X., et al. Prospective surveillance of acute serious liver disease unrelated to infectious, obstructive, or metabolic diseases: epidemiological and clinical features, and exposure to drugs. J Hepatol 2002, 37:592-600.
117. Andrade R.J., Lucena M.I., Kaplowitz N., et al. Outcome of acute idiosyncratic drug-induced liver injury: long-term follow-up in a hepatotoxicity registry. Hepatology 2006, 44:1581-1588.
118. Björnsson E., Kalaitzakis E., Av Klinteberg V., et al. Long-term follow-up of patients with mild to moderate drug-induced liver injury. Aliment Pharmacol Ther 2007, 26:79-85.
119. Bjornsson E., Davidsdottir L. The long-term follow-up after idiosyncratic drug-induced liver injury with jaundice. J Hepatol 2009, 50:511.