1,508
Views
207
CrossRef citations to date
0
Altmetric
Research Article

Detoxification of Lithocholic Acid, A Toxic Bile Acid: Relevance to Drug Hepatotoxicity

, M.D.
Pages 703-722 | Published online: 25 Oct 2004

References

  • Bagheri S. A., Bolt M. G., Boyer J. L., Palmer R. H. Stimulation of thymidine incorporation in mouse liver and biliary tract epithelium by lithocholate an deoxycholate. Gastroenterology 1978; 74: 188–192, [PUBMED], [INFOTRIEVE]
  • Barbier O., Torra I. P., Sirvent A., Claudel T., Blanquart C., Duran‐Sandoval D., Kuipers F., Kosykh V., Fruchart J. C., Staels B. FXR inducs the UGT2B4 enzyme in hepatocytes: a potential mechanism of negative feedback control of FXR activity. Gastroenterology 2003; 124: 1926–1940, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Bell G. D., Mok H. Y., Thwe M., Murphy G. M., Henry K., Dowling R. H. Liver structure and function in cholelithiasis: effect of chenodeoxycholic acid. Gut 1974; 15: 165–172, [PUBMED], [INFOTRIEVE]
  • Beuers U., Denk G. U., Soroka C. J., Wimmer R., Rust C., Paumgartner G., Boyer J. L. Taurolithocholic acid exerts cholestatic effects via phosphatidylinositol 3‐kinase‐dependent mechanisms in perfused rat livers and rat hepatocyte couplets. J. Biol. Chem. 2003; 278: 17810–17818, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Bolder U., Trang N. V., Hagey L. R., Schteingart C. D., Ton‐Nu H.‐T., Cerrè C., Elferink R. O., Hofmann A. F. Sulindac is excreted into bile by a canalicular bile salt pump and undergoes a cholehepatic circulation in rats. Gastroenterology 1999; 117: 962–971, [PUBMED], [INFOTRIEVE]
  • Borgstrom B., Barrowman J., Krabisch L., Lindstrom M., Lillienau J. Effect of cholic acid, 7 beta‐hydroxy‐ and 12 beta‐hydroxy isocholic acid on bile flow, lipid secretion, and bile acid synthesis in the rat. Scand. J. Clin. Lab. Invest. 1986; 46: 167–175, [PUBMED], [INFOTRIEVE]
  • Carey M. C., Small D. M. The physical chemistry of cholesterol solubility in bile. J. Clin. Invest. 1978; 61: 998–1026, [PUBMED], [INFOTRIEVE]
  • Carey J. B., Jr., Wilson I. D., Zaki F. G., Hanson R. F. The metabolism of bile acids with special reference to liver injury. Medicine 1966; 45: 461–470, [PUBMED], [INFOTRIEVE]
  • Chen F., Ma L., Dawson P. A., Sinal C. J., Sehayek E., Gonzalez F. J., Breslow J., Ananthanarayanan M., Shneider B. I. Liver receptor homologue‐1 mediates species‐ and cell line‐specific bile acid‐dependent negative feedback regulation of the apical sodium‐dependent bile acid transporter. J. Biol. Chem. 2003; 278: 19909–19916, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Clayton L. M., Gurantz D., Hofmann A. F., Hagey L. R., Schteingart C. D. The role of bile acid conjugation in hepatic transport of dihydroxy bile acids. J. Pharm. Exp. Ther. 1989; 248: 1130–1137
  • Cowen A. E., Korman M. G., Hofmann A. F., Cass O. W. Metabolism of lithocholate in healthy man. I. Biotransformation and biliary excretion of intravenously administered lithocholate, lithocholylglycine, and their sulfates. Gastroenterology 1975a; 69: 59–66, [PUBMED], [INFOTRIEVE]
  • Cowen A. E., Korman M. G., Hofmann A. F., Cass O. W., Coffin S. B. Metabolism of lithocholate in healthy man. II. Enterohepatic circulation. Gastroenterology 1975b; 69: 67–76, [PUBMED], [INFOTRIEVE]
  • Crocenzi F. A., Mottino A. D., Sanchez Pozzi E. J., Pellegrino J. M., Rodriguez Garay E. A., Milkiewicz P., Vore M., Coleman R., Roma M. G. Impaired localization and transport function of canalicular Bsep in taurolithocholate induced cholestasis in the rat. Gut 2003; 52: 1170–1177, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Czygan P., Stiehl A. Untersuchungen zur Toxizitat sulfatierter und nicht sulfatierter Gallensaeuren. Z. Gastroenterol. 1975; 13: 468–473
  • Danzinger R. G., Hofmann A. F., Schoenfield L. J., Thistle J. L. Dissolution of cholesterol gallstones by chenodeoxycholic acid. N. Engl. J. Med. 1972; 286: 108
  • Dew M. J., Hawker P. C., Nutter S., Allan R. N. Human intestinal sulphation of lithocholate: a new site of bile acid metabolism. Life Sci. 1980; 28: 317–323, [CROSSREF]
  • Dew M. J., James K., Gatehouse D., Dorricott N. J., Allan R. N. Lithocholate sulphation in the baboon. J. Med. Primatol. 1982; 11: 59–64, [PUBMED], [INFOTRIEVE]
  • Duane W. C. The intermicellar bile salt concentration in equilibrium with the mixed micelles of human bile. Biochim. Biophys. Acta. 1975; 398: 275–286, [PUBMED], [INFOTRIEVE]
  • Dumont M., Erlinger S., Uchman S. Hypercholeresis induced by ursodeoxycholic acid and ketolithocholic acid in the rat: possible role of bicarbonate transport. Gastroenterology 1980; 79: 82–89, [PUBMED], [INFOTRIEVE]
  • Dyrszka H., Salen G., Zaki F. G., Chen T., Mosbach E. H. Hepatic toxicity in the Rhesus monkey treated with chenodeoxycholic acid for 7 months: biochemical and ultrastructural studies. Gastroenterology 1976; 70: 93–104, [PUBMED], [INFOTRIEVE]
  • Federowski T., Salen G., Zaki F. G., Shefer S., Mosbach E. H. Comparative effects of ursodeoxycholic acid and chenodeoxycholic acid in the rhesus monkey. Gastroenterology 1978; 74: 75–81
  • Fischer H. Zur Kenntnis der Gallenfarbstoffe. I. Z. Physiol. Chem. 1911; 73: 204–239
  • Fischer C. D., Cooper N. S., Rothschild M. A., Mosbach E. H. Effect of dietary chenodeoxycholic acid and lithocholic acid in the rabbit. Am. J. Dig. Dis. 1974; 18: 877–886
  • Fisher R. L., Hofmann A. F., Converse J. L., Rossi S. S., Lan S.‐P. Lack of relationship between hepatotoxicity and lithocholic acid sulfation during chenodiol therapy in the National Cooperative Gallstone Study. Hepatology 1991; 14: 454–463, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Gadacz T. R., Allan R. N., Mack E., Hofmann A. F. Impaired lithocholate sulfation in the rhesus monkey: a possible mechanism for chenodeoxycholate toxicity. Gastroenterology 1976; 70: 1125–1129, [PUBMED], [INFOTRIEVE]
  • Goto T., Holzinger F., Hagey L. R., Cerre C., Ton‐Nu H.‐T., Schteingart C. D., Steinbach J. H., Shneider B. L., Hofmann A. F. Physicochemical and physiological properties of 5 α‐cyprinol sulfate, the toxic bile salt of cyprinid fish. J. Lipid Res. 2003; 44: 1643–1651, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Grundy S. M., Hofmann A. F., Davignon J., Ahrens E. H., Jr. Human cholesterol synthesis is regulated by bile acids. J. Clin. Invest. 1966; 45: 1018–1019, (abstract)
  • Guo G. L., Lambert G., Negishi M., Ward J. M., Brewer H. B., Jr., Kliewer S. A., Gonzalez F. J., Sinal C. J. Complementary roles of farnesoid X receptor, pregnane receptor, and constitutive androstane receptor in protection against bile acid toxicity. J. Biol. Chem. 2003; 278: 45062–45071, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Halvorsen B., Kase B. F., Prydz K., Garagozlian S., Andresen M. S., Kolset S. O. Sulphation of lithocholic acid in the colon‐carcinoma cell line CaCo‐2. Biochem. J. 1999; 343: 53309, [CROSSREF]
  • Heywood R., Palmer A. K., Foll C. V., Lee M. R. Pathological changes in fetal Rhesus monkey induced by oral chenodeoxycholic acid. Lancet 1973; 2: 1021, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Hofmann A. F. Intestinal absorption of bile acids and biliary constituents: the intestinal component of the enterohepatic circulation and the integrated system. Physiology of the Gastrointestinal Tract3rd Ed., L. R. Johnson, D. H. Alpers, J. Christensen, E. D. Jacobson, J. H. Walsh. Raven Press, New York 1994; Vol. 2: 1845–1865
  • Hofmann A. F., Small D. M. Detergent properties of bile salts: correlation with physiological function. Ann. Rev. Med. 1967; 18: 333–376, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Hofmann A. F., Thistle J. L. An algorithm for monitoring and managing drug hepatotoxicity. Gastroenterology 1974; 67: 309–313, [PUBMED], [INFOTRIEVE]
  • Hofmann A. F., Mysels K. J. Bile salts as biological surfactants. Colloids Surf. 1988; 30: 145–173, [CROSSREF]
  • Hofmann A. F., Mysels K. J. Bile acid solubility and precipitation in vitro and in vivo: the role of conjugation, pH and Ca2 + ions. J. Lipid Res. 1992; 33: 617–626, [PUBMED], [INFOTRIEVE]
  • Hofmann A. F., Schteingart C. D., Hagey L. R. Species differences in bile acid metabolism. Bile Acids and Liver Diseases (International Falk Workshop), G. Paumgartner, U. Beuers. Kluwer Academic Publishers, Boston 1995; 3–30
  • Holsti P. Cirrhosis of the liver induced in rabbits by gastric instillation of 3‐monohydroxycholanic acid. Nature 1960; 186: 250
  • Holsti P. Bile acids as a cause of liver injury: cirrhogenic effect of chenodeoxycholic acid in rabbits. Acta Pathol. Microbiol. Scand. 1962; 54: 479
  • Hunt R. D., Leveille G. A., Sauberlich H. E. Dietary bile acids and lipid metabolism. III. Effects of lithocholic acid in mammalian species. Proc. Soc. Exp. Biol. Med. 1964; 115: 277–280, [PUBMED], [INFOTRIEVE]
  • Hutterer F., Bacchin P. G., Denk H., Schenkman J. B., Schaffner F., Popper H. Mechanism of cholestasis. II. Effect of bile acids on the microsomal electron transfer system in vitro. Life Sci. 1970; 9: 1159–1166, [CROSSREF]
  • Javitt N. B. Cholestasis in rats induced by taurolithocholate. Nature 1966; 210: 1262–1263, [PUBMED], [INFOTRIEVE]
  • Kitada H., Miyata M., Nakamura T., Tozawa A., Honma W., Shimada M., Nagata K., Sinal C. J., Guo G. I., Gonzalez F. J., Yamazoe Y. Protective role of hydroxysteroid sulfotransferase in lithocholic acid‐induced liver toxicity. J. Biol. Chem. 2003; 278: 17838–17844, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Kitani K., Kinai S. Ursodeoxycholate‐induced choleresis in taurine‐deprived and taurine‐supplemented rats. Jpn. J. Physiol. 1985; 35: 443–462, [PUBMED], [INFOTRIEVE]
  • Kubitz R., Sutfels G., Kuhlkamp T., Kolling R., Haussinger D. Trafficking of the bile salt export pump from the Golgi to the canalicular membrane is regulated by the p38 MAP kinase. Gastroenterology 2004; 126: 541–553, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Kuipers F., Heslinga H., Havinga R., Vonk R. J. Intestinal absorption of lithocholic acid sulfates in the rat: inhibitory effects of calcium. Amer. J. Physiol. 1986; 251: G189–G194, [PUBMED], [INFOTRIEVE]
  • Lake J. R., Renner E. L., Scharschmidt B. F., Cragoe E. J., Jr., Hagey L. R., Lambert K. J., Gurantz D., Hofmann A. F. Inhibition of Na+/H+ exchange in the rat is associated with decreased ursodeoxycholate hypercholeresis, decreased secretion of unconjugated ursodeoxycholate, and increased ursodeoxycholate glucuronidation. Gastroenterology 1988; 95: 454–463, [PUBMED], [INFOTRIEVE]
  • Lee T. K., Hammond C. L., Ballatori N. Intracellular glutathione regulates taurocholate transport in HepG2 cells. Toxicol. Appl. Pharmacol. 2001; 174: 207–215, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Leuschner U., Schneider M., Korte L. The influence of chenodeoxycholic acid and ursodeoxycholic acid on the hepatic structure of the rat. Z. Gastroenterol. 1979; 17: 244–255, [PUBMED], [INFOTRIEVE]
  • Lorenzo‐Zuniga V., Bartoli R., Planas R., Hofmann A. F., Vinado B., Hagey L. R., Hernandez J. M., Mane J., Alvarez M. A., Ausina V., Gassull M. A. Oral bile acids reduce bacterial overgrowth, bacterial translocation and endotoxemia in cirrhotic rats. Hepatology 2003; 37: 551–557, [CROSSREF]
  • Makashima M., Lu T. T., Xie W., Whitfield G. K., Domoto H., Evans R. M., Haussler M. R., Mangelsdorf D. J. Vitamin D receptor as an intestinal bile acid sensor. Science 2002; 296: 1313–1316, [CROSSREF]
  • Merrill J. R., Schteingart C. D., Hagey L. R., Peng Y., Ton‐Nu H. T., Frick E., Jirsa M., Hofmann A. F. Hepatic biotransformation in rodents and physicochemical properties of 23(R)‐hydroxychenodeoxycholic acid, a natural α‐hydroxy bile acid. J. Lipid Res. 1996; 37: 98–112, [PUBMED], [INFOTRIEVE]
  • Morrissey K. P., McSherry C. K., Swarm R. L., Nieman W. H., Deitrick J. E. Toxicity of chenodeoxycholic acid in the nonhuman primate. Surgery 1975; 77: 851–860, [PUBMED], [INFOTRIEVE]
  • Nathanson M. H., Boyer J. L. Mechanisms and regulation of bile secretion. Hepatology 1991; 14: 551–566, [PUBMED], [INFOTRIEVE]
  • Okun R., Goldstein L. I., Van Gelder G. A., Goldenthal E. I., Wazeter F. X., Giel R. G. National Cooperative Gallstone Study: nonprimate toxicology of chenodeoxycholic acid. J. Toxicol. Environ. Health 1982; 9: 727–741, [PUBMED], [INFOTRIEVE]
  • O'Maille E. R.L., Kozmary S. V., Hofmann A. F., Gurantz D. Differing effects of norcholate and cholate on bile flow and biliary lipid secretion in the rat. Am. J. Physiol. 1984; 246: G67–G71, [PUBMED], [INFOTRIEVE]
  • Oude Elferink R. P., Groen A. K. Mechanisms of biliary lipid secretion and their role in lipid homeostasis. Semin. Liver Dis. 2000; 20: 293–305, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Oude Elferink R. P.J., de Haan J., Lambert K. J., Hagey L. R., Hofmann A. F., Jansen P. L.M. Selective hepatobiliary transport of nordeoxycholate side chain conjugates in mutant rats with a canalicular transport defect. Hepatology 1989; 9: 861–865, [PUBMED], [INFOTRIEVE]
  • Palmer R. H. Bile acid sulfates. II. Formation, metabolism, and excretion of lithocholic acid sulfates in the rat. J. Lipid Res. 1971; 12: 680–687, [PUBMED], [INFOTRIEVE]
  • Palmer R. H. Toxic effects of lithocholate on the liver and biliary tree. The Hepatobiliary System. Fundamental and Pathological Mechanisms, W. Taylor. Plenum Press, New York 1976; 227–240
  • Palmer R. H., Hruban Z. Production of bile duct hyperplasia and gallstones by lithocholic acid. J. Clin. Invest. 1966; 45: 1255–1267, [PUBMED], [INFOTRIEVE]
  • Palmer R. H., Bolt M. G. Bile acid sulfates. I. Synthesis of lithocholic acid sulfates and their identification in human bile. J. Lipid Res. 1971; 12: 671–679, [PUBMED], [INFOTRIEVE]
  • Palmer A. K., Heywood R. Pathological changes in the rhesus fetus associated with the oral administration of chenodeoxycholic acid. Toxicology 1974; 2: 239–246, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Palmer R. H., McSherry C. K. Lithocholate metabolism in baboons fed chenodeoxycholate. J. Lab. Clin. Med. 1982; 99: 533–538, [PUBMED], [INFOTRIEVE]
  • Pattison N. R., Chapman B. A. Lithocholate detoxification and biliary secretion in the rat. Biochem. Int. 1984; 9: 137–142
  • Paumgartner G., Beuers U. Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited. Hepatology 2002; 36: 525–531, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Pircher P. C., Kitto J. L., Petrowski M. L., Tangirala R. K., Bischoff E. D., Schulman I. G., Westin S. K. Farnesoid X receptor regulates bile acid‐amino acid conjugation. J. Biol. Chem. 2003; 25: 27703–27711, [CROSSREF]
  • Rege R. V., Moore E. W. Pathogenesis of calcium‐containing gallstones. Canine ductular bile, but not gallbladder bile, is supersaturated with calcium carbonate. J. Clin. Invest. 1986; 77: 21–26, [PUBMED], [INFOTRIEVE]
  • Remmer H. The role of the liver in drug metabolism. Am. J. Med. 1970; 49: 617–629, [PUBMED], [INFOTRIEVE]
  • Roda A., Fini A. Effect of nuclear hydroxy substituents on aqueous solubility and acidic strength of bile acids. Hepatology 1984; 4(5 Suppl.)72S–76S, [PUBMED], [INFOTRIEVE]
  • Roda A., Grigolo B., Minutello A., Pellicciari R., Natalini B. Physicochemical and biological properties of natural and synthetic C22 and C‐23 hydroxylated bile acids. 1990; 31: 289–298
  • Roda A., Hofmann A. F., Mysels K. J. The influence of bile salt structure on self‐association in aqueous solutions. J. Biol. Chem. 1983; 258: 6362–6370, [PUBMED], [INFOTRIEVE]
  • Russell D. W. The enzymes, regulation, and genetics of bile acid synthesis. Ann. Rev. Biochem. 2003; 72: 137–174, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Saini S. P., Sonoda J., Xu L., Toma D., Uppal H., Mu Y., Ren S., Moore D. D., Evans R. M., Xie W. A novel constitutive androstane receptor‐mediated CYP3A‐independent pathway of bile acid detoxification. Mol. Pharmacol. 2004; 65: 292–300, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Schoenfield L. J., Lachin J. M., the Steering Committee, the National Cooperative Gallstone Study Group. Chenodiol (chenodeoxycholic acid) for dissolution of gallstones: the National Cooperative Gallstone Study. Ann. Intern. Med. 1981; 95: 257–282, [PUBMED], [INFOTRIEVE]
  • Schwenk M., Hofmann A. F., Carlson G. L., Carter J. A., Coulston F., Greim H. Bile acid conjugation in the chimpanzee: effective sulfation of lithocholic acid. Arch. Toxicol. 1978; 40: 109–118, [PUBMED], [INFOTRIEVE]
  • Stedman C. A., Robertson G. R., Coulter S. A., Liddle C. Feed‐forward regulation of bile acid detoxification by CYP3A4; studies in humanized transgenic mice. J. Biol. Chem. 2003, In press
  • Stellaard F., Klein P. D., Hofmann A. F., Lachin J. M. Mass spectrometry identification of biliary bile acids in bile from gallstone patients before and during treatment with chenodeoxycholic acid. An ancillary study of the National Cooperative Gallstone Study (NCGS). J. Lab. Clin. Med. 1985; 105: 504–513, [PUBMED], [INFOTRIEVE]
  • Thistle J. L., Schoenfield L. J. Induced alterations in composition of bile of persons having cholelithiasis. Gastroenterology 1971; 61: 488–496, [PUBMED], [INFOTRIEVE]
  • Thistle J. L., LaRusso N. F., Hofmann A. F., Turcotte J., Carlson G. L., Ott B. J. Differing effects of ursodeoxycholic or chenodeoxycholic acid on biliary cholesterol saturation and bile acid metabolism in man: a dose response study. Dig. Dis. Sci. 1982; 12: 161–168
  • van Berge Henegouwen G. P., Brandt K.‐H., Eyssen H., Parmentier G. Sulfated and unsulfated bile acids in serum, bile, and urine of patients with cholestasis. Gut 1976; 17: 861–869, [PUBMED], [INFOTRIEVE]
  • Vlahcevic Z. R., Bell C. C., Jr., Buhac I., Farrar J. T., Swell L. Diminished bile acid pool size in patients with gallstones. Gastroenterology 1970; 59: 165–173, [PUBMED], [INFOTRIEVE]
  • Wang H., LeCluyse E. L. Role of orphan nuclear receptors in the regulation of drug‐metabolizing enzymes. Clin. Pharmacokinet. 2003; 42: 1331–1357, [PUBMED], [INFOTRIEVE]
  • Webster K. H., Lancaster M. C., Hofmann A. F., Wease D. F., Baggenstoss A. H. Influence on primary bile acid feeding on cholesterol metabolism and hepatic function in the rhesus monkey. Mayo Clin. Proc. 1975; 50: 134–138, [PUBMED], [INFOTRIEVE]
  • Willson T. M., Jones S. A., Moore J. T., Kliewer S. A. Chemical genomics: functional analysis of orphan nuclear receptors in the regulation of bile acid metabolism. Med. Res. Rev. 2001; 21: 513–522, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Yeh H.‐Z., Schteingart C. D., Hagey L. R., Ton‐Nu H.‐T., Bolder U., Gavrilkina M. A., Steinbach J. H., Hofmann A. F. Effect of side chain length on biotransformation, hepatic transport, and choleretic properties of chenodeoxycholyl homologues in the rodent: studies with Dinor‐ (C22), Nor‐ (C23) and Chenodeoxycholic acid (C24). Hepatology 1997; 26: 374–385, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Yoon Y. B., Hagey L. R., Hofmann A. F., Gurantz D., Michelotti E. L., Steinbach J. L. Effect of side‐chain shortening on the physiological properties of bile acids: hepatic transport and effect on biliary secretion of 23‐nor‐ursodeoxycholate in rodents. Gastroenterology 1986; 90: 837–852, [PUBMED], [INFOTRIEVE]
  • Yousef I. M., Bouchard G., Tuchweber B., Plaa G. L. Monohydroxy bile acid induced cholestasis: role of biotransformation. Drug Metab. Rev. 1997; 29: 167–181, [PUBMED], [INFOTRIEVE]
  • Yu J., Lo J. L., Huang L., Zhao A., Metzger E., Adams A., Meinke P. T., Wright S. D., Cui J. Lithocholic acid decreases expression of bile salt export pump through farnesoid X receptor antagonist activity. J. Biol. Chem. 2002; 277: 31441–31447, [PUBMED], [INFOTRIEVE], [CROSSREF]
  • Zaki F. G., Carey J. B., Jr., Hoffbauer F. W., Nwokolo C. Biliary reaction and choledocholithiasis induced in the rat by lithocholic acid. J. Lab. Clin. Med. 1967; 69: 737–748, [PUBMED], [INFOTRIEVE]

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.