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Review

Hepatotoxicity of targeted therapy for cancer

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Pages 789-802 | Received 04 Mar 2016, Accepted 13 May 2016, Published online: 06 Jun 2016

References

  • Health Canada. Guidance document. Product monograph. Minister of Public Works and Government Services Canada; 2014 [updated 2014 Jun 1; cited 2016 Feb 1]. Available from: http://www.hc-sc.gc.ca/dhp-mps/alt_formats/pdf/prodpharma/applic-demande/guide-ld/monograph/pm_mp_2013-eng.pdf
  • Shah RR, Morganroth J, Shah DR. Hepatotoxicity of tyrosine kinase inhibitors: clinical and regulatory perspectives. Drug Saf. 2013;36:491–503.
  • Iacovelli R, Palazzo A, Procopio G, et al. Incidence and relative risk of hepatic toxicity in patients treated with anti-angiogenic tyrosine kinase inhibitors for malignancy. Br J Clin Pharmacol. 2013;77(6):929–938.
  • Pazopanib. Research Triangle Park (NC): GlaxoSmithKline; 2009 [cited 2016 Feb 1]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2009/022465lbl.pdf
  • Sunitinib. New York (NY): Pfizer Labs; 2011 [cited 2016 Feb 1]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2011/021938s13s17s18lbl.pdf
  • Regorafenib. Wayne (NJ): Bayer Healthcare Pharmaceuticals; 2012 [cited 2016 Feb 1]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2012/203085lbl.pdf
  • Takeda M, Okamoto I, Nakagawa K. Pooled safety analysis of EGFR-TKI treatment for EGFR mutation-positive non-small cell lung cancer. Lung Cancer. 2015;88:74–79.
  • Gefitinib. Wilmington (DE): AstraZeneca Pharmaceuticals LP; 2015 [cited 2016 Feb 1]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2015/206995s000lbl.pdf
  • Erlotinib. Melville (NY): OSI Pharmaceuticals, and Genentech; 2010 [cited 2016 Feb 1]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2010/021743s14s16lbl.pdf
  • Afatinib. Ridgefield (CT): Boehringer Ingelheim Pharmaceuticals; 2015 [cited 2016 Feb 1]. Available from: http://docs.boehringer-ingelheim.com/Prescribing%20Information/PIs/Gilotrif/Gilotrif.pdf?DMW_FORMAT=pdf
  • Lapatinib. Research Triangle Park (NC): GlaxoSmithKline; 2010 [cited 2016 Feb 1]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2010/022059s007lbl.pdf
  • LiverTox: clinical and research information on drug-induced liver injury. Bethesda (MD): United States National Library of Medicine; [updated 2015 Sep 30; cited 2016 Feb 1]. Available from: http://livertox.nih.gov/
  • 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.e4.
  • Andrade RJ, Lucena MI, Fernandez MC, et al. Drug-induced liver injury: an analysis of 461 incidence submitted to the Spanish registry over a 10-year period. Gastroenterology. 2005;129:512.
  • Björnsson E. Drug-induced liver injury: Hy’s rule revisited. Clint Pharmacy Ther. 2006;79:521.
  • Chalsani N, Björnsson E. Risk factors for idiosyncratic drug-induced liver injury. Gastroenterology. 2010;138:2246.
  • Björnsson E, Olsson R. Outcomes and prognostic markers in severe drug-induced liver disease. Hepatology. 2005;42:481.
  • Nelson DR, Kamataki T, Waxman DJ, et al. The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes and nomenclature. DNA Cell Biol. 1993;12:1.
  • Peterson JA, Graham SE. A close family resemblance: the importance of structure in understanding cytochromes P450. Structure. 1998;6:1079–1085.
  • Smith G, Subbins MJ, Harries LW, et al. Molecular genetics of the human cytochrome P450 monooxygenase superfamily. Xenobiotica. 1998;28:1129–1165.
  • Werk-Riechhart D, Feyereisen R. Cytochromes P450: a success story. Genome Biol. 2000;1:REVIEWS3003.
  • Danielson PB. The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curt Drug Metab. 2002;3:561.
  • Waxman DJ. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR and PPAR. Arch Biochem Biophys. 1999;369:11–23.
  • Park BK, Pirmohamed M, Kitteringham NR. The role of the cytochrome P450 enzymes in hepatic and extra hepatic human drug toxicity. Pharmacy There. 1995;68:385–424.
  • Murray M. Mechanisms and significance of inhibitory drug interactions involving cytochrome P450 enzymes (review). Int J Mol Med. 1999;3:277.
  • Sugatani J. Function, genetic polymorphism, an transcriptional regulation of human UDP-glucuronosyltransferase (UGT) 1A1. Drug Metab Pharmacokinet. 2013;28:83.
  • Basheer L, Kerem Z. Interactions between CYP3A4 and dietary polyphenols. Oxid Med Cell Longev. 2015;2015:1–15. Article ID 854015
  • Dai CL, Ma SL, Wang F, et al. Lapatinib promotes the incidence of hepatotoxicity by increasing chemotherapeutic agent accumulation in hepatocytes. Oncotarget. 2015;6(19):17738–17752.
  • Xu CF, Xue Z, Bing N, et al. Concomitant use of pazopanib and simvastatin increases the risk of transaminase elevations in patients with cancer. Ann Oncol. 2012;23(9):2470–2471.
  • Liu Y, Ramirez J, House L, et al. Comparison of the drug-drug interactions potential of erlotinib and gefitinib via inhibition of UDP-glucuronosyltransferases. Drug Metab Dispos. 2010;38:32–39.
  • Liu Y, Ramírez J, Ratain MJ. Inhibition of paracetamol glucuronidation by tyrosine kinase inhibitors. Br J Clin Pharmacol. 2011;71(6):917–920.
  • Nassar I, Pasupati T, Judson JP, et al. Histopathological study of the hepatic and renal toxicity associated with the co-administration of imatinib and acetaminophen in a preclinical mouse model. Malays J Pathol. 2010;32:1–11.
  • Ridruejo E, Cacchione R, Villamil AG, et al. Imatinib-induced fatal acute liver failure. World J Gastroenterol. 2007;13:6608–6611.
  • Committee for Medicinal Products for Human Use. Summary of product characteristics “Glivec” 21/02/2012. Glivec-EMEA/H/C/000406-II/0070. London: European Medicines Agency; [cited 2016 Feb 15]. Available from: www.emea.europa.eu/docs/en_GB/document_library/EPAR_-_Product_INformation/human/000406/WC500022207.pdf
  • Imatinib. East Hanover (NJ): Novartis; 2001 [cited 2016 Feb 15]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2008/021588s024lbl.pdf
  • Kim DW, Tan EY, Jin Y, et al. Effects of imatinib mesylate on the pharmacokinetics of paracetamol (acetaminophen) in Korean patients with chronic myelogenous leukaemia. Br J Clin Pharmacol. 2011;71:199–206.
  • 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;134:1924.
  • Shivakumar C, Farrell GC. Drug-induced liver disease. In: Schiff ER, Maddrey WC, Sorrell MF, editors. Schiff’s diseases of the liver. Hoboken (NJ): Wiley; 2012. p. 703.
  • Benedetti MS, Whomsley R, Canning M. Drug metabolism in the paediatric population and in the elderly. Drug Discov Today. 2007;12:599–610.
  • Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non–small-cell lung cancer with mutated EGFR. N Engl J Med. 2010;362:2380–2388.
  • Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2009;11:121–128.
  • Seki N, Uematsu K, Shibakuki R, et al. Promising new treatment schedule for gefitinib responders after severe hepatotoxicity with daily administration. J Clin Oncol. 2006;24(19):3213–3214.
  • Sim SH, Keam B, Kim DW, et al. The gefitinib dose reduction on survival outcomes in epidermal growth factor receptor mutant non-small cell lung cancer. J Cancer Res Clin Oncol. 2014;140(12):2135–2142.
  • Wang J, Wu Y, Dong M, et al. Observation of hepatotoxicity during long-term gefitinib administration in patients with non-small-cell lung cancer. Anticancer Drugs. 2016;27(3):245–250.
  • Ranson M, Hammond LA, Ferry D, et al. ZD1839, a selective oral epidermal growth factor receptor-tyrosine kinase inhibitor, is well tolerated and active in patients with solid, malignant tumors: results of a phase I trial. J Clin Oncol. 2002;20:2240–22450.
  • Nakagawa K, Tamura T, Negoro S, et al. Phase I pharmacokinetic trial of the selective oral epidermal growth factor receptor tyrosine kinase inhibitor gefitinib (′Iressa’, ZD1839) in Japanese patients with solid malignant tumors. Ann Oncol. 2003;14:922–930.
  • Baselga J, Rischin D, Ranson M, et al. Phase I safety, pharmacokinetic, and pharmacodynamic trial of ZD1839, a selective oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with five selected solid tumor types. J Clin Oncol. 2002;20:4292–4302.
  • Herbst RS, Maddox AM, Rothenberg ML, et al. Selective oral epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 is generally well-tolerated and has activity in non-small-cell lung cancer and other solid tumors: results of a phase I trial. J Clin Oncol. 2002;20:3815–3825.
  • Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer (the IDEAL 1 trial). J Clin Oncol. 2003;21:2237–2246.
  • Imai A, Hachiya T, Ikuyama Y, et al. [Successful treatment of non-small cell lung cancer with afatinib after gefitinib-induced hepatotoxicity]. Gan To Kagaku Ryoho. 2016;43(1):91–94. Japanese.
  • Yonesaka K, Suzumura T, Tsukuda H, et al. Erlotinib is a well-tolerated alternate treatment for non-small cell lung cancer in cases of gefitinib-induced hepatotoxicity. Anticancer Res. 2014;34(9):5211–5215.
  • Yano Y, Namba Y, Mori M, et al. Treatment of non-small-cell lung cancer with erlotinib following gefitinib-induced hepatotoxicity: review of 8 clinical cases. Lung Cancer Int. 2012;2012:354657.
  • Nagano T, Kotani Y, Kobayashi K, et al. Successful erlotinib treatment for a patient with gefitinib-related hepatotoxicity and lung adenocarcinoma refractory to intermittently administered gefitinib. Case Rep Pulmonol. 2011;2011:812972.
  • Kunimasa K, Yoshioka H, Iwasaku M, et al. Successful treatment of non-small cell lung cancer with gefitinib after severe erlotinib-related hepatotoxicity. Intern Med. 2012;51(4):431–434.
  • Nakatomi K, Nakamura Y, Tetsuya I, et al. Treatment with gefitinib after erlotinib-induced liver injury: a case report. J Med Case Rep. 2011;5:593.
  • Ku GY, Chopra A, Lopes Gde L Jr. Successful treatment of two lung cancer patients with erlotinib following gefitinib-induced hepatotoxicity. Lung Cancer. 2010;70(2):223–225.
  • Kijima T, Shimizu T, Nonen S, et al. Safe and successful treatment with erlotinib after gefitinib-induced hepatotoxicity: difference in metabolism as a possible mechanism. J Clin Oncol. 2011 Jul 1;29(19):e588–e590.
  • Takimoto T1, Kijima T, Otani Y, et al. Polymorphisms of CYP2D6 gene and gefitinib-induced hepatotoxicity. Clin Lung Cancer. 2013;14(5):502–507.
  • Sugiyama E, Umemura S, Nomura S, et al. Impact of single nucleotide polymorphisms on severe hepatotoxicity induced by EGFR tyrosine kinase inhibitors in patients with non-small cell lung cancer harboring EGFR mutations. Lung Cancer. 2015;90(2):307–313.
  • Gunawan BK, Kaplowitz N. Mechanisms of drug-induced liver disease. Clint Liver Dis. 2007;111:459.
  • Wong WM, Wu PC, Yuen MF, et al. Antituberculosis drug-related liver dysfunction in chronic hepatitis B infection. Hepatology. 2000;31:201–206.
  • Levy M. Role of viral infections in the induction of adverse drug reactions. Drug Saf. 1997;16:1–8.
  • Kleiner DE, Berman D. Pathologic changes in Ipilimumab-related hepatitis in patients with metastatic melanoma. Dig Dis Sci. 2012;57(8):2233–2240.
  • Spraggs CF, Xu CF, Hunt CM. Genetic characterization to improve interpretation and clinical management of hepatotoxicity caused by tyrosine kinase inhibitors. Pharmacogenomics. 2013;14(5):541–554.
  • Peroukides S, Makatsoris T, Koutras A, et al. Lapatinib-induced hepatitis: a case report. World J Gastroenterol. 2011;17:2349–2352.
  • Spraggs CF, Budde LR, Briley LP, et al. HLA-DQA1*02:01 is a major risk factor for lapatinib-induced hepatotoxicity in women with advanced breast cancer. J Clin Oncol. 2011;29(6):667–673.
  • Schaid DJ, Spraggs CF, McDonnell SK, et al. Prospective validation of HLA-DRB1*07:01 allele carriage as a predictive risk factor for lapatinib-induced liver injury. J Clin Oncol. 2014;32:2296–2303.
  • Spraggs CF, Parham LR, Warren L, et al. HLA-DRB1*07:01 biomarker characterization of hepatotoxicity during lapatinib combination therapies in ALTTO. J Clin Oncol. 2015;33(suppl):abstr 617.
  • Xu CF, Johnson T, Wang X, et al. HLA-B57:01 confers susceptibility to pazopanib-associated liver injury in patients with cancer. Clin Cancer Res. 2016;22(6):1371–1377.
  • Xu CF, Reck BH, Goodman VL, et al. Association of the hemochromatosis gene with pazopanib-induced transaminase elevation in renal cell carcinoma. J Hepatol. 2011;54:1237–1243.
  • Bosma PJ, Chowdhury JR, Bakker C, et al. The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1A1 in Gilbert’s syndrome. N Engl J Med. 1994;333:1171–1175.
  • Xu CF, Reck BH, Xue Z, et al. Pazopanib-induced hyperbilirubinemia is associated with Gilbert’s syndrome UGT1A1 polymorphism. Br J Cancer. 2010;102:1371–1377.
  • Motzer RJU, Johnson T, Choueiri TK, et al. Hyperbilirubinemia in pazopanib- or sunitinib-treated patients in COMPARZ is associated with UGT1A! polymorphisms. Ann Oncol. 2013;24:2927–2928.
  • Peer CJ, Sissung TM, Kim A, et al. Sorafenib is an inhibitor of UGT1A1 but is metabolised by UGT1A9: implications of genetic variants on pharmacokinetics and hyperbilirubinemia. Clin Cancer Res. 2012;18:2009.
  • Spraggs CF, Budde LR, Briley L, et al. Hyperbilirubinemia in lapatinib treated patients is associated with Gilbert’s syndrome UGT1A1 polymorphism. Cancer Res. 2009;69(Suppl. 24):Abstract 1112.
  • Verbeeck RK. Pharmacokinetics and dosage adjustment in patients with hepatic dysfunction. Euro J Clin Pharamcol. 2008;64:1147.
  • Saif MW. Erlotinib-induced acute hepatitis in a patient with pancreatic cancer. Clin Adv Hematol Oncol. 2008;6:191–199.
  • Tonyali O, Coskun U, Yildiz R, et al. Imatinib mesylate-induced acute liver failure in a patient with gastrointestinal stromal tumors. Med Oncol. 2010;27:768–773.
  • Kong JH, Yoo SH, Lee KE, et al. Early imatinib-mesylate- induced hepatotoxicity in chronic myelogenous leukaemia. Acta Haematol. 2007;118:205–208.
  • Spataro V. Nilotinib in a patient with postnecrotic liver cirrhosis related to imatinib. J Clin Oncol. 2011;29:e50–e52.
  • Klempner SJ, Choueiri TK, Yee E, et al. Severe pazopanib-induced hepatotoxicity: clinical and histologic course in two patients. J Clin Oncol. 2012;30:e264–e268.
  • Schieren G, Bölke E, Scherer A, et al. Severe everolimus-induced steatohepatis: a case report. Eur J Med Res. 2013;18:22.
  • Force J, Saxena R, Schneider BP, et al. Nodular regenerative hyperplasia after treatment with trastuzumab emtansine. J Clin Oncol. 2014 20;34(3):e9–e12.
  • Lakhani S, Davidson L, Priebat DA, et al. Reactivation of chronic hepatitis B infection related to imatinib mesylate therapy. Hepatol Int. 2008;2(4):498–499.
  • Walker EJ, Simko JP, Ko AH. Hepatitis B viral reactivation secondary to imatinib treatment in a patient with gastrointestinal stromal tumor. Anticancer Res. 2014;34(7):3629–3634.
  • Kang BW, Lee SJ, Moon JH, et al. Chronic myeloid leukemia patient manifesting fatal hepatitis B virus reactivation during treatment with imatinib rescued by liver transplantation: case report and literature review. Int J Hematol. 2009;90:383–387.
  • Lai GM, Yan SL, Chang CS, et al. Hepatitis B reactivation in chronic myeloid leukemia patients receiving tyrosine kinase inhibitor. World J Gastroenterol. 2013;19(8):1318–1321.
  • Shiah HS, Chen CY, Dai CY, et al. Randomised clinical trial: comparison of two everolimus dosing schedules in patients with advanced hepatocellular carcinoma. Aliment Pharmacol Ther. 2013;37:62–73.
  • Mizuno S, Yamagishi Y, Ebinuma H, et al. Progressive liver failure induced by everolimus for renal cell carcinoma in a 58-year-old male hepatitis B virus carrier. Clin J Gastroenterol. 2013;6:188–192.
  • Sezgin Göksu S, Bilal S, Coşkun HŞ. Hepatitis B reactivation related to everolimus. World J Hepatol. 2013;5:43–45.
  • Teplinsky E, Cheung D, Weisberg I, et al. Fatal hepatitis B reactivation due to everolimus in metastatic breast cancer: case report and review of literature. Breast Cancer Res Treat. 2013;141:167–172.
  • LiverTox: clinical and research information on drug-induced liver injury: drug record: Rituximab. Bethesda (MD): United States National Library of Medicine; [updated 2015 Sep 30; cited 2016 Feb 15]. Available from: http://livertox.nlm.nih.gov/Rituximab.htm
  • Mitka M. FDA: increased HBV reactivation risk with ofatumumab or rituximab. JAMA. 2013;310(16):1664.
  • Sachdeva M, Dhingra S. Obinutuzumab: a FDA approved monoclonal antibody in the treatment of untreated chronic lymphocytic leukemia. Int J Appl Basic Med Res. 2015;5(1):54–57.
  • Cil T, Altintas A, Tuzun Y, et al. Hepatitis B virus reactivation induced by Yttrium-90-ibritumomab-tiuxetan. Leuk Lymphoma. 2007;48(9):1866–1868.
  • Heider U, Fleissner C, Zavrski I, et al. Treatment of refractory chronic lymphocytic leukemia with Campath-1H in combination with lamivudine in chronic hepatitis B infection. Eur J Haematol. 2004;72:64–66.
  • Iannitto E, Minardi V, Calvaruso G, et al. Hepatitis B virus reactivation and alemtuzumab therapy. Eur J Haematol. 2005;74:254–258.
  • Moses SE, Lim ZY, Sudhanva M, et al. Lamivudine prophylaxis and treatment of hepatitis B virus-exposed recipients receiving reduced intensity conditioning hematopoietic stem cell transplants with alemtuzumab. J Med Virol. 2006;78:1560–1563.
  • Pembrolizumab. Whitehouse Station (NJ): Merck; 2014 [cited 2016 Feb 15]. Available from: https://www.merck.com/product/usa/pi_circulars/k/keytruda/keytruda_pi.pdf
  • Nivolumab. Princeton (NJ): Bristol-Myers Squibb; 2014 [cited 2016 Feb 15]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2014/125554lbl.pdf
  • Kapoor R, Kottilil S. Strategies to eliminate HBV infection. Future Virology. 2014;9(6):565–585.
  • Seruga B, Sterling L, Wang L, et al. Reporting of serious adverse drug reactions of targeted anticancer agents in pivotal phase III clinical trials. J Clin Oncol. 2011;29:174–185.
  • Niraula S, Seruga B, Ocana A, et al. The price we pay for progress: a meta-analysis of harms of newly approved anticancer drugs. J Clin Oncol. 2012;30:3012–3019.
  • Chang J, Rand M, Blumenthal GM, et al. FDA evaluation of hepatotoxicity related to tyrosine kinase inhibitors. J Clin Oncol. 2011;29(suppl):abstr 3106.
  • Gupta-Abramson V, Troxel AB, Nellore A, et al. Phase II trial of sorafenib in advanced thyroid cancer. J Clin Oncol. 2008;26:4714–4719.
  • Llanos L, Bellot P, Zapater P, et al. Acute hepatitis in a patient with cirrhosis and hepatocellular carcinoma treated with sorafenib. Am J Gastroenterol. 2009;104:257–258.
  • Fairfax B, Pratap S, Roberts I, et al. Fatal case of sorafenib-associated idiosyncratic hepatotoxicity in the adjuvant treatment of a patient with renal cell carcinoma. BMC Cancer. 2012;12:590.
  • Herden U, Fischer L, Schafer H, et al. Sorafenib-induced severe acute hepatitis in a stable liver transplant recipient. Transplantation. 2010;90:98–99.
  • Schramm C, Schuch G, Lohse AW. Sorafenib-induced liver failure. Am J Gastroenterol. 2008;103:2162–2163.
  • Marks AB, Gerard R, Fournier P, et al. Sorafenib-induced hepatic encephalopathy. Ann Pharmacother. 2009;43:2121.
  • Van Hootegem A, Verslype A, Van Steenbergen W. Sorafenib-induced liver failure: a case report and review of the literature. Case Rep Hepatol. 2011;2011:1–4. Article ID 941395
  • European Medicines Agency. Nexavar: procedural steps taken and scientific information after the authorisation; [cited 2016 Feb 14]. Available from: http://www.emea.europa.eu/docs/en_GB/document_library/EPAR_-_Procedural_steps_taken_and_scientific_information_after_authorisation/human/000690/WC500027709.pdf
  • Rini BI, Escudier B, Tomczak P, et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial. Lancet 2011;378:1931–1939.

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