Autoimmune-like drug-induced liver injury: a review and update for the clinician

References

• Reuben A, Koch DG, Lee WM. Drug-induced acute liver failure: results of a U.S. multicenter, prospective study. Hepatology. 2010;52(6):2065–2076.
   PubMed Web of Science ®Google Scholar
• Bjornsson 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(9):1095–1101.
   PubMed Web of Science ®Google Scholar
• Chalasani N, Fontana RJ, Bonkovsky HL, et al. Causes, clinical features, and outcomes from a prospective study of drug-induced liver injury in the United States. Gastroenterology. 2008;135(6):1924–1934. 1934.e1921–e1924
   PubMed Web of Science ®Google Scholar
• Stine JG, Lewis JH. Drug-induced liver injury: a summary of recent advances. Expert Opin Drug Metab Toxicol. 2011;7(7):875–890.
   PubMed Web of Science ®Google Scholar
• Andrade RJ, Lucena MI, Fernandez MC, et al. 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.
   PubMed Web of Science ®Google Scholar
• Chalasani NP, Hayashi PH, Bonkovsky HL, et al. ACG Clinical Guideline: the diagnosis and management of idiosyncratic drug-induced liver injury. Am J Gastroenterol. 2014;109(7):950–966. quiz 967
   PubMed Web of Science ®Google Scholar
• Stine JG, Chalasani N. Chronic liver injury induced by drugs: a systematic review. Liver Int. 2015;35(11):2343–2353. doi:10.1111/liv.12958. Epub 2015 Sep 27.
   PubMed Web of Science ®Google Scholar
• Fontana RJ, Hayashi PH, Gu J, et al. Idiosyncratic drug-induced liver injury is associated with substantial morbidity and mortality within 6 months from onset. Gastroenterology. 2014;147(1):96–108. e104
   PubMed Web of Science ®Google Scholar
• Czaja AJ. Drug-induced autoimmune-like hepatitis. Dig Dis Sci. 2011;56(4):958–976.
   PubMed Web of Science ®Google Scholar
• Castiella A, Zapata E, Lucena MI, et al. Drug-induced autoimmune liver disease: a diagnostic dilemma of an increasingly reported disease. World J Hepatol. 2014;6(4):160–168.
   PubMedGoogle Scholar
• Zimmerman HJ. Hepatotoxicity: the adverse effects of drugs and other chemicals on the liver. Philadelphia: Lippincott-Williams & Wilkins; 1999.
   Google Scholar
• Shoenfeld Y, Vilner Y, Reshef T, et al. Increased presence of common systemic lupus erythematosus (SLE) anti-DNA idiotypes (16/6 Id, 32/15 Id) is induced by procainamide. J Clin Immunol. 1987;7(5):410–419.
   PubMed Web of Science ®Google Scholar
• Bjornsson E, Talwalkar J, Treeprasertsuk S, et al. Drug-induced autoimmune hepatitis: clinical characteristics and prognosis. Hepatology. 2010;51(6):2040–2048.
   PubMed Web of Science ®Google Scholar
• Hisamochi A, Kage M, Ide T, et al. An analysis of drug-induced liver injury, which showed histological findings similar to autoimmune hepatitis. J Gastroenterol. 2016;51(6):597–607. doi:10.1007/s00535-015-1131-7. Epub 2015 Oct 30.
   PubMed Web of Science ®Google Scholar
• Stine JG, Lewis JH. Current and future directions in the treatment and prevention of drug-induced liver injury: a systematic review. Expert Rev Gastroenterol Hepatol. 2016;10(4):517–536. doi:10.1586/17474124.2016.1127756. Epub 2015 Dec 25.
   PubMed Web of Science ®Google Scholar
• Stine JG, Intagliata N, Shah NL, et al. Hepatic decompensation likely attributable to simeprevir in patients with advanced cirrhosis. Dig Dis Sci. 2015;60(4):1031–1035. Epub 12014 Nov 10626. doi:10.1007/s10620-10014-13422-x.
   PubMed Web of Science ®Google Scholar
• Agarwal VK, McHutchison JG, Hoofnagle JH. Important elements for the diagnosis of drug-induced liver injury. Clin Gastroenterol Hepatol. 2010;8(5):463–470.
   PubMed Web of Science ®Google Scholar
• Aithal GP, Watkins PB, Andrade RJ, et al. Case definition and phenotype standardization in drug-induced liver injury. Clin Pharmacol Ther. 2011;89(6):806–815.
   PubMed Web of Science ®Google Scholar
• Liu ZX, Kaplowitz N. Immune-mediated drug-induced liver disease. Clin Liver Dis. 2002;6(3):755–774.
   PubMedGoogle Scholar
• Hoofnagle JH. Drug-induced liver injury network (DILIN). Hepatology. 2004;40(4):773.
   PubMedGoogle Scholar
• Hoofnagle JH, Serrano J, Knoben JE, et al. LiverTox: a website on drug-induced liver injury. Hepatology. 2013;57(3):873–874.
   PubMed Web of Science ®Google Scholar
• Hoofnagle JH. [cited 2016 Apr 20]. Available from: http://livertox.nih.gov/Phenotypes_auto.html.
   Google Scholar
• Homberg JC, Andre C, Abuaf N. A new anti-liver-kidney microsome antibody (anti-LKM2) in tienilic acid-induced hepatitis. Clin Exp Immunol. 1984;55(3):561–570.
   PubMed Web of Science ®Google Scholar
• Beaune PH, Lecoeur S, Bourdi M, et al. Anti-cytochrome P450 autoantibodies in drug-induced disease. Eur J Haematol Suppl. 1996;60:89–92.
   PubMedGoogle Scholar
• Lecoeur S, Andre C, Beaune PH. Tienilic acid-induced autoimmune hepatitis: anti-liver and-kidney microsomal type 2 autoantibodies recognize a three-site conformational epitope on cytochrome P4502C9. Mol Pharmacol. 1996;50(2):326–333.
   PubMed Web of Science ®Google Scholar
• Bourdi M, Gautier JC, Mircheva J, et al. Anti-liver microsomes autoantibodies and dihydralazine-induced hepatitis: specificity of autoantibodies and inductive capacity of the drug. Mol Pharmacol. 1992;42(2):280–285.
   PubMed Web of Science ®Google Scholar
• Ravi S, Shoreibah M, Raff E, et al. Autoimmune markers do not impact clinical presentation or natural history of steatohepatitis-related liver disease. Dig Dis Sci. 2015;60(12):3788–3793.
   PubMed Web of Science ®Google Scholar
• Tsuneyama K, Baba H, Kikuchi K, et al. Autoimmune features in metabolic liver disease: a single-center experience and review of the literature. Clin Rev Allergy Immunol. 2013;45(1):143–148.
   PubMed Web of Science ®Google Scholar
• Vuppalanchi R, Gould RJ, Wilson LA, et al. Clinical significance of serum autoantibodies in patients with NAFLD: results from the nonalcoholic steatohepatitis clinical research network. Hepatol Int. 2012;6(1):379–385.
   PubMed Web of Science ®Google Scholar
• Suzuki A, Brunt EM, Kleiner DE, et al. The use of liver biopsy evaluation in discrimination of idiopathic autoimmune hepatitis versus drug-induced liver injury. Hepatology. 2011;54(3):931–939.
   PubMed Web of Science ®Google Scholar
• Manns MP, Czaja AJ, Gorham JD, et al. Diagnosis and management of autoimmune hepatitis. Hepatology. 2010;51(6):2193–2213. doi:10.1002/hep.23584.
   PubMed Web of Science ®Google Scholar
• Kuzu UB, Oztas E, Turhan N, et al. Clinical and histological features of idiosyncratic liver injury: dilemma in diagnosis of autoimmune hepatitis. Hepatol Res. 2016;46(4):277–291. doi:10.1111/hepr.12530. Epub 2015 May 21.
   PubMed Web of Science ®Google Scholar
• European Association for the Study of the Liver. EASL clinical practice guidelines: autoimmune hepatitis. J Hepatol. 2015; 63(4): 971–1004.
   PubMed Web of Science ®Google Scholar
• Chalasani N, Bjornsson E. Risk factors for idiosyncratic drug-induced liver injury. Gastroenterology. 2010;138(7):2246–2259.
   PubMed Web of Science ®Google Scholar
• Pande JN, Singh SP, Khilnani GC, et al. Risk factors for hepatotoxicity from antituberculosis drugs: a case-control study. Thorax. 1996;51(2):132–136.
   PubMed Web of Science ®Google Scholar
• Bjornsson E, Davidsdottir L. The long-term follow-up after idiosyncratic drug-induced liver injury with jaundice. J Hepatol. 2009;50(3):511–517.
   PubMed Web of Science ®Google Scholar
• Stine JG, Sateesh P, Lewis JH. Drug-induced liver injury in the elderly. Curr Gastroenterol Rep. 2013;15(1):299.
   PubMedGoogle Scholar
• Cotreau MM, Von Moltke LL, Greenblatt DJ. The influence of age and sex on the clearance of cytochrome P450 3A substrates. Clin Pharmacokinet. 2005;44(1):33–60.
   PubMed Web of Science ®Google Scholar
• Voskuhl R. Sex differences in autoimmune diseases. Biol Sex Differ. 2011;2(1):1.
   PubMedGoogle Scholar
• Lindberg J, Lindholm A, Iwarson S. Genetic factors in the development of chronic active hepatitis. Lancet. 1977;1(8002):67–68.
   PubMed Web of Science ®Google Scholar
• Lucena MI, 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(4):820–827. Epub 2011 Feb 1019. 10.1016/j.jhep.2010.12.041.
   PubMed Web of Science ®Google Scholar
• Podymow T, August P. Hypertension in pregnancy. Adv Chronic Kidney Dis. 2007;14(2):178–190.
   PubMed Web of Science ®Google Scholar
• Goldstein GB, Lam KC, Mistilis SP. Drug-induced active chronic hepatitis. Am J Dig Dis. 1973;18(3):177–184.
   PubMedGoogle Scholar
• Toghill PJ, Smith PG, Benton P, et al. Methyldopa liver damage. Br Med J. 1974;3(5930):545–548.
   PubMed Web of Science ®Google Scholar
• Sotaniemi EA, Hokkanen OT, Ahokas JT, et al. Hepatic injury and drug metabolism in patients with alpha-methyldopa-induced liver damage. Eur J Clin Pharmacol. 1977;12(6):429–435.
   PubMed Web of Science ®Google Scholar
• Arranto AJ, Sotaniemi EA. Morphologic alterations in patients with alpha-methyldopa-induced liver damage after short- and long-term exposure. Scand J Gastroenterol. 1981;16(7):853–863.
   PubMed Web of Science ®Google Scholar
• Beaugrand M, Gavillon C, Ferrier JP. [High levels of endoplasmic reticulum antibody titer in a case of alpha-methyldopa-induced chronic active hepatitis (author’s transl)]. Gastroenterol Clin Biol. 1980;4(3):219–221.
   PubMedGoogle Scholar
• Lee WM, Denton WT. Chronic hepatitis and indolent cirrhosis due to methyldopa: the bottom of the iceberg? J S C Med Assoc. 1989;85(2):75–79.
   PubMedGoogle Scholar
• Arranto AJ, Sotaniemi EA. Histologic follow-up of alpha-methyldopa-induced liver injury. Scand J Gastroenterol. 1981;16(7):865–872.
   PubMed Web of Science ®Google Scholar
• Roberts WC. Safety of fenofibrate – US and worldwide experience. Cardiology. 1989;76(3):169–179.
   PubMed Web of Science ®Google Scholar
• Dumortier J, Slim R, Chevallier M, et al. [Acute severe fibrosing hepatitis associated with ciprofibrate treatment]. Gastroenterol Clin Biol. 1999;23(12):1399–1400.
   PubMedGoogle Scholar
• Chatrenet P, Regimbeau C, Ramain JP, et al. [Chronic active cirrhogenic hepatitis induced by fenofibrate]. Gastroenterol Clin Biol. 1993;17(8–9):612–613.
   PubMedGoogle Scholar
• Bernard PH, Lamouliatte H, Le Bail B, et al. [Chronic active hepatitis associated with antinuclear antibodies induced by fenofibrate]. Gastroenterol Clin Biol. 1994;18(11):1048–1049.
   PubMedGoogle Scholar
• Parra JL, Reddy KR. Hepatotoxicity of hypolipidemic drugs. Clin Liver Dis. 2003;7(2):415–433.
   PubMedGoogle Scholar
• Couzigou P, Boutillier P, Boisseau C, et al. [Drug-induced hepatitis due to fenofibrate]. Therapie. 1980;35(3):403.
   PubMed Web of Science ®Google Scholar
• FDA Drug Safety Communication: Important safety label changes to cholesterol-lowering statin drugs [Internet; cited 2016 Mar 21]. Available from: www.fda.gov/Drugs/DrugSafety/ucm293101.htm
   Google Scholar
• Lewis JH. Clinical perspective: statins and the liver – harmful or helpful? Dig Dis Sci. 2012;57(7):1754–1763.
   PubMed Web of Science ®Google Scholar
• Funatsu T, Kakuta H, Takasu T, et al. Experimental model of postprandial hypertriglyceridemia in sucrose-fed rats and the effectiveness of atorvastatin in the model. Metabolism. 2003;52(5):609–615.
   PubMed Web of Science ®Google Scholar
• Pelli N, Setti M, Ceppa P, et al. Autoimmune hepatitis revealed by atorvastatin. Eur J Gastroenterol Hepatol. 2003;15(8):921–924.
   PubMed Web of Science ®Google Scholar
• Alla V, Abraham J, Siddiqui J, et al. Autoimmune hepatitis triggered by statins. J Clin Gastroenterol. 2006;40(8):757–761.
   PubMed Web of Science ®Google Scholar
• Russo MW, Hoofnagle JH, Gu J, et al. Spectrum of statin hepatotoxicity: experience of the drug-induced liver injury network. Hepatology. 2014;60(2):679–686.
   PubMed Web of Science ®Google Scholar
• van Heyningen C. Drug-induced acute autoimmune hepatitis during combination therapy with atorvastatin and ezetimibe. Ann Clin Biochem. 2005;42(Pt 5):402–404.
   PubMed Web of Science ®Google Scholar
• Wolters LM, Van Buuren HR. Rosuvastatin-associated hepatitis with autoimmune features. Eur J Gastroenterol Hepatol. 2005;17(5):589–590.
   PubMed Web of Science ®Google Scholar
• Kasliwal R, Wilton LV, Cornelius V, et al. Safety profile of rosuvastatin: results of a prescription-event monitoring study of 11,680 patients. Drug Safety. 2007;30(2):157–170.
   PubMed Web of Science ®Google Scholar
• Punthakee Z, Scully LJ, Guindi MM, et al. Liver fibrosis attributed to lipid lowering medications: two cases. J Intern Med. 2001;250(3):249–254.
   PubMed Web of Science ®Google Scholar
• Mansilla-Tinoco R, Harland SJ, Ryan PJ, et al. Hydralazine, antinuclear antibodies, and the lupus syndrome. Br Med J (Clin Res Ed). 1982;284(6320):936–939.
   PubMed Web of Science ®Google Scholar
• Belloc C, Gauffre A, Andre C, et al. Epitope mapping of human CYP1A2 in dihydralazine-induced autoimmune hepatitis. Pharmacogenetics. 1997;7(3):181–186.
   PubMedGoogle Scholar
• Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723.
   PubMed Web of Science ®Google Scholar
• Kahler KC, Hauschild A. Treatment and side effect management of CTLA-4 antibody therapy in metastatic melanoma. J Dtsch Dermatol Ges. 2011;9(4):277–286.
   PubMed Web of Science ®Google Scholar
• Cheng R, Cooper A, Kench J, et al. Ipilimumab-induced toxicities and the gastroenterologist. J Gastroenterol Hepatol. 2015;30(4):657–666.
   PubMed Web of Science ®Google Scholar
• Kleiner DE, Berman D. Pathologic changes in ipilimumab-related hepatitis in patients with metastatic melanoma. Dig Dis Sci. 2012;57(8):2233–2240.
   PubMed Web of Science ®Google Scholar
• Weber JS, Kahler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30(21):2691–2697.
   PubMed Web of Science ®Google Scholar
• Ahmed T, Pandey R, Shah B, et al. Resolution of ipilimumab induced severe hepatotoxicity with triple immunosuppressants therapy. BMJ Case Rep. 2015;2015: pii:bcr2014208102. doi:10.1136/bcr-2014-208102.
   Google Scholar
• Chmiel KD, Suan D, Liddle C, et al. Resolution of severe ipilimumab-induced hepatitis after antithymocyte globulin therapy. J Clin Oncol. 2011;29(9):e237–240.
   PubMed Web of Science ®Google Scholar
• 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(8):934–939.
   PubMed Web of Science ®Google Scholar
• Gleckman R, Alvarez S, Joubert DW. Drug therapy reviews: nitrofurantoin. Am J Hosp Pharm. 1979;36(3):342–351.
   PubMedGoogle Scholar
• Sharp JR, Ishak KG, Zimmerman HJ. Chronic active hepatitis and severe hepatic necrosis associated with nitrofurantoin. Ann Intern Med. 1980;92(1):14–19.
   PubMed Web of Science ®Google Scholar
• Amit G, Cohen P, Ackerman Z. Nitrofurantoin-induced chronic active hepatitis. Isr Med Assoc J. 2002;4(3):184–186.
   PubMed Web of Science ®Google Scholar
• Sippel PJ, Agger WA. Nitrofurantoin-induced granulomatous hepatitis. Urology. 1981;18(2):177–178.
   PubMed Web of Science ®Google Scholar
• Stine JG, Lewis JH. Hepatotoxicity of antibiotics: a review and update for the clinician. Clin Liver Dis. 2013;17(4):609–642, ix.
   PubMed Web of Science ®Google Scholar
• Strohscheer H, Wegener HH. [Nitrofurantoin-induced granulomatous hepatitis]. MMW Munch Med Wochenschr. 1977;119(47):1535–1536.
   PubMedGoogle Scholar
• Selroos O, Edgren J. Lupus-like syndrome associated with pulmonary reaction to nitrofurantoin. Report of three cases. Acta Med Scand. 1975;197(1–2):125–129.
   PubMedGoogle Scholar
• Iwarson S, Lindberg J, Lundin P. Nitrofurantoin-induced chronic liver disease. Clinical course and outcome of five cases. Scand J Gastroenterol. 1979;14(4):497–502.
   PubMed Web of Science ®Google Scholar
• Klemola H, Penttila O, Runeberg L, et al. Anicteric liver damage during nitrofurantoin medication. Scand J Gastroenterol. 1975;10(5):501–505.
   PubMed Web of Science ®Google Scholar
• Fagrell B, Strandberg I, Wengle B. A nitrofurantoin-induced disorder simulating chronic active hepatitis. A case report. Acta Med Scand. 1976;199(3):237–239.
   PubMedGoogle Scholar
• Stine JG, Khokhar OS, Charalambopoulos J, et al. Rheumatologists’ awareness of and screening practices for hepatitis B virus infection prior to initiating immunomodulatory therapy. Arthritis Care & Research. 2010;62(5):704–711.
   Web of Science ®Google Scholar
• Khokhar OS, Lewis JH. Hepatotoxicity of agents used in the management of inflammatory bowel disease. Dig Dis. 2010;28(3):508–518.
   PubMed Web of Science ®Google Scholar
• Adar T, Mizrahi M, Pappo O, et al. Adalimumab-induced autoimmune hepatitis. J Clin Gastroenterol. 2010;44(1):e20–22.
   PubMedGoogle Scholar
• Mancini S, Amorotti E, Vecchio S, et al. Infliximab-related hepatitis: discussion of a case and review of the literature. Intern Emerg Med. 2010;5(3):193–200.
   PubMed Web of Science ®Google Scholar
• Poulin Y, Therien G. Drug-induced hepatitis and lupus during infliximab treatment for psoriasis: case report and literature review. J Cutan Med Surg. 2010;14(2):100–104.
   PubMed Web of Science ®Google Scholar
• Mancini S, Amorotti E, Vecchio S, et al. Infliximab-related hepatitis: discussion of a case and review of the literature. Intern Emerg Med. 2010;5(3):193–200. Epub 12010 Jan 11727. doi:10.1007/s11739-009-0342-4.
   PubMed Web of Science ®Google Scholar
• Lewis JH. The art and science of diagnosing and managing drug-induced liver injury in 2015 and beyond. Clin Gastroenterol Hepatol. 2015;13(12):2173–2189.e8. doi:10.1016/j.cgh.2015.06.017. Epub 2015 Jun 23.
   Web of Science ®Google Scholar
• Aithal GP. Pharmacogenetic testing in idiosyncratic drug-induced liver injury: current role in clinical practice. Liver Int. 2015;35(7): 1801–1808.
   PubMed Web of Science ®Google Scholar
• Hawkins MT, Lewis JH. Latest advances in predicting DILI in human subjects: focus on biomarkers. Expert Opin Drug Metab Toxicol. 2012;8(12):1521–1530.
   PubMed Web of Science ®Google Scholar
• Senior JR. New biomarkers for drug-induced liver injury: are they really better? What do they diagnose? Liver Int. 2014;34(3):325–327.
   PubMed Web of Science ®Google Scholar
• Watkins PB. Managing the risk of drug-induced liver injury. Clin Pharmacol Ther. 2013;94(6):629–631.
   PubMed Web of Science ®Google Scholar
• Phillips E, Mallal S. Successful translation of pharmacogenetics into the clinic: the abacavir example. Mol Diagn Ther. 2009;13(1):1–9.
   PubMed Web of Science ®Google Scholar
• Daly AK. Human leukocyte antigen (HLA) pharmacogenomic tests: potential and pitfalls. Curr Drug Metab. 2014;15(2):196–201.
   PubMed Web of Science ®Google Scholar
• Urban TJ, Daly AK, Aithal GP. Genetic basis of drug-induced liver injury: present and future. Semin Liver Dis. 2014;34(2):123–133.
   PubMed Web of Science ®Google Scholar
• Yang X, Salminen WF, Shi Q, et al. Potential of extracellular microRNAs as biomarkers of acetaminophen toxicity in children. Toxicol Appl Pharmacol. 2015;284(2):180–187.
   PubMed Web of Science ®Google Scholar
• Momen-Heravi F, Bala S, Bukong T, et al. Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine. 2014;10(7):1517–1527.
   PubMed Web of Science ®Google Scholar
• Possamai LA, McPhail MJ, Khamri W, et al. The role of intestinal microbiota in murine models of acetaminophen-induced hepatotoxicity. Liver Int. 2015;35(3):764–773.
   PubMed Web of Science ®Google Scholar