The pathogenesis of drug-induced liver injury

References

• Abboud G, Kaplowitz N. Drug-induced liver injury. Drug Saf. 2007;30:277–294.
   PubMed Web of Science ®Google Scholar
• Bale SS, Vernetti L, Senutovitch N, et al. In vitro platforms for evaluating liver toxicity. Exp Biol Med (Maywood). 2014;239:1180–1191.
   PubMed Web of Science ®Google Scholar
• Boelsterli UA, Lim PL. Mitochondrial abnormalities–a link to idiosyncratic drug hepatotoxicity? Toxicol Appl Pharmacol. 2007;220:92–107.
   PubMed Web of Science ®Google Scholar
• Ingawale DK, Mandlik SK, Naik SR. Models of hepatotoxicity and the underlying cellular, biochemical and immunological mechanism(s): a critical discussion. Environ Toxicol Pharmacol. 2014;37:118–133.
   PubMed Web of Science ®Google Scholar
• Ostapowicz G, Fontana RJ, 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;137:947–954.
   PubMed Web of Science ®Google Scholar
• Khoury T, Rmeileh AA, Yosha L, et al. Drug induced liver injury: review with a focus on genetic factors, tissue diagnosis, and treatment options. J Clin Transl Hepatol. 2015;3:99–108.
   PubMed Web of Science ®Google Scholar
• Lee WM. Drug-induced acute liver failure. Clin Liver Dis. 2013;17:575–586, viii.
   PubMed Web of Science ®Google Scholar
• Watkins PB. Drug safety sciences and the bottleneck in drug development. Clin Pharmacol Ther. 2011;89:788–790.
   PubMed Web of Science ®Google Scholar
• Zimmerman HJ. Hepatotoxicity: the adverse effects of drugs and other chemicals on the liver. Philadelphia (PA): Lippincott Williams & Wilkins; 1999.
   Google Scholar
• Luedde T, Kaplowitz N, Schwabe RF. Cell death and cell death responses in liver disease: mechanisms and clinical relevance. Gastroenterology. 2014;147:765–783; e764.
   PubMed Web of Science ®Google Scholar
• Stephens C, Andrade RJ, Lucena MI. Mechanisms of drug-induced liver injury. Curr Opin Allergy Clin Immunol. 2014;14:286–292.
   PubMed Web of Science ®Google Scholar
• Fontana RJ, Watkins PB, Bonkovsky HL, et al. Drug-induced liver injury network (DILIN) prospective study: rationale, design and conduct. Drug Saf. 2009;32:55–68.
   PubMed Web of Science ®Google Scholar
• Takikawa H, Murata Y, Horiike N, et al. Drug-induced liver injury in Japan: an analysis of 1676 cases between 1997 and 2006. Hepatol Res. 2009;39:427–431.
   PubMed Web of Science ®Google Scholar
• Molokhia M, McKeigue P. EUDRAGENE: European collaboration to establish a case-control DNA collection for studying the genetic basis of adverse drug reactions. Pharmacogenomics. 2006;7:633–638.
   PubMed Web of Science ®Google Scholar
• Andrade RJ, Lucena MI, Fernández MC, et al. Drug-induced liver injury: an analysis of 461 incidences submitted to the Spanish registry over a 10-year period. Gastroenterology. 2005;129:512–521.
   PubMed Web of Science ®Google Scholar
• Mayoral W, Lewis JH, Zimmerman H. Drug-induced liver disease. Curr Opin Gastroenterol. 1999;15:208–216.
   PubMed Web of Science ®Google Scholar
• Karczmarek-Borowska B, Sałek-Zań A. Hepatotoxicity of molecular targeted therapy. Contemp Oncol (Pozn). 2015;19:87–92.
   PubMedGoogle Scholar
• Blumenthal KG, Patil SU, Long AA. The importance of vancomycin in drug rash with eosinophilia and systemic symptoms (DRESS) syndrome. Allergy Asthma Proc. 2012;33:165–171.
   PubMed Web of Science ®Google Scholar
• Björnsson E. Hepatotoxicity associated with antiepileptic drugs. Acta Neurol Scand. 2008;118:281–290.
   PubMed Web of Science ®Google Scholar
• O’Grady JG, Schalm SW, Williams R. Acute liver failure: redefining the syndromes. Lancet. 1993;342:273–275.
   PubMed Web of Science ®Google Scholar
• Mindikoglu AL, Magder LS, Regev A. Outcome of liver transplantation for drug-induced acute liver failure in the United States: analysis of the united network for organ sharing database. Liver Transpl. 2009;15:719–729.
   PubMed Web of Science ®Google Scholar
• Green RM, Flamm S. AGA technical review on the evaluation of liver chemistry tests. Gastroenterology. 2002;123:1367–1384.
   PubMed Web of Science ®Google Scholar
• Senior JR. Monitoring for hepatotoxicity: what is the predictive value of liver “function” tests? Clin Pharmacol Ther. 2009;85:331–334.
   PubMed Web of Science ®Google Scholar
• Watkins PB, Seeff LB. Drug-induced liver injury: summary of a single topic clinical research conference. Hepatology. 2006;43:618–631.
   PubMed Web of Science ®Google Scholar
• Bénichou C. Criteria of drug-induced liver disorders. Report of an international consensus meeting. J Hepatol. 1990;11:272–276.
   PubMed Web of Science ®Google Scholar
• Zheng EX, Navarro VJ. Liver injury from herbal, dietary, and weight loss supplements: a review. J Clin Transl Hepatol. 2015;3:93–98.
   PubMedGoogle Scholar
• Lewis JH. The art and science of diagnosing and managing drug-induced liver injury in 2015 and beyond. Clin Gastroenterol Hepatol. 2015;13:2173–2189; e2178.
   Web of Science ®Google Scholar
• Hayashi PH, Fontana RJ. Clinical features, diagnosis, and natural history of drug-induced liver injury. Semin Liver Dis. 2014;34:134–144.
   PubMed Web of Science ®Google Scholar
• Shi Q, Hong H, Senior J, et al. Biomarkers for drug-induced liver injury. Expert Rev Gastroenterol Hepatol. 2010;4:225–234.
   PubMed Web of Science ®Google Scholar
• Steuerwald NM, Foureau DM, Norton HJ, et al. Profiles of serum cytokines in acute drug-induced liver injury and their prognostic significance. PLoS One. 2013;8:e81974.
   PubMed Web of Science ®Google Scholar
• Starkey Lewis PJ, Dear J, Platt V, et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology. 2011;54:1767–1776.
   PubMed Web of Science ®Google Scholar
• Roderburg C, Benz F, Vargas Cardenas D, et al. Elevated miR-122 serum levels are an independent marker of liver injury in inflammatory diseases. Liver Int. 2015;35:1172–1184.
   PubMed Web of Science ®Google Scholar
• Russmann S, Kullak-Ublick GA, Grattagliano I. Current concepts of mechanisms in drug-induced hepatotoxicity. Curr Med Chem. 2009;16:3041–3053.
   PubMed Web of Science ®Google Scholar
• Fontana RJ. Pathogenesis of idiosyncratic drug-induced liver injury and clinical perspectives. Gastroenterology. 2014;146:914–928.
   PubMed Web of Science ®Google Scholar
• Boelsterli UA, Lee KK. Mechanisms of isoniazid-induced idiosyncratic liver injury: emerging role of mitochondrial stress. J Gastroenterol Hepatol. 2014;29:678–687.
   PubMed Web of Science ®Google Scholar
• Leigh DA, Lusby PJ, McBurney RT, et al. Getting harder: cobalt(III)-template synthesis of catenanes and rotaxanes. J Am Chem Soc. 2009;131:3762–3771.
   PubMed Web of Science ®Google Scholar
• Saab L, Peluso J, Muller CD, et al. Implication of hepatic transporters (MDR1 and MRP2) in inflammation-associated idiosyncratic drug-induced hepatotoxicity investigated by microvolume cytometry. Cytometry A. 2013;83:403–408.
   PubMed Web of Science ®Google Scholar
• Woodhead JL, Yang K, Brouwer KL, et al. Mechanistic modeling reveals the critical knowledge gaps in bile acid-mediated DILI. CPT Pharmacometrics Syst Pharmacol. 2014;3:e123.
   PubMedGoogle Scholar
• Welch MA, Kock K, Urban TJ, et al.. Toward predicting drug-induced liver injury: parallel computational approaches to identify multidrug resistance protein 4 and bile salt export pump inhibitors. Drug Metab Dispos. 2015;43:725–734.
   PubMed Web of Science ®Google Scholar
• Adams DH, Ju C, Ramaiah SK, et al. Mechanisms of immune-mediated liver injury. Toxicol Sci. 2010;115:307–321.
   PubMed Web of Science ®Google Scholar
• Uetrecht J, Naisbitt DJ. Idiosyncratic adverse drug reactions: current concepts. Pharmacol Rev. 2013;65:779–808.
   PubMed Web of Science ®Google Scholar
• Au JS, Navarro VJ, Rossi S. Review article: drug-induced liver injury–its pathophysiology and evolving diagnostic tools. Aliment Pharmacol Ther. 2011;34:11–20.
   PubMed Web of Science ®Google Scholar
• Eun JW, Bae HJ, Shen Q, et al. Characteristic molecular and proteomic signatures of drug-induced liver injury in a rat model. J Appl Toxicol. 2015;35:152–164.
   PubMed Web of Science ®Google Scholar
• Knudsen TB, Keller DA, Sander M, et al. FutureTox II: in vitro data and in silico models for predictive toxicology. Toxicol Sci. 2015;143:256–267.
   PubMed Web of Science ®Google Scholar
• Kalgutkar AS, Soglia JR. Minimising the potential for metabolic activation in drug discovery. Expert Opin Drug Metab Toxicol. 2005;1:91–142.
   PubMedGoogle Scholar
• Roth RA, Ganey PE. Intrinsic versus idiosyncratic drug-induced hepatotoxicity–two villains or one? J Pharmacol Exp Ther. 2010;332:692–697.
   PubMed Web of Science ®Google Scholar
• Fisher K, Vuppalanchi R, Saxena R. Drug-induced liver injury. Arch Pathol Lab Med. 2015;139:876–887.
   PubMed Web of Science ®Google Scholar
• Mitchell JR, Jollow DJ, Potter WZ, et al. Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism. J Pharmacol Exp Ther. 1973;187:185–194.
   PubMed Web of Science ®Google Scholar
• Hinson JA, Roberts DW, James LP. Mechanisms of acetaminophen-induced liver necrosis. Handb Exp Pharmacol. 2010;(196):369–405. doi:10.1007/978-3-642-00663-0_12.
   PubMedGoogle Scholar
• Kleiner DE, Chalasani NP, Lee WM, et al. Hepatic histological findings in suspected drug-induced liver injury: systematic evaluation and clinical associations. Hepatology. 2014;59:661–670.
   PubMed Web of Science ®Google Scholar
• Lewis W, Levine ES, Griniuviene B, et al. Fialuridine and its metabolites inhibit DNA polymerase gamma at sites of multiple adjacent analog incorporation, decrease mtDNA abundance, and cause mitochondrial structural defects in cultured hepatoblasts. Proc Natl Acad Sci U S A. 1996;93:3592–3597.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Uetrecht J. Idiosyncratic drug reactions: past, present, and future. Chem Res Toxicol. 2008;21:84–92.
   PubMed Web of Science ®Google Scholar
• Park BK, Pirmohamed M, Kitteringham NR. Role of drug disposition in drug hypersensitivity: a chemical, molecular, and clinical perspective. Chem Res Toxicol. 1998;11:969–988.
   PubMed Web of Science ®Google Scholar
• Ju C, Pohl LR. Tolerogenic role of Kupffer cells in immune-mediated adverse drug reactions. Toxicology. 2005;209:109–112.
   PubMed Web of Science ®Google Scholar
• Pichler WJ. Pharmacological interaction of drugs with antigen-specific immune receptors: the p-i concept. Curr Opin Allergy Clin Immunol. 2002;2:301–305.
   PubMed Web of Science ®Google Scholar
• Bhadauria S, Mishra R, Kanchan R, et al.. Isoniazid-induced apoptosis in HepG2 cells: generation of oxidative stress and Bcl-2 down-regulation. Toxicol Mech Methods. 2010;20:242–251.
   PubMed Web of Science ®Google Scholar
• Ramachandran A, Lebofsky M, Weinman SA, et al. The impact of partial manganese superoxide dismutase (SOD2)-deficiency on mitochondrial oxidant stress, DNA fragmentation and liver injury during acetaminophen hepatotoxicity. Toxicol Appl Pharmacol. 2011;251:226–233.
   PubMed Web of Science ®Google Scholar
• Bibi Z. Role of cytochrome P450 in drug interactions. Nutr Metab (Lond). 2008;5:27.
   PubMed Web of Science ®Google Scholar
• Boelsterli UA, Redinbo MR, Saitta KS. Multiple NSAID-induced hits injure the small intestine: underlying mechanisms and novel strategies. Toxicol Sci. 2013;131:654–667.
   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;34:123–133.
   PubMed Web of Science ®Google Scholar
• Matsumoto T, Ohno M, Azuma J. Future of pharmacogenetics-based therapy for tuberculosis. Pharmacogenomics. 2014;15:601–607.
   PubMed Web of Science ®Google Scholar
• Chen M, Suzuki A, Borlak J, et al. Drug-induced liver injury: interactions between drug properties and host factors. J Hepatol. 2015;63:503–514.
   PubMed Web of Science ®Google Scholar
• Aithal GP. Pharmacogenetic testing in idiosyncratic drug-induced liver injury: current role in clinical practice. Liver Int. 2015;35:1801–1808.
   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;109:950–966; quiz 967.
   PubMed Web of Science ®Google Scholar
• Chalasani N, Björnsson E. Risk factors for idiosyncratic drug-induced liver injury. Gastroenterology. 2010;138:2246–2259.
   PubMed Web of Science ®Google Scholar
• Hurwitz ES, Barrett MJ, Bregman D, et al. Public health service study of Reye’s syndrome and medications. Report of the main study. JAMA. 1987;257:1905–1911.
   PubMed Web of Science ®Google Scholar
• Scheffner D, König S, Rauterberg-Ruland I, et al. Fatal liver failure in 16 children with valproate therapy. Epilepsia. 1988;29:530–542.
   PubMed Web of Science ®Google Scholar
• Fountain FF, Tolley E, Chrisman CR, et al. Isoniazid hepatotoxicity associated with treatment of latent tuberculosis infection: a 7-year evaluation from a public health tuberculosis clinic. Chest. 2005;128:116–123.
   PubMed Web of Science ®Google Scholar
• Lucena MI, Andrade RJ, Fernández MC, et al. Determinants of the clinical expression of amoxicillin-clavulanate hepatotoxicity: a prospective series from Spain. Hepatology. 2006;44:850–856.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Chen M, Borlak J, Tong W. High lipophilicity and high daily dose of oral medications are associated with significant risk for drug-induced liver injury. Hepatology. 2013;58:388–396.
   PubMed Web of Science ®Google Scholar
• Kaplowitz N. Avoiding idiosyncratic DILI: two is better than one. Hepatology. 2013;58:15–17.
   PubMed Web of Science ®Google Scholar
• Ikemura K, Iwamoto T, Okuda M. Altered functions and expressions of drug transporters in liver, kidney and intestine in disorders of local and remote organs: possible role of oxidative stress in the pathogenesis. Expert Opin Drug Metab Toxicol. 2009;5:907–920.
   PubMed Web of Science ®Google Scholar
• Verbeeck RK. Pharmacokinetics and dosage adjustment in patients with hepatic dysfunction. Eur J Clin Pharmacol. 2008;64:1147–1161.
   PubMed Web of Science ®Google Scholar
• Daly AK, Day CP. Genetic association studies in drug-induced liver injury. Drug Metab Rev. 2012;44:116–126.
   PubMed Web of Science ®Google Scholar
• Stewart JD, Horvath R, Baruffini E, et al. Polymerase gamma gene POLG determines the risk of sodium valproate-induced liver toxicity. Hepatology. 2010;52:1791–1796.
   PubMed Web of Science ®Google Scholar
• Lucena MI, Molokhia M, Shen Y, et al. Susceptibility to amoxicillin-clavulanate-induced liver injury is influenced by multiple HLA class I and II alleles. Gastroenterology. 2011;141:338–347.
   PubMed Web of Science ®Google Scholar
• Stephens C, Lopez-Nevot MA, Ruiz-Cabello F, et al. HLA alleles influence the clinical signature of amoxicillin-clavulanate hepatotoxicity. PLoS One. 2013;8:e68111.
   PubMed Web of Science ®Google Scholar
• Perwitasari DA, Atthobari J, Wilffert B. Pharmacogenetics of isoniazid-induced hepatotoxicity. Drug Metab Rev. 2015;47:222–228.
   PubMed Web of Science ®Google Scholar
• Sharma SK, Balamurugan A, Saha PK, et al. Evaluation of clinical and immunogenetic risk factors for the development of hepatotoxicity during antituberculosis treatment. Am J Respir Crit Care Med. 2002;166:916–919.
   PubMed Web of Science ®Google Scholar
• Fontana RJ, Hayashi P, Bonkovsky HL, et al. Presentation and outcomes with clinically apparent interferon beta hepatotoxicity. Dig Dis Sci. 2013;58:1766–1775.
   PubMed Web of Science ®Google Scholar
• Watkins PB. Biomarkers for the diagnosis and management of drug-induced liver injury. Semin Liver Dis. 2009;29:393–399.
   PubMed Web of Science ®Google Scholar
• Teschke R, Frenzel C, Schulze J, et al. Herbal hepatotoxicity: challenges and pitfalls of causality assessment methods. World J Gastroenterol. 2013;19:2864–2882.
   PubMed Web of Science ®Google Scholar
• Davern TJ, Chalasani N, Fontana RJ, et al. Acute hepatitis E infection accounts for some cases of suspected drug-induced liver injury. Gastroenterology. 2011;141:1665–1672; e1661–e1669.
   PubMed Web of Science ®Google Scholar
• García-Cortés M, Lucena MI, Pachkoria K, et al. Evaluation of naranjo adverse drug reactions probability scale in causality assessment of drug-induced liver injury. Aliment Pharmacol Ther. 2008;27:780–789.
   PubMed Web of Science ®Google Scholar
• Lucena MI, Camargo R, Andrade RJ, et al. Comparison of two clinical scales for causality assessment in hepatotoxicity. Hepatology. 2001;33:123–130.
   PubMed Web of Science ®Google Scholar
• Teschke R, Frenzel C, Wolff A, et al. Drug induced liver injury: accuracy of diagnosis in published reports. Ann Hepatol. 2014;13:248–255.
   PubMed Web of Science ®Google Scholar
• Aithal GP, Rawlins MD, Day CP. Accuracy of hepatic adverse drug reaction reporting in one English health region. BMJ. 1999;319:1541.
   PubMed Web of Science ®Google Scholar
• Ishak KG, Zimmerman HJ. Morphologic spectrum of drug-induced hepatic disease. Gastroenterol Clin North Am. 1995;24:759–786.
   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;135:1924–1934, 1934; e1921–e1924.
   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;54:931–939.
   PubMed Web of Science ®Google Scholar
• Kleiner DE. The pathology of drug-induced liver injury. Semin Liver Dis. 2009;29:364–372.
   PubMed Web of Science ®Google Scholar
• Hennes EM, Zeniya M, Czaja AJ, et al. Simplified criteria for the diagnosis of autoimmune hepatitis. Hepatology. 2008;48:169–176.
   PubMed Web of Science ®Google Scholar
• Raja K, Thung SN, Fiel MI, et al. Drug-induced steatohepatitis leading to cirrhosis: long-term toxicity of amiodarone use. Semin Liver Dis. 2009;29:423–428.
   PubMed Web of Science ®Google Scholar
• Ramachandran R, Kakar S. Histological patterns in drug-induced liver disease. J Clin Pathol. 2009;62:481–492.
   PubMed Web of Science ®Google Scholar
• Robinson MJ, Rywlin AM. Tetracycline-associated fatty liver in the male. Report of an autopsied case. Am J Dig Dis. 1970;15:857–862.
   PubMedGoogle Scholar
• Larosche I, Lettéron P, Fromenty B, et al. Tamoxifen inhibits topoisomerases, depletes mitochondrial DNA, and triggers steatosis in mouse liver. J Pharmacol Exp Ther. 2007;321:526–535.
   PubMed Web of Science ®Google Scholar
• Bleeker-Rovers CP, Kadir SW, Van Leusen R, et al. Hepatic steatosis and lactic acidosis caused by stavudine in an HIV-infected patient. Neth J Med. 2000;57:190–193.
   PubMed Web of Science ®Google Scholar
• Kaplowitz N. Drug-induced liver injury. Clin Infect Dis. 2004;38(Suppl 2):S44–S48.
   PubMed Web of Science ®Google Scholar
• Holt MP, Cheng L, Ju C. Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol. 2008;84:1410–1421.
   PubMed Web of Science ®Google Scholar
• Krishnan PV, Feng -Z-Z, Gordon SC. Prolonged intrahepatic cholestasis and renal failure secondary to anabolic androgenic steroid-enriched dietary supplements. J Clin Gastroenterol. 2009;43:672–675.
   PubMed Web of Science ®Google Scholar
• Narita M, Oussoultzoglou E, Chenard M-P, et al. Liver injury due to chemotherapy-induced sinusoidal obstruction syndrome is associated with sinusoidal capillarization. Ann Surg Oncol. 2012;19:2230–2237.
   PubMed Web of Science ®Google Scholar
• Vietor NO, George BJ. Oxaliplatin-induced hepatocellular injury and ototoxicity: a review of the literature and report of unusual side effects of a commonly used chemotherapeutic agent. J Oncol Pharm Pract. 2012;18:355–359.
   PubMedGoogle Scholar
• Marino G, Zimmerman HJ, Lewis JH. Management of drug-induced liver disease. Curr Gastroenterol Rep. 2001;3:38–48.
   PubMedGoogle Scholar
• Aithal PG, Day CP. The natural history of histologically proved drug induced liver disease. Gut. 1999;44:731–735.
   PubMed Web of Science ®Google Scholar
• Mohi-ud-din R, Lewis JH. Drug- and chemical-induced cholestasis. Clin Liver Dis. 2004;8:95–132, vii.
   PubMedGoogle Scholar
• Andrade RJ, Lucena MI, 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.
   PubMed Web of Science ®Google Scholar
• Ventham NT, Kennedy NA, Nimmo ER, et al. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology. 2013;145:293–308.
   PubMed Web of Science ®Google Scholar