Hepatotoxicity by antibiotics: Update in 2008;Hepatotoxicidad por antibióticos: Actualización en 2008

Revista Espanola de Quimioterapia

Volumn 21, Issue 4, 2008, Pages 224-233

  Robles, M ^a   Andrade, Raúl J ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^b UNIVERSIDAD DE MÁLAGA   (Spain)

Author keywords

Age; Amoxicillin clavulanate; Antibiotics; Hepatotoxicity

Indexed keywords

AMOXICILLIN; AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; ANTIBIOTIC AGENT; AZITHROMYCIN; CEFTRIAXONE; CEPHALOSPORIN DERIVATIVE; CIPROFLOXACIN; CLARITHROMYCIN; CLINDAMYCIN; CLOXACILLIN; COTRIMOXAZOLE; DAPSONE; DAPTOMYCIN; DOXYCYCLINE; ERYTHROMYCIN; FANSIDAR; MACROLIDE; MINOCYCLINE; NITROFURANTOIN; NORFLOXACIN; PENICILLIN G; PENICILLIN V; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SALAZOSULFAPYRIDINE; SULFONAMIDE; TELITHROMYCIN; TETRACYCLINE DERIVATIVE; TROVAFLOXACIN; UNINDEXED DRUG;

ABDOMINAL PAIN; ARTICLE; ASCITES; AUTOIMMUNE HEPATITIS; CHOLELITHIASIS; CHOLESTASIS; DRUG FEVER; DRUG INDUCED DISEASE; DRUG MEGADOSE; DRUG USE; FATTY LIVER; HEPATITIS; HOSPITALIZATION; HUMAN; INCIDENCE; JAUNDICE; LIVER GRANULOMA; LIVER INJURY; LIVER TOXICITY; MICROVESICULAR STEATOSIS; MYOPATHY; PRESCRIPTION; RISK ASSESSMENT; SIDE EFFECT;

ANTI-BACTERIAL AGENTS; BETA-LACTAMS; HUMANS; LIVER DISEASES; MACROLIDES;

EID: 58149084885     PISSN: 02143429     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (112)

1. Lee WM, Senior J. Recognizing Drug-Induced Liver Injury: Current Problems, Possible Solutions. Toxicol Pathol 2005;33:155-64.
2. Sgro C, Clinard F, Ouazir K, Chanay H, Allard C, Guilleminet C, et al. Incidence of drug-induced hepatic injuries: a French population-based study. Hepatology 2002;36:451-5.
3. Andrade RJ, Lucena MI, Fernández MC, Pelaez G, Pachkoria K, García-Ruiz E, et al. Drug-Induced Liver Injury: An analysis of 461 incidences submitted to the Spanish Registry over a 10-year period. Gastroenterology 2005;129:512-21.
4. Chalasani N, Fontana R, Watkins PB; Drug induced liver injury network (DILIN). Prospective study: initial results. Am J Gastroenterol 2006;101:S168.
5. Hussaini SH, O'Brien CS, Despott EJ, Dalton HR. Antibiotic therapy: a major cause of drug-induced jaundice in southwest England. Eur J Gastroenterol Hepatol 2007;19:15-20.
6. Thiim M, Friedman LS. Hepatotoxicity of antibiotics and antifungals. Clin Liver Dis 2003;7:381-99.
7. Bénichou C. Report of an International Consensus Meeting. Criteria of drug-induced liver disorders. J Hepatol 1990;11:272-6.
8. Björnsson E, Olsson R. Outcome and prognostic markers in severe drug-induced liver disease. Hepatology 2005;42:481-489.
9. Andrade RJ, Lucena MI, Kaplowitz N, García-Muñoz B, Borraz Y, Pachkoria K, et al. Outcome of acute idiosyncratic drug-induced liver injury: Long-term follow-up in a hepatotoxicity registry. Hepatology 2006;44:1581-8.
10. Andrade RJ, Camargo R, Lucena MI, González-Grande R. Causality assessment in drug-induced hepatotoxicity. Expert Opin Drug Saf 2004;3:329-44.
11. Moseley RH. Sepsis and cholestasis. Clin Liver Dis 2004;8:83-94.
12. Parry MF. The penicillins. Med Clin North Am 1987;71:1093-112.
13. Goldstein LI, Ishak KG. Hepatic injury associated with penicillin therapy. Arch Pathol 1974;98:114-7.
14. Williams CN, Malatjalian DA. Severe penicillin-induced cholestasis in a 91-year-old woman. Dig Dis Sci 1981;26:470-3.
15. Onate J, Montejo M, Aguirrebengoa K, Ruiz-Irastorza G, Gonzalez de Zarate P, Aguirre C. Hepatotoxicity associated with penicillin V therapy. Gin Infect Dis 1995;20:474-5.
16. Andrade RJ, Guilarte J, Salmeron FJ, Lucena MI, Bellot V. Benzylpenicillin-induced prolonged cholestasis. Ann Pharmacother 2001;35:783-4.
17. Cavanzo FJ, Garcia CF, Botero RC. Chronic cholestasis, paucity of bile ducts, red cell aplasia, and the Stevens-Johnson syndrome: an ampicillin-associated case report. Gastroenterology 1990;99:854-6.
18. Koklu S, Yuksel O, Filik L, Uskudar O, Altundag K, Altiparmak E. Recurrent cholestasis due to ampicillin. Ann Pharmacother 2003;37:395-7.
19. Koklu S, Koksal AS, Asil M, Kiyici H, Coban S, Arhan M. Probable Sulbactam/ampicillin-associated prolonged cholestasis. Ann Pharmacother 2004;38:2055-8.
20. Davies MH, Harrison RF, Elias E, Hubscher SG. Antibiotic-associated acute vanishing bile duct syndrome: a pattern associated with severe, prolonged, intrahepatic cholestasis. J Hepatol 1994;20:112-6.
21. Garcia Rodriguez LA, Stricker BH, Zimmerman HJ. Risk of acute liver injury associated with the combination of amoxicillin and clavulanic acid. Arch Intern Med 1996;156:1327-32.
22. Konikoff F, Alcalay J, Halevy J. Cloxacillin-induced cholestatic jaundice. Am J Gastroenterol 1986;81:1082-3.
23. Lotric S, Lejko-Zupanc T, Jereb M. Cloxacillin-induced cholestasis. Clin Infect Dis 1994;19:981-2.
24. Turner IB, Eckstein RP, Riley JW, Lunzer MR. Prolonged hepatic cholestasis after flucloxacillin therapy. Med J Aust 1989;151:701-5.
25. Fairley CK, McNeil JJ, Desmond P, Smallwood R, Young H, Forbes A, et al. Risk factors for development of flucloxacillin associated jaundiced. BMJ 1993;306:233-5.
26. Anderka D, Livni E, Salamon F, Weinberger A, Pinkhas J. Use of macrophage inhibition factor and mast-cell degranulation test for diagnosis of cloxacillin induced-cholestasis. Am J Gastroenterol 1986;81:1084-6.
27. Horikawa M, Kato Y, Tyson CA, Sugiyama Y. Potential cholestasis activity of various therapeutic agents assessed by bile canalicular membrane vesicles isolated from rats and humans. Drug Metab Pharmacokinet 2003;18:16-22.
28. Dowsett JF, Gillow T, Heagerty A, Radcliffe M, Toadi R, Isle I, et al. Amoxicillin/clavulanic acid (Augmentin)-induced intrahepatic cholestasis. Dig Dis Sci 1989;34:1290-3.
29. Stricker BH, Van den Broek JW, Keuning J, Eberhardt W, Houben HG, Johnson M, et al. Cholestatic hepatitis due to antibacterial combination of amoxicillin and clavulanic acid (augmentin). Dig Dis Sci 1989;34:1576-80.
30. Reddy KR, Brillant P, Schiff ER. Amoxicillin-clavulanate potassium-associated cholestasis. Gastroenterology 1989;96: 1135-41.
31. Lucena MI, Andrade RJ, Fernandez MC, Pachkoria K, Pelaez G, Duran JA, et al. Determinants of the clinical expression of amoxicillin-clavulanate hepatotoxicity: a prospective series from Spain. Hepatology 2006;44:850-6.
32. O'Donohue JA, Oien KA, Donaldson P, Underhill J, Clare M, MacSween RNM, et al. Co-amoxiclav jaundice: clinical and histological features and HLA class II association. Gut 2000; 47:717-720.
33. Larrey D, Vial T, Micaleff A, Babany G, Morichau-Beauchant M, Michel H, et al. Hepatitis associated with amoxycillin-clavulanic acid combination report of 15 cases. Gut 1992;33:368-71.
34. Silvain C, Fort E, Levillain P, Labat-Labourdette J, Beauchant M. Granulomatous hepatitis due to combination of amoxicillin and calvulanic acid. Dig Dis Sci 1992;37:150-2.
35. Cundiff J, Joe S. Amoxicillin-clavulanic acid-induced hepatitis. Am J Otolaryngol 2007;28:28-30.
36. Hautekeete ML, Horsmans Y, Van Waeyenberge C, Demanet C, Henrion J, Verbist L, et al. HLA association of amoxicillin-clavulanate-induced hepatitis. Gastroenterology 1999;117:1181-6.
37. Chawla A, Kahn E Yunis EJ, Daum F. Rapidly progressive cholestasis. An inusual reaction to amoxicillin/clavulanic acid therapy in a child. J Pediatr 2000;136:121-3.
38. Smith LA, Ignacio JR, Winesett MP, Kaiser GC, Lacson AG, Gilbert-Barness E, et al. Vanishing bile duct syndrome: amoxicillin-clavulanic acid associated intrahepatic cholestasis responsive to ursodeoxycholic acid. J Pediatr Gastroenterol Nutr 2005;41:469-73.
39. Katsinelos P, Vasiliadis T, Xiarchos P, Patakiouta F, Christodoulou K, Pilpilidis I, et al. Ursodeoxycholic acid (UDCA) for the treatment of amoxicillin-clavulanate potassium (Augmentin)-induced intrahepatic cholestasis: report of two cases. Eur J Gastroenterol Hepatol 2000;12:365-8.
40. Ryley NG, Fleming KA, Chapman RW. Focal destructive cholangiopathy associated with amoxicillin/clavulanic acid (Augmentin). J Hepatol 1995;23:278-82.
41. Nathani MG, Mutchnick MG, Tynes DJ, Ehrinpreis MN. An unusual case of amoxicillin/clavulanic acid-related hepatotoxicity. Am J Gastroenterol 1998;93:1363-5.
42. Andrade RJ, Lucena MI, Alonso A, García-Cortes M, García-Ruiz E, Benitez R, et al. HLA class II genotype influences the type of liver injury in drug-induced idiosyncratic liver disease. Hepatology 2004;39:1603-12.
43. Ammann R, Neftel K, Hardmeier T, Reinhardt M. Cephalosporin-induced cholestasis jaundice. Lancet 1982;2:336-7.
44. Skoog SM, Smyrk TC, Talwalkar JA. Cephalexin-induced cholestasis hepatitis. J Clin Gastroenterol 2004;38:833.
45. Eggleston SM, Belandres MM. Jaundice associated with cephalosporin therapy. Drug Intell Clin Pharm 1985;19:553-5.
46. Derby LE, Jick H, Henry DA, Dean AD. Erythromycin-associated cholestatic hepatitis. Med J Aust 1993;158:600-2.
47. Carson JL, Strom BL, Duff A, Gupta A, Shaw M, Lundin FE, et al. Acute liver disease associated with erythromycins, sulfonamides and tetracyclines. Ann Intern Med 1993;119:576-83.
48. Zafrani ES, Ishak KG, Rudeki C. Cholestatic and hepatocellular injury associated with erythromycin esters. Dig Dis 1979;24: 385-96.
49. Degott C, Feldmann G, Larrey D. Drug-induced prolonged cholestasis in adults: a histoligical semiquantitative study demonstrating progressive ductopenia. Hepatology 1992;15:244-51.
50. Gaholson CF, Warren GH. Fulminant hepatic failure associated with intravenosus erythromycin lactobianate. Arch Intern Med 1990;150:215-6.
51. Lazarczyk DA, Duffy MC. Erythroycin-induced primary biliary cirrhosis. Dig Dis Sci 2000;45:1115-8.
52. Cascaval RI, Lancaster DJ. Hypersensitivity syndrome associated with azithromycin. [letter] Am J Med 2001;110:330-1.
53. Chandrupatla S, Demetrio AJ, Rabinovitz M. Azithromycin-induced intrahepatic cholestasis. Dig Dis Sci 2002;47:2186-8.
54. Yew WW, Chau CH, Lee J, Leung CW. Cholestatic hepatitis in a patient who received clarithromycin therapy for a Mycobacterium chelonae lung infection. [letter] Clin Infect Dis 1994;18:1025-6.
55. Fox JC, Szyjkowski RS, Sanderson SO Levine RA. Progressive cholestasis liver disease associated with clarithromycin treatment. J Clin Pharmacol 2002;42:676-80.
56. Masiá M, Gutiérrez F, Jimeno A, Navarro A, Borrás J, Matarredona J, et al. Fulminant hepatitis and fatal toxic epidermal necrolysis (Lyell disease) coincident with clarithromycin administration in an alcoholic patient receiving disulfiram therapy. Arch Intern Med 2002;162:474-6.
57. Nguyen M, Chung EP. Telithromycin: the first ketolide antimicrobial. Clin Ther 2005;27:1144-63.
58. Clay KD, Hanson JS, Pope SD, Rissmiller RW, Purdum PP III, Banks PM. Brief communication: severe hepatotoxicity of telithromycin: three case reports and literature review. Ann Intern Med 2006;144:415-20.
59. Onur O, Guneysel O, Denizbasi A, Celikel C. Acute hepatitis attack after exposure to telithromycin. Clin Therap 2007:29: 1725-29.
60. Bolesta S, Roslund BP. Elevated hepatic transaminases associated with telithromycin therapy: a case report and literature review. Am J Health-Syst Pharm 2008;65:37-41.
61. Brinker A, Wassel R, Lyndly J, Serrano J, Avigan M, Lee WM, et al. Telithromycin-associated hepatotoxicity: clinical spectrum and causality assessment of 42 cases. Hepatology 2008; in press.
62. Pessayre D, Larrey D, Funck-Brentano C, Benhamou JP. Drug interactions and hepatitis produced by some macrolide antibiotics. Antimicrob Chemother 1985;16(Suppl A):181-94.
63. Dujovne CA, Chan CH, Zimmerman HJ. Sulfonamide hepatic injury: Review of the literature and report of a case due to sulfamethoxazole. N Engl J Med 1967;277:785-8.
64. Gordin FM, Simon GL, Wofsy CB, Mills J. Adverse reactions to trimethoprim-sulfamethoxazole in patients with the acquired immunodeficiency syndrome. Ann Intern Med 1984;100:495-9.
65. Espiritu CR, Kim TS, Levine RA. Granulomatous hepatitis associated with sulfadimethoxine hypersensitivity. JAMA 1967; 202:985-8.
66. Lazar HP, Murphy RL, Phair JP. Fansidar and hepatic granulomas. [letter] Ann Intern Med 1985;102:722.
67. Alberti-Flor JJ, Hernandez ME, Ferrer JP, Howell S, Jeffers L. Fulminant liver failure and pancreatitis associated with the use of sulfamethoxazole-trimethoprim. Am J Gastroenterol 1989;84: 1577-9.
68. Ransohoff DF, Jacobs G. Terminal hepatic failure following a small dose of sulfamethoxazoletrimethoprim. Gastroenterology 1981;80:816-9.
69. Altraif I, Lilly L, Wanless IR, Heathcote J. Cholestatic liver disease with ductopenia (vanishing bile duct syndrome) after administration of clindamycin and trimethoprim-sulfamethoxazole. Am J Gastroenterol 1994;89:1230-4.
70. Yao F, Behling CA, Saab S, Hatr M, Lyche KD. Trimethoprim-sulfamethoxazole-induced vanishing bile duet syndrome. Am J Gastroenterol 1997;92:167-9.
71. Zitelli BJ, Alexander J, Taylor S, Miller KD, Howrie DL, Kuritsky JN, et al. Fatal hepatic necrosis due to pyrimethamine-sulfadoxine (Fansidar). Ann Intern Med 1987;106:393-5.
72. Konttinen A, Perasalo JO, Eisalo A. Sulfonamide hepatitis. Acta Med Scan 1972;191:389-91.
73. Wolkenstein P, Carrière V, Charue D, Bastuji-Garin S, Revuz J, Roujeau JC, et al. A slow acetylador genotype is a risk factor for sulphonamide-induced toxic epidermal necrolysis and Stevens-Johnson syndrome. Pharmacogenetics 1995;5:255-8.
74. Alfirevic A, Stalford AC, Vilar FJ, Wilkins EG, Park BK, Pirmohamed M. Slow acetylador phenotype and genotype in HIV-positive patients with sulphamethoxazol hypersensitivity. Br J Clin Pharmacol 2003;55:158-65.
75. Zimmerman HJ. Hepatotoxicity: The Adverse Effects of Drugs and Other Chemicals on the Liver. 2nd ed. Philadelphia: Lippincott Williams and Wilkins, 1999.
76. Whalley PJ, Adams RH, Combes B. Tetracycline toxicity in pregnancy. JAMA 1964;189:357-62.
77. Bjornsson E, Lindberg J, Olsson R. Liver reactions to oral low-dose tetracyclines. Scand J Gastroenterol 1997;32:390-5.
78. Fréneaux E, Labbe G, Letteron P, The Le Dinh, Degott C, Genève J, et al. Inhibition of the mitrochondrial oxidation of fatty acids by tetracycline in mice and in man: Possible role in microvesicular steatosis induced by this antibiotic. Hepatology 1988;8: 1056-62.
79. Westermann GW, Bohm M, Bonsmann G, Rahn KH, Kisters K. Chronic intoxication by doxycycline use for more than 12 years. J Intern Med 1999;246:591-2.
80. Gough A, Chapman S, Wagstaff K, Emery P, Elias E. Minocycline induced autoimmune hepatitis and systemic lupus erythematosus-like syndrome. BJM 1996;312:169-72.
81. Lawrenson RA, Seaman HE, Sundstrom A, Williams TJ, Farmer RD. Liver damage associated with minocycline use in acne: a systematic review of the published literature and pharmacovigilance data. Drug Staf 2000;23:333-49.
82. Knowles SR, Shapiro L, Shear NH. Serious adverse reactions induced by minocycline. Report of 13 patients and review of the literature. Arch Dermatol 1996;132:934-9.
83. Liu ZX, Kaplowitz N. Immuned-mediated drug-induced liver disease. Clin Liver Dis 2002;6:755-74.
84. Heaton PC, Fenwick SR, Brewer DE. Association between tetracycline or doxycycline and hepatotoxicity: a population based case-control study. J Clin Pharm Ther 2007;32:483-7.
85. Owen RC, Jr., Ambrose PG. Antimicrobial safety: focus on fluoroquinolones. Clin Infect Dis 2005;41(Suppl.2):S144-57.
86. Lopez-Navidad A, Domingo P, Cadafalch J, Farrerons J. Norfloxacin-induced hepatotoxicity. J Hepatol 1990;11:277-8.
87. Hautekeete ML, Kockx MM, Naegels S, Holvoet JK, Hubens H, Kloppel G. Cholestatic hepatitis related to quinolones: a report of two cases. J Hepatol 1995;23:759-60.
88. Lucena MI, Andrade RJ, Sánchez-Martínez H, Pérez-Serrano JM, Gómez-Outes A. Norfloxacin induced cholestatic jaundice. Am J Gastroenterol 1998;93:2309-11.
89. 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;37:696-9.
90. Grassmick BK, Lehr VT, Sundareson AS. Fulminant hepatic failure possibly related to ciprofloxacin. Ann Pharmacother 1992; 26:636-9.
91. Zimpfer A, Propst A, Mikuz G, Vogel W, Terracciano L, Stadlmann S. Ciprofloxacin-induced acute liver injury: case report and review of the literature. Virchows Arch 2004;444:87-9.
92. Bertino J, Jr., Fish D, Bertino J, Fish D. The safety profile of the fluoroquinolones. Clin Ther 2000;22:798-817.
93. Lucena MI, Andrade RJ, Rodrigo L, Salmerón J, Álvarez A, López-Garrido MJ, et al. Trovafloxacin-induced acute hepatitis. Clin Infect Dis 2000;30:401-2.
94. Coban S, Ceydilek B, Ekiz F, Erden E, Soykan I. Levofloxacin-induced acute fulminant hepatic failure in a patient with chronic hepatitis B infection. Ann Pharmacother 2005;39:1737-40.
95. Soto S, López-Rosés L, Avila S, Lancho A, González A, Santos E, Urraca B. Moxifloxacin-induced acute liver injury. Am J Gastroenterol 2002;97:1853-4.
96. D'Arcy PF. Nitrofurantoin. Drug Intell Clin Pharm 1985;19:540-7.
97. Goldstein LI, Ishak KG, Burns W. Hepatic injury associated with nitrofurantoin therapy. Am J Dig Dis 1974;19:987-98.
98. Black M, Rabin L, Schatz N. Nitrofurantoin-induced chronic active hepatitis. Ann Intern Med 1980;92:62-4.
99. Klemola H, Penttila O, Runeberg L, Tallqvist G. Anicteric liver damage during nitrofurantoin medication. Scand J Gastroenterol 1975;10:501-5.
100. Sharp JR, Ishak KG, Zimmerman HJ. Chronic active hepatitis and severe hepatic necrosis associated with nitrofurantoin. Ann Intern Med 1980;92:14-9.
101. Stricker BH, Blok AP, Claas FH, Van Parys GE, Desmet VJ. Hepatic injury associated with the use of nitrofurantoins:A clinicopathological study of 52 reported cases. Hepatology 1988;8:599-606.
102. Sippel PJ, Agger WA. Nitrofurantoin-induced granulomatous hepatitis. Urology 1981;18:177-8.
103. Holmberg L, Boman G, Bottiger LE, Eriksson B, Spross R, Wessling A. Adverse reactions to nitrofurantoin. Analysi of 921 reports. Am J Med 1980;69:733-8.
104. Paiva LA, Wright PJ, Koff RS. Long-term hepatic memory for hypersensitivity to nitrofurantoin. Am J Gastroenterol 1992;87:891-3.
105. Engel JJ Vogt TR, Wilson DE. Cholestasis hepatitis after administration of furan derivatives. Arch Intern Med 1975;135:733-5.
106. Elmore M, Rissing JP, Rink L, Brooks GF. Clindamycin-associated hepatotoxicity. Am J Med 1974;57:627-30.
107. Arbeit RD, Maki D, Tally FP, Campanaro E, Eisenstein BI, Daptomycin 98-01 and 99-01 Investigators. The safety and efficacy of daptomycin for the treatment of complicated skin and skin-structure infections. Clin Infect Dis 2004;38:1673-81.
108. Echevarria K, Datta P, Cadena J, Lewis JS. Severe Myopathy and possible hepatotoxicity related to daptomycin. J Antimicrob Chemother 2005;55:599-600.
109. de Abajo FJ, Montero D, Madurga M, García Rodríguez LA. Acute and clinically relevant drug-induced liver injury: a population based case-control study. Br J Clin Pharmacol 2004;58:71-80.
110. Russo MW, Galanko JA, Shrestha R, Fried MW, Watkins P. Liver transplantation for acute liver failure from drug induced liver injury in the United States. Liver Transpl 2004;10:1018-23.
111. Galan MV, Potts JA, Silverman AL, Gordon SC. The burden of acute nonfulminant drug-induced hepatitis in a United States tertiary referral center [corrected]. J Clin Gastroenterol 2005; 39:64-7.
112. De Valle MB, Av Klinteberg V, Alem N, Olsson R, Björnsson E. Drug-induced liver injury in a Swedish University hospital out-patient hepatology clinic. Aliment Pharmacol Ther 2006;24: 1187-95.