Herb-Drug Interactions and Hepatotoxicity

Author(s): Mohammad K. Parvez* , Vikas Rishi .

Journal Name: Current Drug Metabolism

Volume 20 , Issue 4 , 2019


Graphical Abstract:


Abstract:

Background: In recent times, herbals or phytomedicines have become very popular due to their global acceptance as a complementary and alternative remedy. While modern drugs are commercially available only after laboratory validations, clinical trials, as well as approval from drug regulatory authorities, majority of the marketed herbal products lack such scientific evidence of efficacy and safety. This results in herb or herb-drug interaction induced unfavorable clinical outcomes without crucial documentation on their temporal relations and concomitant use.

Methods: An online literature search for peer-reviewed articles was conducted on the PubMed, Europe PMC, Medline and Google Scholar portals, using the phrases: complementary & alternative medicine, traditional Chinese medicine, herb-drug interaction, mechanisms of herb-drug interaction, herb-induced toxicity, herbal hepatotoxicity and causality, traditional medicine, viral hepatitis, etc.

Results: The retrieved data showed that globally, patients are attracted to herbal remedies with the misconception that these are completely safe and therefore, use them simultaneously with prescription drugs. Notably, there exists a potential risk of herb-drug interactions leading to some adverse side effects, including hepatotoxicity. The toxicological effect of a drug or herb is due to the inhibition of drug metabolizing enzymes (e.g., cytochrome P450), including interactions with certain prescription drugs through various mechanisms. Several cases of hepatotoxicity due to use of herbals in viral hepatitis-related liver diseases have been recently reported. However, limited experimental data and clinical evidence on herbal pharmacokinetics hamper the evaluation and reporting of adverse reactions and the underlying mechanisms.

Conclusion: Herb-drug interaction related morbidity is thus an emerging serious public health issue with broad implications for clinicians, pharmaceutical industries and health authorities. Nonetheless, despite increasing recognition of herb-drug interaction, a standard system for interaction prediction and evaluation is still nonexistent. This review article discusses the herb-drug interactions related hepatotoxicity and underlying mechanisms, including drug metabolizing enzymes and their regulation.

Keywords: Complementary & alternative medicine, traditional Chinese medicine, herbals, drug metabolism, herb-drug interaction, hepatotoxicity.

[1]
Ganesan, A. The impact of natural products upon modern drug discovery. Curr. Opin. Chem. Biol., 2008, 12, 306-317.
[2]
Clardy, J.; Walsh, C. Lessons from natural molecules. Nature, 2004, 432, 829-837.
[3]
Song, P.P.; Gao, J.J.; Kokudo, N.; Tang, W. Standardization of traditional Chinese medicine and evaluation of evidence from its clinical practice. Drug Discov. Ther., 2011, 5, 261-265.
[4]
Kennedy, J. Herb and supplement use in the US adult population. Clin. Ther., 2005, 27, 1847-1858.
[5]
Bronstein, A.C.; Spyker, D.A.; Cantilena, L.R., Jr; Green, J.; Rumack, B.H.; Heard, S.E. 2006 annual report of the american association of poison control centers’ National Poison Data System (NPDS). Clin. Toxicol. (Phila.), 2007, 45, 815-917.
[6]
Glisson, J.K.; Walker, L.A. How physicians should evaluate dietary supplements. Am. J. Med., 2010, 123, 577-582.
[7]
Chen, X-W.; Sneed, K.B.; Pan, S.Y.; Cao, C.; Kanwar, J.R.; Chew, H.; Zhou, S-F. Herb-Drug interactions and mechanistic and clinical considerations. Curr. Drug Metab., 2012, 13, 640-6451.
[8]
Werneke, U.; Earl, J.; Seydel, C.; Horn, O.; Crichton, P.; Fannon, D. Potential health risks of complementary alternative medicines in cancer patients. Br. J. Cancer, 2004, 90, 408-413.
[9]
Bunchorntavakul, C.; Reddy, K.R. Review article: Herbal and dietary supplement hepatotoxicity. Aliment. Pharmacol. Ther., 2013, 37, 3-17.
[10]
Aithal, G.P.; Rawlins, M.D.; Day, C.P. Accuracy of hepatic adverse drug reaction reporting in one English health region. BMJ, 1999, 319, 41-45.
[11]
Dalton, H.R. Fellows, H.J: Stableforth, W.; Joseph, M.; Thurairajah, P.H. The role of hepatitis E virus testing in drug-induced liver injury. Aliment. Pharmacol. Ther., 2007, 26, 1429-1435.
[12]
Davern, T.J.; Chalasani, N.; Fontana, R.J.; Hayashi, P.H.; Protiva, P.; Kleiner, D.E.; Engle, R.E.; Nguyen, H.; Emerson, S.U.; Purcell, R.H.; Tillmann, H.L.; Gu, J.; Serrano, J.; Hoofnagle, J.H. Drug-Induced Liver Injury Network (DILIN). Acute hepatitis E infection accounts for some cases of suspected drug-induced liver injury. Gastroenterology, 2011, 141, 1665-1672.
[13]
Teschke, R.; Schulze, J.; Schwarzenboeck, A.; Eickhoff, A.; Frenzel, C. Herbal hepatotoxicity: Suspected cases assessed for alternative causes. Eur. J. Gastroenterol. Hepatol., 2013, 25, 1093-1098.
[14]
Liddle, C.; Goodwin, B. Regulation of hepatic drug metabolism: Role of the nuclear receptors PXR and CAR. Semin. Liver Dis., 2002, 22, 115-122.
[15]
Omura, T. Forty years of cytochrome P450. Biochem. Biophys. Res. Commun., 1999, 266, 690-698.
[16]
Gonzalez, F.J. The molecular biology of cytochrome P450s. Pharmacol. Rev., 1998, 40, 243-288.
[17]
Waxman, D.J.; Azaroff, L. Phenobarbital induction of cytochrome P-450 gene expression. Biochem. J., 1992, 281, 577-592.
[18]
Nelson, D.R.; Kamataki, T.; Waxman, D.J.; Guengerich, F.P.; Estabrook, R.W.; Feyereisen, R.; Gonzalez, F.J.; Coon, M.J.; Gunsalus, I.C.; Gotoh, O. The P450 superfamily: Update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol., 1993, 12, 1-51.
[19]
Rendic, S.; Di Carlo, F.J. Human cytochrome P450 enzymes: A status report summarizing their reactions, substrates, inducers, and inhibitors. Drug Metab. Rev., 1997, 29, 413-480.
[20]
Gray, I.C.; Nobile, C.; Muresu, R.; Ford, S.; Spurr, N.K.A. 2.4-megabase physical map spanning the CYP2C gene cluster on chromosome 10q24. Genomics, 1995, 28, 328-332.
[21]
Miners, J.O.; Birkett, D.J. Use of tolbutamide as a substrate probe for human hepatic cytochrome P450 2C9. Methods Enzymol., 1996, 272, 139-145.
[22]
Rettie, A.E.; Korzekwa, K.R.; Kunze, K.L.; Lawrence, R.F.; Eddy, A.C.; Aoyama, T.; Gelboin, H.V.; Gonzalez, F.J.; Trager, W.F. Hydroxylation of warfarin by human cDNA-expressed cytochrome P-450: A role for P-4502C9 in the etiology of (S)-warfarin-drug interactions. Chem. Res. Toxicol., 1992, 5, 54-59.
[23]
Henthorn, T.K.; Benitez, J.; Avram, M.J. Assessment of the debrisoquin and dextromethorphan phenotyping tests by gaussian mixture distributions analysis. Clin. Pharmacol. Ther., 1989, 45, 328-333.
[24]
Girre, C.; Lucas, D.; Hispard, E.; Menez, C.; Dally, S.; Menez, J-F. Assessment of cytochrome P4502E1 induction in alcoholic patients by chlorzoxazone pharmacokinetics. Biochem. Pharmacol., 1994, 47, 1503-1508.
[25]
Lieber, C.S. Cytochrome P-4502E1: Its physiological and pathological role. Physiol. Rev., 1997, 77, 517-544.
[26]
Kolars, J.C.; Schmiedlin-Ren, P.; Schuetz, J.D.; Fang, C.; Watkins, P.B. Identification of rifampin-inducible P450IIIA4 (CYP3A4) in human small bowel enterocytes. J. Clin. Invest., 1992, 90, 1871-1878.
[27]
Schuetz, E.G.; Guzelian, P.S. Induction of cytochrome P-450 by glucocorticoids in rat liver. II. Evidence that glucocorticoids regulate induction of cytochrome P-450 by a nonclassical receptor mechanism. J. Biol. Chem., 1984, 259, 2007-2012.
[28]
Zhou, S.F.; Lai, X. An update on clinical drug interactions with the herbal antidepressant St. John’s wort. Curr. Drug Metab., 2008, 9, 394-409.
[29]
Harmsen, S.; Meijerman, I.; Beijnen, J.H.; Schellens, J.H. Nuclear receptor mediated induction of cytochrome P450 3A4 by anticancer drugs: A key role for the pregnane X receptor. Cancer Chemother. Pharmacol., 2009, 64, 35-43.
[30]
Quattrochi, L.C.; Guzelian, P.S. Cyp3A regulation: From pharmacology to nuclear receptors. Drug Metab. Dispos., 2001, 29, 615-622.
[31]
Li, Y.; Ross-Viola, J.S.; Shay, N.F.; Moore, D.D.; Ricketts, M.L. Human CYP3A4 and murine Cyp3A11 are regulated by equol and genistein via the pregnane X receptor in a species-specific manner. J. Nutr., 2009, 139, 898-904.
[32]
Al-Dosari, M.S.; Parvez, M.K. Novel plant inducers of PXR-dependent cytochrome P450 3A4 expression in HepG2 cells. Saudi Pharm. J., 2018, 26, 1069-1072.
[33]
Ritter, J.K. Roles of glucuronidation and UDP-glucuronosyl-transferases in xenobiotic bioactivation reactions. Chem. Biol. Interact., 2000, 129, 171-193.
[34]
Radominska-Pandya, A.; Czernik, P.J.; Little, J.M.; Battaglia, E.; Mackenzie, P.I. Structural and functional studies of UDP-glucuronosyltransferases. Drug Metab. Rev., 1999, 31, 817-899.
[35]
Gregory, P.A.; Lewinsky, R.H.; Gardner-Stephen, D.A.; Mackenzie, P.I. Regulation of UDP glucuronosyltransferases in the gastrointestinal tract. Toxicol. Appl. Pharmacol., 2004, 199, 354-363.
[36]
Eraly, S.A.; Bush, K.T.; Sampogna, R.V.; Bhatnagar, V.; Nigam, S.K. The molecular pharmacology of organic anion transporters: from DNA to FDA? Mol. Pharmacol., 2004, 65, 479-487.
[37]
Marchetti, S.; Mazzanti, R.; Beijnen, J.H.; Schellens, J.H. Concise review: Clinical relevance of drug drug and herb drug interactions mediated by the ABC transporter ABCB1 (MDR1, P-glycoprotein). Oncologist, 2004, 12, 927-941.
[38]
Otsuka, M.; Matsumoto, T.; Morimoto, R.; Arioka, S.; Omote, H.; Moriyama, Y. A human transporter protein that mediates the final excretion step for toxic organic cations. Proc. Natl. Acad. Sci. USA, 2005, 102, 17923-17928.
[39]
Aleksunes, L.M.; Cui, Y.; Klaassen, C.D. Prominent expression of xenobiotic efflux transporters in mouse extraembryonic fetal membranes compared with placenta. Drug Metab. Dispos., 2008, 36, 1960-1970.
[40]
Al-Dosari, M.S.; Parvez, M.K. Genetic polymorphisms of drug eliminating enzymes and transporters. Biomed. Genet. Genom., 2016, 1, 44-50.
[41]
Gonzalez, F.J.; Kasper, C.B. Cloning of DNA complementary to rat liver NADPH-cytochrome c (P-450) oxidoreductase and cytochrome P-450b mRNAs. Evidence that phenobarbital augments transcription of specific genes. J. Biol. Chem., 1982, 257, 5962-5968.
[42]
Klotz, U.; Ammon, E. Clinical and toxicological consequences of the inductive potential of ethanol. Eur. J. Clin. Pharmacol., 1998, 54, 7-12.
[43]
Wang, H.; LeCluyse, E.L. Role of orphan nuclear receptors in the regulation of drug-metabolising enzymes. Clin. Pharmacokinet., 2003, 42, 1331-1357.
[44]
Bertilsson, G.; Heidrich, J.; Svensson, K.; Asman, M.; Jendeberg, L.; Sydow-Bäckman, M.; Ohlsson, R.; Postlind, H.; Blomquist, P.; Berkenstam, A. Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc. Natl. Acad. Sci. USA, 1998, 95, 12208-12013.
[45]
Lehmann, J.M.; McKee, D.D.; Watson, M.A.; Willson, T.M.; Moore, J.T.; Kliewer, S.A. The human orphan nuclear receptor PXR is activated by compounds that regulate CYP3A4 gene expression and cause drug interactions. J. Clin. Invest., 1998, 102, 1016-1023.
[46]
Goodwin, B.; Moore, L.B.; Stoltz, C.M.; McKee, D.D.; Kliewer, S.A. Regulation of the human CYP2B6 gene by the nuclear pregnane X receptor. Mol. Pharmacol., 2001, 60, 427-431.
[47]
Gerbal-Chaloin, S.; Pascussi, J.M.; Pichard-Garcia, L.; Daujat, M.; Waechter, F.; Fabre, J.M.; Carrère, N.; Maurel, P. Induction of CYP2C genes in human hepatocytes in primary culture. Drug Metab. Dispos., 2001, 29, 242-251.
[48]
Moore, J.T.; Kliewer, S.A. Use of the nuclear receptor PXR to predict drug interactions. Toxicology, 2000, 153, 1-10.
[49]
Moore, L.B.; Goodwin, B.; Jones, S.A.; Wisely, G.B.; Serabjit-Singh, C.J.; Willson, T.M.; Collins, J.L.; Kliewer, S.A.St. John’s wort induces hepatic drug metabolism through activation of the pregnane X receptor. Proc. Natl. Acad. Sci. USA, 2000, 97, 7500-7502.
[50]
Moore, L.B.; Parks, D.J.; Jones, S.A.; Bledsoe, R.K.; Consler, T.G.; Stimmel, J.B.; Goodwin, B.; Liddle, C.; Blanchard, S.G.; Willson, T.M.; Collins, J.L.; Kliewer, S.A. Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J. Biol. Chem., 2000, 275, 15122-15127.
[51]
Xu, L.W.; Jia, M.; Salchow, R.; Kentsch, M.; Cui, X.J.; Deng, H.Y.; Sun, Z.J.; Kluwe, L. Efficacy and side effects of Chinese herbal medicine for menopausal symptoms: A critical review. Evid. Based Complement. Alternat. Med., 2012, 2012, 568106.
[52]
Hu, D.; Wang, Y.; Chen, Z.; Ma, Z.; You, Q.; Zhang, X.; Liang, Q.; Tan, H.; Xiao, C.; Tang, X.; Gao, Y. The protective effect of piperine on dextran sulfate sodium induced inflammatory bowel disease and its relation with pregnane X receptor activation. J. Ethnopharmacol., 2015, 169, 109-123.
[53]
Hu, D.; Wang, Y.; Chen, Z.; Ma, Z.; You, Q.; Zhang, X.; Zhou, T.; Xiao, Y.; Liang, Q.; Tan, H.; Xiao, C.; Tang, X.; Zhang, B.; Gao, Y. Artemisinin protects against dextran sulfate-sodium-induced inflammatory bowel disease, which is associated with activation of the pregnane X receptor. Eur. J. Pharmacol., 2014, 738, 273-284.
[54]
Zhang, J.; Ding, L.; Wang, B.; Ren, G.; Sun, A.; Deng, C.; Wei, X.; Mani, S.; Wang, Z.; Dou, W. Notoginsenoside R1 attenuates experimental inflammatory bowel disease via pregnane X receptor activation. J. Pharmacol. Exp. Ther., 2015, 352, 315-324.
[55]
Moore, L.B.; Maglich, J.M.; McKee, D.D.; Wisely, B.; Willson, T.M.; Kliewer, S.A.; Lambert, M.H.; Moore, J.T.; Pregnane, X. Receptor (PXR), Constitutive Androstane Receptor (CAR), and Benzoate X Receptor (BXR) define three pharmacologically distinct classes of nuclear receptors. Mol. Endocrinol., 2002, 16, 977-986.
[56]
Carazo, A.; Dusek, J.; Holas, O.; Skoda, J.; Hyrsova, L.; Smutny, T.; Soukup, T.; Dosedel, M.; Pávek, P. Teriflunomide is an indirect human Constitutive Androstane Receptor (CAR) activator interacting with Epidermal Growth Factor (EGF) signaling. Front. Pharmacol., 2018, 9, 993-1006.
[57]
Knebel, C.; Neeb, J.; Zahn, E.; Schmidt, F.; Carazo, A.; Holas, O.; Pavek, P.; Püschel, G.P.; Zanger, U.M.; Süssmuth, R.; Lampen, A.; Marx-Stoelting, P.; Braeuning, A. Unexpected effects of propiconazole, tebuconazole, and their mixture on the receptors CAR and PXR in human liver cells. Toxicol. Sci., 2018, 163, 170-181.
[58]
Benedict, W.F.; Considine, N.; Nebert, D.W. Genetic differences in aryl hydrocarbon hydroxylase induction and benzo(a)pyrene-produced tumorigenesis in the mouse. Mol. Pharmacol., 1973, 9, 266-277.
[59]
Poland, A.; Glover, E.; Kende, A.S. Stereospecific, high affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol. Evidence that the binding species is receptor for induction of aryl hydrocarbon hydroxylase. J. Biol. Chem., 1976, 251, 4936-4946.
[60]
Hankinson, O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol., 1995, 35, 307-340.
[61]
Diaz, D.; Fabre, I.; Daujat, M.; Saint Aubert, B.; Bories, P.; Michel, H.; Maurel, P. Omeprazole is an aryl hydrocarbon-like inducer of human hepatic cytochrome P450. Gastroenterology, 1990, 99, 737-747.
[62]
Fuhr, U. Induction of drug metaboliing enzymes: Pharmacokinetic and toxicological consequences in humans. Clin. Pharmacokinet., 2000, 38, 493-504.
[63]
Nguyen, N.T.; Nakahama, T.; Nguyen, C.H.; Tran, T.T.; Le, V.S.; Chu, H.H.; Kishimoto, T. Aryl hydrocarbon receptor antagonism and its role in rheumatoid arthritis. J. Exp. Pharmacol., 2015, 7, 29-35.
[64]
Issemann, I.; Green, S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature, 1990, 347, 645-650.
[65]
Forman, B.M.; Chen, J.; Evans, R.M. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc. Natl. Acad. Sci. USA, 1997, 94, 4312-4317.
[66]
Schmiedlin-Ren, P.; Thummel, K.E.; Fisher, J.M.; Paine, M.F.; Lown, K.S.; Watkins, P.B. Expression of enzymatically active CYP3A4 by Caco-2 cells grown on extracellular matrix-coated permeable supports in the presence of 1alpha,25-dihydroxyvitamin D3. Mol. Pharmacol., 1997, 51, 741-754.
[67]
Drocourt, L.; Ourlin, J.C.; Pascussi, J.M.; Maurel, P.; Vilarem, M.J. Expression of CYP3A4, CYP2B6, and CYP2C9 is regulated by the vitamin D receptor pathway in primary human hepatocytes. J. Biol. Chem., 2002, 277, 25125-25132.
[68]
Chen, K.S.; DeLuca, H.F. Cloning of the human 1 alpha,25-dihydroxyvitamin D-3 24-hydroxylase gene promoter and identification of two vitamin D-responsive elements. Biochim. Biophys. Acta, 1995, 1263, 1-9.
[69]
Goodwin, B.; Jones, S.A.; Price, R.R.; Watson, M.A.; McKee, D.D.; Moore, L.B.; Galardi, C.; Wilson, J.G.; Lewis, M.C.; Roth, M.E.; Maloney, P.R.; Willson, T.M.; Kliewer, S.A. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell, 2000, 6, 517-526.
[70]
Janowski, B.A.; Willy, P.J.; Devi, T.R.; Falck, J.R.; Mangelsdorf, D.J. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature, 1996, 383, 728-731.
[71]
Forman, B.M.; Goode, E.; Chen, J.; Oro, A.E.; Bradley, D.J.; Perlmann, T.; Noonan, D.J.; Burka, L.T.; McMorris, T.; Lamph, W.W.; Evans, R.M.; Weinberger, C. Identification of a nuclear receptor that is activated by farnesol metabolites. Cell, 1995, 81, 687-693.
[72]
Cheung, C.; Akiyama, T.E.; Kudo, G.; Gonzalez, F.J. Hepatic expression of cytochrome P450s in hepatocyte nuclear factor 1-alpha (HNF1alpha)-deficient mice. Biochem. Pharmacol., 2003, 66, 2011-2020.
[73]
Jover, R.; Bort, R.; Gomez-Lechon, M.J.; Castell, J.V. Cytochrome P450 regulation by hepatocyte nuclear factor 4 in human hepatocytes: a study using adenovirus- mediated antisense targeting. Hepatology, 2001, 33, 668-675.
[74]
Corchero, J.; Granvil, C.P.; Akiyama, T.E.; Hayhurst, G.P.; Pimprale, S.; Feigenbaum, L.; Idle, J.R.; Gonzalez, F.J. The CYP2D6 humanized mouse: effect of the human CYP2D6 transgene and HNF4 alpha on the disposition of debrisoquine in the mouse. Mol. Pharmacol., 2001, 60, 1260-1267.
[75]
Jover, R.; Bort, R.; Gómez-Lechón, M.J.; Castell, J.V. Re-expression of C/EBP alpha induces CYP2B6, CYP2C9 and CYP2D6 genes in HepG2 cells. FEBS Lett., 1998, 431, 227-230.
[76]
Teschke, R.; Wolff, A.; Frenzel, C.; Schwarzenboeck, A.; Schulze, J.; Eickhoff, A. Drug and herb induced liver injury: Council for international organizations of medical sciences scale for causality assessment. World J. Hepatol., 2014, 6, 17-32.
[77]
Aithal, G.P.; Watkins, P.B.; Andrade, R.J.; Larrey, D.; Molokhia, M.; Takikawa, H.; Hunt, C.M.; Wilke, R.A.; Avigan, M.; Kaplowitz, N.; Bjornsson, E.; Daly, A.K. Case definition and phenotype standardization in drug-induced liver injury. Clin. Pharmacol. Ther., 2011, 89, 806-815.
[78]
Teschke, R.; Schmidt-Taenzer, W.; Wolff, A. Spontaneous reports of assumed herbal hepatotoxicity by black cohosh: is the liver-unspecific Naranjo scale precise enough to ascertain causality? Pharmacoepidemiol. Drug Saf., 2011, 20, 567-582.
[79]
Kim, T.Y.; Kim, D. Acute-on-chronic liver failure. Clin. Mol. Hepatol., 2013, 19, 349-359.
[80]
Larson, A.M. Diagnosis and management of acute liver failure. Curr. Opin. Gastroenterol., 2010, 26, 214-221.
[81]
Larson, A.M.; Polson, J.; Fontana, R.J.; Davern, T.J.; Lalani, E.; Hynan, L.S.; Reisch, J.S.; Schiødt, F.V.; Ostapowicz, G.; Shakil, A.O.; Lee, W.M. Acute Liver Failure Study Group. Acetaminophen-induced acute liver failure: Results of a United States multicenter, prospective study. Hepatology, 2005, 42, 1364-1372.
[82]
Krishna, Y.R.; Mittal, V.; Grewal, P.; Fiel, M.I.; Schiano, T. Acute liver failure caused by ‘fat burners’ and dietary supplements: A case report and literature and literature review. Can. J. Gastroenterol., 2011, 25, 157-160.
[83]
Gunawan, B.; Kaplowitz, N. Clinical perspectives on xenobiotic induced hepatoxicity. Drug Metab. Rev., 2004, 36, 301-312.
[84]
Stewart, M.J.; Steenkamp, V. Pyrrolizidine poisoning: A neglected area in human toxicology. Ther. Drug Monit., 2001, 23, 698-708.
[85]
Pittler, M.H.; Ernst, E. Systematic review: Hepatotoxic events associated with herbal medicinal products. Aliment. Pharmacol. Ther., 2003, 18, 451-471.
[86]
Schiano, T.D. Hepatotoxicity and complementary and alternative medicines. Clin. Liver Dis., 2003, 7, 453-473.
[87]
Stedman, C. Herbal hepatotoxicity. Semin. Liver Dis., 2002, 22, 195-206.
[88]
Teschke, R.; Bahre, R. Severe hepatotoxicity by Indian Ayurvedic herbal products: A structured causality assessment. Ann. Hepatol., 2009, 8, 258-266.
[89]
Dantuluri, S.; North-Lewis, P.; Karthik, S.V. Gotu Kola induced hepatotoxicity in a child- need for caution with alternative remedies. Dig. Liver Dis., 2011, 43, 500-504.
[90]
Jorge, O.A.; Jorge, A.D. Hepatotoxicity associated with the ingestion of Centella asiatica. Rev. Esp. Enferm. Dig., 2005, 97, 115-124.
[91]
Fleig, W.W.; Morgan, M.Y.; Holzer, M.A. European multicenter study group. The ayurvedic drug Liv.52 in patients with alcoholic cirrhosis. Results of a prospective, randomized, double-blind, placebo-controlled clinical trial. J. Hepatol., 1997, 126, 127-132.
[92]
Modi, A.A.; Wright, E.C.; Leonard, B.S. Complementary and Alternative Medicine for the treatment of hepatitis B and C: A review. Antivir. Ther., 2007, 12, 285-295.
[93]
Yuen, M.F.; Tam, S.; Fung, J.; Wong, D.K.; Wong, B.C.; Lai, C.L. Traditional Chinese Medicine causing hepatotoxicity in patients with chronic hepatitis B infection: A 1-year prospective study. Aliment. Pharmacol. Ther., 2006, 24, 1179-1186.
[94]
Lee, C.H.; Wang, J.D.; Chen, P.C. Risk of liver injury associated with Chinese herbal products containing Radix bupleuri in 639,779 patients with hepatitis B virus infection. PLoS One, 2011, 6, e16064.
[95]
Estes, J.D.; Stolpman, D.; Olyaei, A.; Corless, C.L.; Ham, J.M.; Schwartz, J.M.; Orloff, S.L. High prevalence of potentially hepatotoxic herbal supplement use in patients with fulminant hepatic failure. Arch. Surg., 2003, 138, 852-858.
[96]
Petry, J.J. Garlic and postoperative bleeding. Plast. Reconstr. Surg., 1995, 96, 483-484.
[97]
Sunter, W.H. Warfarin and garlic. Pharm. J., 1991, 246, 772-775.
[98]
Evans, V. Herbs and the brain: Friend or foe? The effects of ginkgo and garlic on warfarin use. J. Neurosci. Nurs., 2000, 32, 229-232.
[99]
Galluzzi, S.; Zanetti, O.; Binetti, G.; Trabucchi, M.; Frisoni, G.B. Coma in a patient with Alzheimer’s disease taking low dose trazodone and Ginkgo biloba. J. Neurol. Neurosurg. Psychiatry, 2000, 68, 679-680.
[100]
Jones, B.D.; Runikis, A.M. Interaction of ginseng with phenelzine. J. Clin. Psychopharmacol., 1987, 7, 201-202.
[101]
Piscitelli, S.C.; Burstein, A.H.; Welden, N.; Gallicano, K.D.; Falloon, J. The effect of garlic supplements on the pharmacokinetics of saquinavir. Clin. Infect. Dis., 2002, 34, 234-238.
[102]
Sitprija, S.; Plengvidhya, C.; Kangkaya, V.; Bhuvapanich, S.; Tunkayoon, M. Garlic and diabetes mellitus phase II clinical trial. J. Med. Assoc. Thai., 1987, 70, 223-227.
[103]
Gorski, J.C.; Jones, D.R.; Hamman, M.A.; Wrighton, S.A.; Hall, S.D. Biotransformation of alprazolam by members of the human cytochrome P4503A subfamily. Xenobiotica, 1999, 29, 931-944.
[104]
Piscitelli, S.C.; Formentini, E.; Burstein, A.H.; Alfaro, R.; Jagannatha, S.; Falloon, J. Effect of milk thistle on the pharmacokinetics of indinavir in healthy volunteers. Pharmacotherapy, 2002, 22, 551-556.
[105]
Mauro, V.F.; Mauro, L.S.; Kleshinski, J.F. Khuder, S.A.; Wang, Y.; Erhardt, P.W. Impact of Ginkgo biloba on the pharmacokinetics of digoxin. Am. J. Ther., 2003, 10, 247-251.
[106]
Hu, Z.; Yang, X.; Ho, P.C.; Chan, S.Y.; Heng, P.W.; Chan, E.; Duan, W.; Koh, H.L.; Zhou, S. Herb-drug interactions: A literature review. Drugs, 2005, 65, 1239-1282.
[107]
Izzo, A.A. Interactions between Herbs and conventional drugs: Overview of the clinical data. Med. Princ. Pract., 2012, 21, 404-428.
[108]
Tsukamoto, S; Aburatani, M; Ohta, T. Isolation of CYP3A4 inhibitors from the black cohosh (Cimicifuga racemosa). eCAM, 2005, 2, 223-226.
[109]
Budzinski, J.W.; Foster, B.C.; Vandenhoek, S.; Arnason, J.T. An in vitro evaluation of human cytochrome P450 3A4 inhibition by selected commercial herbal extracts and tinctures. Phytomedicine, 2000, 7, 273-282.
[110]
Toselli, F.; Matthiasv, A.; Gillam, E.M.J. Echinacea metabolism and drug interactions: The case for standardization of a complementary medicine. Life Sci., 2009, 85, 97-106.
[111]
Choi, H.A.; Kim, M-R.; Park, K.A.; Hong, J. Interaction of over-the-Counter Drugs with Curcumin: Influence on Stability and Bioactivities in Intestinal Cells. J. Agric. Food Chem., 2012, 60, 10578-10584.
[112]
Chen, X-W.; Sneed, K.B.; Pan, S-Y.; Cao, C.; Kanwar, J.R.; Chew, H.; Zhou, S-F. Herb-drug interactions and mechanistic and clinical considerations. Curr. Drug Metab., 2012, 13, 640-651.
[113]
Meng, Q.; Liu, K. Pharmacokinetic interactions between herbal medicines and prescribed drugs: Focus on drug metabolic enzymes and transporters. Curr. Drug Metab., 2014, 15, 791-707.
[114]
Darwich, A.S.; Neuhoff, S.; Jamei, M.; Rostami-Hodjegan, A. Interplay of metabolism and transport in determining oral drug absorption and gut wall metabolism: A simulation assessment using the “Advanced Dissolution, Absorption, Metabolism (ADAM)” model. Curr. Drug Metab., 2010, 11, 716-729.
[115]
Choi, J.G.; Eom, S.M.; Kim, J.; Kim, S.H.; Huh, E.; Kim, H.; Lee, Y.; Lee, H.; Oh, M.S. A Comprehensive review of recent studies on herb-drug interaction: A focus on pharmacodynamic interaction. J. Altern. Complement. Med. NYN, 2016, 22, 262-279.
[116]
Reeta, K.H.; Mehla, J.; Pahuja, M.; Gupta, Y.K. Pharmacokinetic and pharmacodynamic interactions of valproate, phenytoin, phenobarbitone and carbamazepine with curcumin in experimental models of epilepsy in rats. Pharmacol. Biochem. Behav., 2011, 99, 399-407.
[117]
Zhou, S.; Gao, Y.; Jiang, W.; Huang, M.; Xu, A.; Paxton, J.W. Interactions of herbs with cytochrome P450. Drug Metab. Rev., 2003, 35, 35-98.
[118]
Fasinu, P.S.; Bouic, P.J.; Rosenkranz, B. An overview of the evidence and mechanisms of herb-drug interactions. Front. Pharmacol., 2012, 3, 69-73.
[119]
Posadzki, P.; Watson, L.; Ernst, E. Herb-drug interactions: An overview of systematic reviews. Br. J. Clin. Pharmacol., 2013, 75, 603-618.
[120]
Nowack, R. Review article: Cytochrome P450 enzyme, and transport protein mediated herb-drug interactions in renal transplant patients: Grapefruit juice, St John’s Wort - and beyond! Nephrology, 2008, 13, 337-347.
[121]
Yang, S.Y.; Juang, S.H.; Tsai, S.Y.; Chao, P.D.; Hou, Y.C.St. John’s wort significantly increased the systemic exposure and toxicity of methotrexate in rats. Toxicol. Appl. Pharmacol., 2012, 263, 39-43.
[122]
Lin, K.; Lin, A.N.; Linn, S.; Hlaing, P.P.; Vasudev, V.; Reddy, M. Ginseng-related drug-induced liver injury. Case Rep. Gastroenterol., 2018, 12, 439-446.
[123]
Danan, G.; Teschke, R. Drug-induced liver injury: Why is the Roussel Uclaf Causality Assessment Method (RUCAM) still used 25 years after its launch? Drug Saf., 2018, 41(8), 735-743.
[124]
Teschke, R.; Schulze, J.; Eickhoff, A.; Danan, G. Drug induced liver injury: Can biomarkers assist RUCAM in causality assessment? Int. J. Mol. Sci., 2017, 18, E803.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 20
ISSUE: 4
Year: 2019
Page: [275 - 282]
Pages: 8
DOI: 10.2174/1389200220666190325141422
Price: $58

Article Metrics

PDF: 46
HTML: 3