808
Views
10
CrossRef citations to date
0
Altmetric
Reviews

Hepatic drug transporters: the journey so far

, , , &
Pages 201-216 | Received 05 Oct 2015, Accepted 11 Dec 2015, Published online: 08 Jan 2016

References

  • Papers of special note have been highlighted as:
  • • of interest
  • •• of considerable interest
  • Hediger MA, Clemencon B, Burrier RE, et al. The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol Aspects Med. 2013;34(2–3):95–107.
  • Nigam SK. What do drug transporters really do? Nat Rev Drug Discov. 2015;14(1):29–44.
  • Kock K, Ferslew BC, Netterberg I, et al. Risk factors for development of cholestatic drug-induced liver injury: inhibition of hepatic basolateral bile acid transporters multidrug resistance-associated proteins 3 and 4. Drug Metab Dispos. 2014;42(4):665–674.
  • Yoshida K, Maeda K, Sugiyama Y. Transporter-mediated drug–drug interactions involving OATP substrates: predictions based on in vitro inhibition studies. Clin Pharmacol Ther. 2012;91(6):1053–1064.
  • Fenner KS, Jones HM, Ullah M, et al. The evolution of the OATP hepatic uptake transport protein family in DMPK sciences: from obscure liver transporters to key determinants of hepatobiliary clearance. Xenobiotica. 2012;42(1):28–45.
  • van de Steeg E, Stranecky V, Hartmannova H, et al. Complete OATP1B1 and OATP1B3 deficiency causes human Rotor syndrome by interrupting conjugated bilirubin reuptake into the liver. J Clin Invest. 2012;122(2):519–528.
  • Jedlitschky G, Hoffmann U, Kroemer HK. Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Expert Opin Drug Metab Toxicol. 2006;2(3):351–366.
  • Benet LZ. The role of BCS (biopharmaceutics classification system) and BDDCS (biopharmaceutics drug disposition classification system) in drug development. J Pharm Sci. 2013;102(1):34–42.
  • Olah M, Rad R, Ostopovici L, et al. WOMAT and WOMBAT-PK: bioactivity databases for lead and drug discovery. In: Chemical biology. Weinheim: Wiley-VCH Verlag GmbH; 2007. p. 760–786.
  • Huang SM, Zhang L, Giacomini KM. The International Transporter Consortium: a collaborative group of scientists from academia, industry, and the FDA. Clin Pharmacol Ther. 2010;87(1):32–36.

• A summary of transporter regulatory guidelines.

  • Generaux GT, Bonomo FM, Johnson M, et al. Impact of SLCO1B1 (OATP1B1) and ABCG2 (BCRP) genetic polymorphisms and inhibition on LDL-C lowering and myopathy of statins. Xenobiotica. 2011;41(8):639–651.
  • (CDER) Cf DEaR. Guidance for industry. drug interaction studies — study design, data analysis, implications for dosing, and labeling recommendations. Clinical Pharmacology. U.S. Department of Health and Human Services Food and Drug Administration Center for Drug Evaluation and Research (CDER); 2012 [cited 2015 Dec 24]. Available from: http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM292362.pdf
  • European Medical Agency. Guideline on the investigation of drug interactions. (CPMP/EWP/560/95/Rev. 1 Corr. 2). Committee for Human Medicinal Products (CHMP); 2012 [cited 2015 Dec 24]. Available form: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2012/07/WC500129606.pdf
  • Giacomini KM, Balimane PV, Cho SK, et al. International Transporter Consortium commentary on clinically important transporter polymorphisms. Clin Pharmacol Ther. 2013;94(1):23–26.
  • Maeda K, Sugiyama Y. Transporter biology in drug approval: regulatory aspects. Mol Aspects Med. 2013;34(2–3):711–718.
  • Gu Q, Paulose-Ram R, Burt VL, et al. Prescription cholesterol-lowering medication use in adults aged 40 and over: United States, 2003–2012. NCHS Data Brief. 2014;177:1–8.
  • Elsby R, Hilgendorf C, Fenner K. Understanding the critical disposition pathways of statins to assess drug-drug interaction risk during drug development: it’s not just about OATP1B1. Clin Pharmacol Ther. 2012;92(5):584–598.
  • Varma MV, Bi YA, Kimoto E, et al. Quantitative prediction of transporter- and enzyme-mediated clinical drug-drug interactions of organic anion-transporting polypeptide 1B1 substrates using a mechanistic net-effect model. J Pharmacol Exp Ther. 2014;351(1):214–223.
  • National Statistics HaSCIC. National statistics prescription cost analysis - England, 2010 [NS]. Health and Social Care Information Centre, Prescribing Support Unit; 2011 [cited 2015 Dec 24]. Available from: http://www.hscic.gov.uk/pubs/prescostanalysis2010
  • Karlgren M, Vildhede A, Norinder U, et al. Classification of inhibitors of hepatic organic anion transporting polypeptides (OATPs): influence of protein expression on drug-drug interactions. J Med Chem. 2012;55(10):4740–4763.
  • Jigorel E, Le Vee M, Boursier-Neyret C, et al. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab Dispos. 2006;34(10):1756–1763.
  • Williamson B, Soars AC, Owen A, et al. Dissecting the relative contribution of OATP1B1-mediated uptake of xenobiotics into human hepatocytes using siRNA. Xenobiotica. 2013;43(10):920–931.
  • Aszalos A. Drug-drug interactions affected by the transporter protein, P-glycoprotein (ABCB1, MDR1) I. Preclinical aspects. Drug Discov Today. 2007;12(19–20):833–837.
  • Neumanova Z, Cerveny L, Ceckova M, et al. Interactions of tenofovir and tenofovir disoproxil fumarate with drug efflux transporters ABCB1, ABCG2, and ABCC2; role in transport across the placenta. Aids. 2014;28(1):9–17.
  • Wang H, Jin G, Wang H, et al. Genetic susceptibility of lung cancer associated with common variants in the 3’ untranslated regions of the adenosine triphosphate-binding cassette B1 (ABCB1) and ABCC1 candidate transporter genes for carcinogen export. Cancer. 2009;115(3):595–607.
  • Zhang W, Yu BN, He YJ, et al. Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin Chim Acta. 2006;373(1–2):99–103.
  • Zamber CP, Lamba JK, Yasuda K, et al. Natural allelic variants of breast cancer resistance protein (BCRP) and their relationship to BCRP expression in human intestine. Pharmacogenetics. 2003;13(1):19–28.
  • Goldkind L, Laine L. A systematic review of NSAIDs withdrawn from the market due to hepatotoxicity: lessons learned from the bromfenac experience. Pharmacoepidemiol Drug Saf. 2006;15(4):213–220.
  • Cusatis G, Gregorc V, Li J, et al. Pharmacogenetics of ABCG2 and adverse reactions to gefitinib. J Natl Cancer Inst. 2006;98(23):1739–1742.
  • Hirano M, Maeda K, Shitara Y, et al. Drug-drug interaction between pitavastatin and various drugs via OATP1B1. Drug Metab Dispos. 2006;34(7):1229–1236.
  • Pauli-Magnus C, Meier PJ, Stieger B. Genetic determinants of drug-induced cholestasis and intrahepatic cholestasis of pregnancy. Semin Liver Dis. 2010;30(2):147–159.
  • Russmann S, Jetter A, Kullak-Ublick GA. Pharmacogenetics of drug-induced liver injury. Hepatology. 2010;52(2):748–761.
  • Harris HW, Davis BR, Vitale GC. Cholecystectomy after endoscopic sphincterotomy for common bile duct stones: is surgery necessary? Surg Innov. 2005;12(3):187–194.
  • Rodrigues AD, Lai Y, Cvijic ME, et al. Drug-induced perturbations of the bile acid pool, cholestasis, and hepatotoxicity: mechanistic considerations beyond the direct inhibition of the bile salt export pump. Drug Metab Dispos. 2014;42(4):566–574.
  • Dawson S, Stahl S, Paul N, et al. In vitro inhibition of the bile salt export pump correlates with risk of cholestatic drug-induced liver injury in humans. Drug Metab Dispos. 2012;40(1):130–138.
  • Morgan RE, Trauner M, Van Staden CJ, et al. Interference with bile salt export pump function is a susceptibility factor for human liver injury in drug development. Toxicol Sci. 2010;118(2):485–500.
  • Glavinas H, Mehn D, Jani M, et al. Utilization of membrane vesicle preparations to study drug-ABC transporter interactions. Expert Opin Drug Metab Toxicol. 2008;4(6):721–732.
  • Liang Y, Li S, Chen L. The physiological role of drug transporters. Protein Cell. 2015;6(5):334–350.
  • Zhang YJ. In silico technologies in drug design, discovery and development. Curr Top Med Chem. 2010;10(6):617–618.
  • Kunze A, Huwyler J, Camenisch G, et al. Prediction of organic anion-transporting polypeptide 1B1- and 1B3-mediated hepatic uptake of statins based on transporter protein expression and activity data. Drug Metab Dispos. 2014;42(9):1514–1521.
  • Karlgren M, Ahlin G, Bergstrom CA, et al. In vitro and in silico strategies to identify OATP1B1 inhibitors and predict clinical drug-drug interactions. Pharm Res. 2012;29(2):411–426.

•• Details the approaches available to delineate OATP1B1 inhibitors and associated drug–drug interaction (DDI) risk.

  • Ito K, Houston JB. Prediction of human drug clearance from in vitro and preclinical data using physiologically based and empirical approaches. Pharm Res. 2005;22(1):103–112.
  • Ismair MG, Stieger B, Cattori V, et al. Hepatic uptake of cholecystokinin octapeptide by organic anion-transporting polypeptides OATP4 and OATP8 of rat and human liver. Gastroenterology. 2001;121(5):1185–1190.
  • Kullak-Ublick GA, Ismair MG, Stieger B, et al. Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology. 2001;120(2):525–533.
  • Paine SW, Parker AJ, Gardiner P, et al. Prediction of the pharmacokinetics of atorvastatin, cerivastatin, and indomethacin using kinetic models applied to isolated rat hepatocytes. Drug Metab Dispos. 2008;36(7):1365–1374.
  • Poirier A, Funk C, Scherrmann JM, et al. Mechanistic modeling of hepatic transport from cells to whole body: application to napsagatran and fexofenadine. Mol Pharm. 2009;6(6):1716–1733.
  • Wei L, Wang J, Thompson P, et al. Adherence to statin treatment and readmission of patients after myocardial infarction: a six year follow up study. Heart. 2002;88(3):229–233.
  • Izumi S, Nozaki Y, Komori T, et al. Substrate-dependent inhibition of organic anion transporting polypeptide 1B1: comparative analysis with prototypical probe substrates estradiol-17beta-glucuronide, estrone-3-sulfate, and sulfobromophthalein. Drug Metab Dispos. 2013;41(10):1859–1866.
  • Amundsen R, Christensen H, Zabihyan B, et al. Cyclosporine A, but not tacrolimus, shows relevant inhibition of organic anion-transporting protein 1B1-mediated transport of atorvastatin. Drug Metab Dispos. 2010;38(9):1499–1504.
  • Shitara Y, Takeuchi K, Nagamatsu Y, et al. Long-lasting inhibitory effects of cyclosporin A, but not tacrolimus, on OATP1B1- and OATP1B3-mediated uptake. Drug Metab Pharmacokinet. 2012;27(4):368–378.
  • Cui Y, Konig J, Leier I, et al. Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J Biol Chem. 2001;276(13):9626–9630.
  • Kopplow K, Letschert K, Konig J, et al. Human hepatobiliary transport of organic anions analyzed by quadruple-transfected cells. Mol Pharmacol. 2005;68(4):1031–1038.
  • Kotani N, Maeda K, Debori Y, et al. Expression and transport function of drug uptake transporters in differentiated HepaRG cells. Mol Pharm. 2012;9(12):3434–3441.
  • Soars MG, Grime K, Sproston JL, et al. Use of hepatocytes to assess the contribution of hepatic uptake to clearance in vivo. Drug Metab Dispos. 2007;35(6):859–865.
  • Yue W, Abe K, Brouwer KL. Knocking down breast cancer resistance protein (Bcrp) by adenoviral vector-mediated RNA interference (RNAi) in sandwich-cultured rat hepatocytes: a novel tool to assess the contribution of Bcrp to drug biliary excretion. Mol Pharm. 2009;6(1):134–143.
  • Powell J, Farasyn T, Kock K, et al. Novel mechanism of impaired function of organic anion-transporting polypeptide 1B3 in human hepatocytes: post-translational regulation of OATP1B3 by protein kinase C activation. Drug Metab Dispos. 2014;42(11):1964–1970.
  • Varma MV, Scialis RJ, Lin J, et al. Mechanism-based pharmacokinetic modeling to evaluate transporter-enzyme interplay in drug interactions and pharmacogenetics of glyburide. AAPS J. 2014;16(4):736–748.
  • Olsavsky Goyak KM, Laurenzana EM, Omiecinski CJ. Hepatocyte differentiation. Methods Mol Biol. 2010;640:115–138.
  • Pfeifer ND, Bridges AS, Ferslew BC, et al. Hepatic basolateral efflux contributes significantly to rosuvastatin disposition II: characterization of hepatic elimination by basolateral, biliary, and metabolic clearance pathways in rat isolated perfused liver. J Pharmacol Exp Ther. 2013;347(3):737–745.
  • Pfeifer ND, Yang K, Brouwer KL. Hepatic basolateral efflux contributes significantly to rosuvastatin disposition I: characterization of basolateral versus biliary clearance using a novel protocol in sandwich-cultured hepatocytes. J Pharmacol Exp Ther. 2013;347(3):727–736.
  • Yu AM. Small interfering RNA in drug metabolism and transport. Curr Drug Metab. 2007;8(7):700–708.
  • Liao M, Raczynski AR, Chen M, et al. Inhibition of hepatic organic anion-transporting polypeptide by RNA interference in sandwich-cultured human hepatocytes: an in vitro model to assess transporter-mediated drug-drug interactions. Drug Metab Dispos. 2010;38(9):1612–1622.
  • Shin N, Oh J, Lee Y. Role of drug transporters: an overview based on knockout animal model studies. J Pharm Investig. 2015;42:2.
  • Lorico A, Nesland J, Emilsen E, et al. Role of the multidrug resistance protein 1 gene in the carcinogenicity of aflatoxin B1: investigations using mrp1-null mice. Toxicology. 2002;171(2–3):201–205.
  • Durmus S, Lozano-Mena G, Van Esch A, et al. Preclinical mouse models to study human OATP1B1- and OATP1B3-mediated drug-drug interactions in vivo. Mol Pharm. 2015;12(12):4259–4269.
  • Mankowski DC, Laddison KJ, Christopherson PA, et al. Molecular cloning, expression, and characterization of CYP2D17 from cynomolgus monkey liver. Arch Biochem Biophys. 1999;372(1):189–196.
  • Chu X, Shih SJ, Shaw R, et al. Evaluation of cynomolgus monkeys for the identification of endogenous biomarkers for hepatic transporter inhibition and as a translatable model to predict pharmacokinetic interactions with statins in humans. Drug Metab Dispos. 2015;43(6):851–863.
  • Riley RJ, McGinnity DF, Austin RP. A unified model for predicting human hepatic, metabolic clearance from in vitro intrinsic clearance data in hepatocytes and microsomes. Drug Metab Dispos. 2005;33(9):1304–1311.
  • Obach RS. Nonspecific binding to microsomes: impact on scale-up of in vitro intrinsic clearance to hepatic clearance as assessed through examination of warfarin, imipramine, and propranolol. Drug Metab Dispos. 1997;25(12):1359–1369.
  • Ito K, Houston JB. Comparison of the use of liver models for predicting drug clearance using in vitro kinetic data from hepatic microsomes and isolated hepatocytes. Pharm Res. 2004;21(5):785–792.
  • Rummler S. [Giant tumor of the vulva. Patient went from doctor to doctor]. MMW Fortschr Med. 2007;149(24):5.
  • Soars MG, Webborn PJ, Riley RJ. Impact of hepatic uptake transporters on pharmacokinetics and drug-drug interactions: use of assays and models for decision making in the pharmaceutical industry. Mol Pharm. 2009;6(6):1662–1677.

• Pivotal publication outlining the clinical impact of uptake transporters (DDIs) and consideration of methods for use in modern-day drug discovery.

  • Chu X, Korzekwa K, Elsby R, et al. Intracellular drug concentrations and transporters: measurement, modeling, and implications for the liver. Clin Pharmacol Ther. 2013;94(1):126–141.
  • Lundquist P, Loof J, Fagerholm U, et al. Prediction of in vivo rat biliary drug clearance from an in vitro hepatocyte efflux model. Drug Metab Dispos. 2014;42(3):459–468.
  • Liu L, Pang KS. An integrated approach to model hepatic drug clearance. Eur J Pharm Sci. 2006;29(3–4):215–230.
  • Miyauchi S, Sawada Y, Iga T, et al. Comparison of the hepatic uptake clearances of fifteen drugs with a wide range of membrane permeabilities in isolated rat hepatocytes and perfused rat livers. Pharm Res. 1993;10(3):434–440.
  • Poirier A, Cascais AC, Funk C, et al. Prediction of pharmacokinetic profile of valsartan in human based on in vitro uptake transport data. J Pharmacokinet Pharmacodyn. 2009;36(6):585–611.
  • Nakakariya M, Ono M, Amano N, et al. In vivo biliary clearance should be predicted by intrinsic biliary clearance in sandwich-cultured hepatocytes. Drug Metab Dispos. 2012;40(3):602–609.
  • Soars MG, Barton P, Ismair M, et al. The development, characterization, and application of an OATP1B1 inhibition assay in drug discovery. Drug Metab Dispos. 2012;40(8):1641–1648.
  • Badolo L, Rasmussen LM, Hansen HR, et al. Screening of OATP1B1/3 and OCT1 inhibitors in cryopreserved hepatocytes in suspension. Eur J Pharm Sci. 2010;40(4):282–288.
  • Feng B, Varma MV, Costales C, et al. In vitro and in vivo approaches to characterize transporter-mediated disposition in drug discovery. Expert Opin Drug Discov. 2014;9(8):873–890.
  • Huang L, Berry L, Ganga S, et al. Relationship between passive permeability, efflux, and predictability of clearance from in vitro metabolic intrinsic clearance. Drug Metab Dispos. 2010;38(2):223–231.
  • Sohlenius-Sternbeck AK, Jones C, Ferguson D, et al. Practical use of the regression offset approach for the prediction of in vivo intrinsic clearance from hepatocytes. Xenobiotica. 2012;42(9):841–853.
  • Yabe Y, Galetin A, Houston JB. Kinetic characterization of rat hepatic uptake of 16 actively transported drugs. Drug Metab Dispos. 2011;39(10):1808–1814.
  • Barton P, Riley RJ. A new paradigm for navigating compound property related drug attrition. Drug Discov Today. 2015 September 25. [Epub ahead of print]
  • Soars MG, Barton P, Elkin LL, et al. Application of an in vitro OAT assay in drug design and optimization of renal clearance. Xenobiotica. 2014;44(7):657–665.
  • Varma MV, Steyn SJ, Allerton C, et al. Predicting clearance mechanism in drug discovery: extended clearance classification system (ECCS). Pharm Res. 2015;32(12):3785–3802.

•• Incorporation of transporter and enzyme parameters into an extended model to predict drug clearance.

  • Hughes JD, Blagg J, Price DA, et al. Physiochemical drug properties associated with in vivo toxicological outcomes. Bioorg Med Chem Lett. 2008;18(17):4872–4875.
  • Muthas D, Boyer S, Hasselgren C. A critical assessment of modeling safety-related drug attrition. Med Chem Commun. 2013;4(7):1058–1065.
  • Deng D, Xu C, Sun P, et al. Crystal structure of the human glucose transporter GLUT1. Nature. 2014;510(7503):121–125.
  • Shintre CA, Pike AC, Li Q, et al. Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states. Proc Natl Acad Sci U S A. 2013;110(24):9710–9715.
  • Boccard J, Bajot F, Di Pietro A, et al. A 3D linear solvation energy model to quantify the affinity of flavonoid derivatives toward P-glycoprotein. Eur J Pharm Sci. 2009;36(2–3):254–264.
  • Broccatelli F, Carosati E, Neri A, et al. A novel approach for predicting P-glycoprotein (ABCB1) inhibition using molecular interaction fields. J Med Chem. 2011;54(6):1740–1751.
  • Gombar VK, Polli JW, Humphreys JE, et al. Predicting P-glycoprotein substrates by a quantitative structure-activity relationship model. J Pharm Sci. 2004;93(4):957–968.
  • Hillgren KM, Keppler D, Zur AA, et al. Emerging transporters of clinical importance: an update from the International Transporter Consortium. Clin Pharmacol Ther. 2013;94(1):52–63.
  • 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(5):725–734.
  • Dolghih E, Bryant C, Renslo AR, et al. Predicting binding to p-glycoprotein by flexible receptor docking. PLoS Comput Biol. 2011;7(6):e1002083.
  • Guthrie B, Makubate B, Hernandez-Santiago V, et al. The rising tide of polypharmacy and drug-drug interactions: population database analysis 1995–2010. BMC Med. 2015;13:74.
  • Shugarts S, Benet LZ. The role of transporters in the pharmacokinetics of orally administered drugs. Pharm Res. 2009;26(9):2039–2054.
  • Varma MV, Lin J, Bi YA, et al. Quantitative rationalization of gemfibrozil drug interactions: consideration of transporters-enzyme interplay and the role of circulating metabolite gemfibrozil 1-O-beta-glucuronide. Drug Metab Dispos. 2015;43(7):1108–1118.
  • Zheng LS, Wang F, Li YH, et al. Vandetanib (Zactima, ZD6474) antagonizes ABCC1- and ABCG2-mediated multidrug resistance by inhibition of their transport function. PLoS One. 2009;4(4):e5172.
  • Jonker JW, Wagenaar E, Mol CA, et al. Reduced hepatic uptake and intestinal excretion of organic cations in mice with a targeted disruption of the organic cation transporter 1 (Oct1 [Slc22a1]) gene. Mol Cell Biol. 2001;21(16):5471–5477.
  • Prueksaritanont T, Chu X, Gibson C, et al. Drug-drug interaction studies: regulatory guidance and an industry perspective. AAPS J. 2013;15(3):629–645.
  • Kusuhara H, Sugiyama Y. In vitro-in vivo extrapolation of transporter-mediated clearance in the liver and kidney. Drug Metab Pharmacokinet. 2009;24(1):37–52.
  • Godoy P, Hewitt NJ, Albrecht U, et al. Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Arch Toxicol. 2013;87(8):1315–1530.
  • Fahmi OA, Hurst S, Plowchalk D, et al. Comparison of different algorithms for predicting clinical drug-drug interactions, based on the use of CYP3A4 in vitro data: predictions of compounds as precipitants of interaction. Drug Metab Dispos. 2009;37(8):1658–1666.
  • Watanabe T, Kusuhara H, Maeda K, et al. Physiologically based pharmacokinetic modeling to predict transporter-mediated clearance and distribution of pravastatin in humans. J Pharmacol Exp Ther. 2009;328(2):652–662.
  • Jones H, Rowland-Yeo K. Basic concepts in physiologically based pharmacokinetic modeling in drug discovery and development. CPT. 2013;2:e63.
  • Jones HM, Gardner IB, Collard WT, et al. Simulation of human intravenous and oral pharmacokinetics of 21 diverse compounds using physiologically based pharmacokinetic modelling. Clin Pharmacokinet. 2011;50(5):331–347.

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.