Publication Cover
Xenobiotica
the fate of foreign compounds in biological systems
Volume 39, 2009 - Issue 8: Commemorative Issue: Professor George Gordon Gibson
547
Views
75
CrossRef citations to date
0
Altmetric
Review Article

Species differences in the hepatic effects of inducers of CYP2B and CYP4A subfamily forms: relationship to rodent liver tumour formation

Pages 582-596 | Accepted 08 Jun 2009, Published online: 21 Jul 2009

Keep up to date with the latest research on this topic with citation updates for this article.

Read on this site (7)

Tomoya Yamada, Brian G. Lake & Samuel M. Cohen. (2022) Evaluation of the human hazard of the liver and lung tumors in mice treated with permethrin based on mode of action. Critical Reviews in Toxicology 52:1, pages 1-31.
Read now
Milu T Cherian, Sergio C Chai & Taosheng Chen. (2015) Small-molecule modulators of the constitutive androstane receptor. Expert Opinion on Drug Metabolism & Toxicology 11:7, pages 1099-1114.
Read now
Matthew J. LeBaron, B. Bhaskar Gollapudi, Claire Terry, Richard Billington & Reza J. Rasoulpour. (2014) Human relevance framework for rodent liver tumors induced by the insecticide sulfoxaflor. Critical Reviews in Toxicology 44:sup2, pages 15-24.
Read now
Clifford R. Elcombe, Richard C. Peffer, Douglas C. Wolf, Jason Bailey, Remi Bars, David Bell, Russell C. Cattley, Stephen S. Ferguson, David Geter, Amber Goetz, Jay I. Goodman, Susan Hester, Abigail Jacobs, Curtis J. Omiecinski, Rita Schoeny, Wen Xie & Brian G. Lake. (2014) Mode of action and human relevance analysis for nuclear receptor-mediated liver toxicity: A case study with phenobarbital as a model constitutive androstane receptor (CAR) activator. Critical Reviews in Toxicology 44:1, pages 64-82.
Read now
Nico Scheer & C. Roland Wolf. (2013) Xenobiotic receptor humanized mice and their utility. Drug Metabolism Reviews 45:1, pages 110-121.
Read now

Articles from other publishers (68)

M. Estefanía González-Alvarez & Aileen F. Keating. (2023) Hepatic and ovarian effects of perfluorooctanoic acid exposure differ in lean and obese adult female mice. Toxicology and Applied Pharmacology 474, pages 116614.
Crossref
Michela Cantiello, Monica Carletti, Mery Giantin, Giulia Gardini, Francesca Capolongo, Paolo Cascio, Marianna Pauletto, Flavia Girolami, Mauro Dacasto & Carlo Nebbia. (2022) Induction by Phenobarbital of Phase I and II Xenobiotic-Metabolizing Enzymes in Bovine Liver: An Overall Catalytic and Immunochemical Characterization. International Journal of Molecular Sciences 23:7, pages 3564.
Crossref
Shengzhong Su, Laura J. Billy, Sue Chang, Frank J. Gonzalez, Andrew D. Patterson & Jeffrey M. Peters. (2022) The role of mouse and human peroxisome proliferator-activated receptor-α in modulating the hepatic effects of perfluorooctane sulfonate in mice. Toxicology 465, pages 153056.
Crossref
Maike Gährs & Dieter Schrenk. (2021) Suppression of apoptotic signaling in rat hepatocytes by non-dioxin-like polychlorinated biphenyls depends on the receptors CAR and PXR. Toxicology 464, pages 153023.
Crossref
Lynea Murphy, Matthew J. LeBaron, Kamin Johnson, Reza J. Rasoulpour, Xiujuan Wang & Jessica LaRocca. (2021) Bridging Sex-Specific Differences in the CAR-Mediated Hepatocarcinogenesis of Nitrapyrin Using Molecular and Apical Endpoints. Frontiers in Toxicology 3.
Crossref
Tomoya Yamada. (2021) Application of humanized mice to toxicology studies: Evaluation of the human relevance of the mode of action for rodent liver tumor formation by activators of the constitutive androstane receptor (CAR). Journal of Toxicologic Pathology 34:4, pages 283-297.
Crossref
Katherine Roth, Zunaira Imran, Wanqing Liu & Michael C. Petriello. (2020) Diet as an Exposure Source and Mediator of Per- and Polyfluoroalkyl Substance (PFAS) Toxicity. Frontiers in Toxicology 2.
Crossref
Ramona Nudischer, Kasper Renggli, Cristina Bertinetti-Lapatki, Jean-Christophe Hoflack, Nicholas Flint, Sabine Sewing, Lykke Pedersen, Simone Schadt, Larry G Higgins, Audrey Vardy, Barbara Lenz, Laurent Gand, Franziska Boess, Barbara M Elcombe, Andreas Hierlemann & Adrian B Roth. (2020) Combining In Vivo and Organotypic In Vitro Approaches to Assess the Human Relevance of Basimglurant (RG7090), a Potential CAR Activator. Toxicological Sciences 176:2, pages 329-342.
Crossref
Brian G. Lake, Roger J. Price, Mary P. Scott, Lynsey R. Chatham, Audrey Vardy & Thomas G. Osimitz. (2020) Piperonyl butoxide: Mode of action analysis for mouse liver tumour formation and human relevance. Toxicology 439, pages 152465.
Crossref
Vicky Nicolaidou & Costas Koufaris. (2020) Application of transcriptomic and microRNA profiling in the evaluation of potential liver carcinogens. Toxicology and Industrial Health 36:5, pages 386-397.
Crossref
Miwa Kondo, Hiroko Kikumoto, Thomas G Osimitz, Samuel M Cohen, Brian G Lake & Tomoya Yamada. (2020) An Evaluation of the Human Relevance of the Liver Tumors Observed in Female Mice Treated With Permethrin Based on Mode of Action. Toxicological Sciences 175:1, pages 50-63.
Crossref
Manuela Goettel, Ivana Fegert, Naveed Honarvar, Audrey Vardy, Corinne Haines, Lynsey R. Chatham & Brian G. Lake. (2020) Comparative studies on the effects of sodium phenobarbital and two other constitutive androstane receptor (CAR) activators on induction of cytochrome P450 enzymes and replicative DNA synthesis in cultured hepatocytes from wild type and CAR knockout rats. Toxicology 433-434, pages 152394.
Crossref
Limin Zhang, Bipin Rimal, Robert G. Nichols, Yuan Tian, Philip B. Smith, Emmanuel Hatzakis, Shu-Ching Chang, John L. Butenhoff, Jeffrey M. Peters & Andrew D. Patterson. (2020) Perfluorooctane sulfonate alters gut microbiota-host metabolic homeostasis in mice. Toxicology 431, pages 152365.
Crossref
James E. Sidaway, Terry C. Orton, Kassiani Kalaitzi, Huw B. Jones, Alison Foster & Brian G. Lake. (2020) Analysis of β-catenin gene mutations and gene expression in liver tumours of C57BL/10J mice produced by chronic administration of sodium phenobarbital. Toxicology 430, pages 152343.
Crossref
Christiane Wiemann, Manuela Goettel, Audrey Vardy, Barbara M. Elcombe, Clifford R. Elcombe, Lynsey R. Chatham, Hongbing Wang, Linhao Li, Roland Buesen, Naveed Honarvar, Silke Treumann, Heike Marxfeld, Sibylle Groeters & Brian G. Lake. (2019) Metazachlor: Mode of action analysis for rat liver tumour formation and human relevance. Toxicology 426, pages 152282.
Crossref
Eleni A. Rekka, Panos N. Kourounakis & Maria Pantelidou. (2019) Xenobiotic Metabolising Enzymes: Impact on Pathologic Conditions, Drug Interactions and Drug Design. Current Topics in Medicinal Chemistry 19:4, pages 276-291.
Crossref
Miwa Kondo, Kaori Miyata, Hirohisa Nagahori, Kayo Sumida, Thomas G Osimitz, Samuel M Cohen, Brian G Lake & Tomoya Yamada. (2019) Involvement of Peroxisome Proliferator-Activated Receptor-Alpha in Liver Tumor Production by Permethrin in the Female Mouse. Toxicological Sciences 168:2, pages 572-596.
Crossref
Brian G. Lake. (2018) Human relevance of rodent liver tumour formation by constitutive androstane receptor (CAR) activators. Toxicology Research 7:4, pages 697-717.
Crossref
Tomoya Yamada. (2018) Case examples of an evaluation of the human relevance of the pyrethroids/pyrethrins-induced liver tumours in rodents based on the mode of action. Toxicology Research 7:4, pages 681-696.
Crossref
Richard C. Peffer, Matthew J. LeBaron, Michael Battalora, Werner H. Bomann, Christoph Werner, Manoj Aggarwal, Rocky R. Rowe & Helen Tinwell. (2018) Minimum datasets to establish a CAR-mediated mode of action for rodent liver tumors. Regulatory Toxicology and Pharmacology 96, pages 106-120.
Crossref
Corinne Haines, Lynsey R. Chatham, Audrey Vardy, Clifford R. Elcombe, John R. Foster & Brian G. Lake. (2018) Comparison of the hepatic and thyroid gland effects of sodium phenobarbital in wild type and constitutive androstane receptor (CAR) knockout rats and pregnenolone-16α-carbonitrile in wild type and pregnane X receptor (PXR) knockout rats. Toxicology 400-401, pages 20-27.
Crossref
Richard C Peffer, David E Cowie, Richard A Currie & Daniel J Minnema. (2018) Sedaxane—Use of Nuclear Receptor Transactivation Assays, Toxicogenomics, and Toxicokinetics as Part of a Mode of Action Framework for Rodent Liver Tumors. Toxicological Sciences 162:2, pages 582-598.
Crossref
Corinne Haines, Barbara M. Elcombe, Lynsey R. Chatham, Audrey Vardy, Larry G. Higgins, Clifford R. Elcombe & Brian G. Lake. (2018) Comparison of the effects of sodium phenobarbital in wild type and humanized constitutive androstane receptor (CAR)/pregnane X receptor (PXR) mice and in cultured mouse, rat and human hepatocytes. Toxicology 396-397, pages 23-32.
Crossref
Thamil Selvee Ramasamy, Agnes Lee Chen Ong & Wei Cui. 2018. Novel Biomaterials for Regenerative Medicine. Novel Biomaterials for Regenerative Medicine 41 66 .
Yu Okuda, Masahiko Kushida, Kayo Sumida, Hirohisa Nagahori, Yoshimasa Nakamura, Hashihiro Higuchi, Satoshi Kawamura, Brian G. Lake, Samuel M. Cohen & Tomoya Yamada. (2017) Editor’s Highlight: Mode of Action Analysis for Rat Hepatocellular Tumors Produced by the Synthetic Pyrethroid Momfluorothrin: Evidence for Activation of the Constitutive Androstane Receptor and Mitogenicity in Rat Hepatocytes. Toxicological Sciences 158:2, pages 412-430.
Crossref
Christopher J. Choi, Erik K. Rushton, Audrey Vardy, Larry Higgins, Andrea Augello & Ralph J. Parod. (2017) Mode of action and human relevance of THF-induced mouse liver tumors. Toxicology Letters 276, pages 138-143.
Crossref
Hassaan Mehboob Awan, Abdullah Shah, Farooq Rashid & Ge Shan. (2017) Primate-specific Long Non-coding RNAs and MicroRNAs. Genomics, Proteomics & Bioinformatics 15:3, pages 187-195.
Crossref
Ayako Ohara, Yasuhiko Takahashi, Miwa Kondo, Yu Okuda, Shuji Takeda, Masahiko Kushida, Kentaro Kobayashi, Kayo Sumida & Tomoya Yamada. (2017) Candidate genes responsible for early key events of phenobarbital-promoted mouse hepatocellular tumorigenesis based on differentiation of regulating genes between wild type mice and humanized chimeric mice. Toxicology Research 6:6, pages 795-813.
Crossref
Yan Li, Hongmei Mao, Yanfeng Xu, Xiaocen Li, Lishan Pan, Xin Wu, Yang Li, Yi Li & Jun He. (2017) Application research on PPARα-transgenic mice in preclinical safety evaluation of gemfibrozil. Toxicology Research 6:1, pages 98-104.
Crossref
Jessica L. LaRocca, Reza J. Rasoulpour, B. Bhaskar Gollapudi, David L. Eisenbrandt, Lynea A. Murphy & Matthew J. LeBaron. (2017) Integration of novel approaches demonstrates simultaneous metabolic inactivation and CAR-mediated hepatocarcinogenesis of a nitrification inhibitor. Toxicology Reports 4, pages 586-597.
Crossref
B.J. Hughes, J. Thomas, A.M. Lynch, S.J. Borghoff, S. Green, T. Mensing, S.S. Sarang & M.J. LeBaron. (2016) Methyl isobutyl ketone-induced hepatocellular carcinogenesis in B6C3F1 mice: A constitutive androstane receptor (CAR)-mediated mode of action. Regulatory Toxicology and Pharmacology 81, pages 421-429.
Crossref
Sergio C. Chai, Milu T. Cherian, Yue-Ming Wang & Taosheng Chen. (2016) Small-molecule modulators of PXR and CAR. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1859:9, pages 1141-1154.
Crossref
Ann E. Bradley, Joanna L. Shoenfelt & Judi L. Durda. (2016) Carcinogenicity and mode of action evaluation for alpha-hexachlorocyclohexane: Implications for human health risk assessment. Regulatory Toxicology and Pharmacology 76, pages 152-173.
Crossref
Costas Koufaris. (2016) Human and primate-specific microRNAs in cancer: Evolution, and significance in comparison with more distantly-related research models. BioEssays 38:3, pages 286-294.
Crossref
Kazunori Kuwata, Kaoru Inoue, Ryohei Ichimura, Miwa Takahashi, Yukio Kodama & Midori Yoshida. (2016) Constitutive active/androstane receptor, peroxisome proliferator-activated receptor α, and cytotoxicity are involved in oxadiazon-induced liver tumor development in mice. Food and Chemical Toxicology 88, pages 75-86.
Crossref
Nico Scheer & Ian D. Wilson. (2016) A comparison between genetically humanized and chimeric liver humanized mouse models for studies in drug metabolism and toxicity. Drug Discovery Today 21:2, pages 250-263.
Crossref
Samuel M. Cohen & Lora L. Arnold. (2016) Critical role of toxicologic pathology in a short-term screen for carcinogenicity. Journal of Toxicologic Pathology 29:4, pages 215-227.
Crossref
Brian G. Lake & Roger J. Price. 2015. New Horizons in Predictive Drug Metabolism and Pharmacokinetics. New Horizons in Predictive Drug Metabolism and Pharmacokinetics 309 332 .
Brian G Lake, Roger J Price & Thomas G Osimitz. (2015) Mode of action analysis for pesticide-induced rodent liver tumours involving activation of the constitutive androstane receptor: relevance to human cancer risk. Pest Management Science 71:6, pages 829-834.
Crossref
. 2002. The MAK‐Collection for Occupational Health and Safety. The MAK‐Collection for Occupational Health and Safety 1 45 .
Tomoya Yamada, Hiroko Kikumoto, Brian G. Lake & Satoshi Kawamura. (2015) Lack of effect of metofluthrin and sodium phenobarbital on replicative DNA synthesis and Ki-67 mRNA expression in cultured human hepatocytes. Toxicology Research 4:4, pages 901-913.
Crossref
Tomoya Yamada, Yu Okuda, Masahiko Kushida, Kayo Sumida, Hayato Takeuchi, Hirohisa Nagahori, Takako Fukuda, Brian G. Lake, Samuel M. Cohen & Satoshi Kawamura. (2014) Human Hepatocytes Support the Hypertrophic but not the Hyperplastic Response to the Murine Nongenotoxic Hepatocarcinogen Sodium Phenobarbital in an In Vivo Study Using a Chimeric Mouse with Humanized Liver. Toxicological Sciences 142:1, pages 137-157.
Crossref
Matthew J. LeBaron, Reza J. Rasoulpour, B. Bhaskar Gollapudi, Radhakrishna Sura, H. Lynn Kan, Melissa R. Schisler, Lynn H. Pottenger, Sabitha Papineni & David L. Eisenbrandt. (2014) Characterization of Nuclear Receptor-Mediated Murine Hepatocarcinogenesis of the Herbicide Pronamide and Its Human Relevance. Toxicological Sciences 142:1, pages 74-92.
Crossref
Richard A. Currie, Richard C. Peffer, Amber K. Goetz, Curtis J. Omiecinski & Jay I. Goodman. (2014) Phenobarbital and propiconazole toxicogenomic profiles in mice show major similarities consistent with the key role that constitutive androstane receptor (CAR) activation plays in their mode of action. Toxicology 321, pages 80-88.
Crossref
Radu M. Nanau, Faustine Delzor & Manuela G. Neuman. (2014) Efficacy and safety of prasugrel in acute coronary syndrome patients. Clinical Biochemistry 47:7-8, pages 516-528.
Crossref
J.E. Kester. 2014. Encyclopedia of Toxicology. Encyclopedia of Toxicology 96 106 .
Thomas G. Osimitz, Wiebke Droege, Alan R. Boobis & Brian G. Lake. (2013) Evaluation of the utility of the lifetime mouse bioassay in the identification of cancer hazards for humans. Food and Chemical Toxicology 60, pages 550-562.
Crossref
Matthew J. LeBaron, David R. Geter, Reza J. Rasoulpour, B. Bhaskar Gollapudi, Johnson Thomas, Jennifer Murray, H. Lynn Kan, Amanda J. Wood, Cliff Elcombe, Audrey Vardy, Jillian McEwan, Claire Terry & Richard Billington. (2013) An integrated approach for prospectively investigating a mode-of-action for rodent liver effects. Toxicology and Applied Pharmacology 270:2, pages 164-173.
Crossref
Costas Koufaris & Nigel J. Gooderham. (2013) Are Differences in MicroRNA Regulation Implicated in Species-Dependent Response to Toxicological Exposures?. Toxicological Sciences 131:2, pages 337-342.
Crossref
A. P. Hall, C. R. Elcombe, J. R. Foster, T. Harada, W. Kaufmann, A. Knippel, K. Küttler, D. E. Malarkey, R. R. Maronpot, A. Nishikawa, T. Nolte, A. Schulte, V. Strauss & M. J. York. (2012) Liver Hypertrophy. Toxicologic Pathology 40:7, pages 971-994.
Crossref
Costas Koufaris, Jayne Wright, Richard A. Currie & Nigel J. Gooderham. (2012) Hepatic MicroRNA Profiles Offer Predictive and Mechanistic Insights After Exposure to Genotoxic and Epigenetic Hepatocarcinogens. Toxicological Sciences 128:2, pages 532-543.
Crossref
John L. Butenhoff, Gerald L. KennedyJr.Jr., Shu-Ching Chang & Geary W. Olsen. (2012) Chronic dietary toxicity and carcinogenicity study with ammonium perfluorooctanoate in Sprague–Dawley rats. Toxicology 298:1-3, pages 1-13.
Crossref
John L. Butenhoff, James A. Bjork, Shu-Ching Chang, David J. Ehresman, George A. Parker, Kaberi Das, Christopher Lau, Paul H. Lieder, François M. van Otterdijk & Kendall B. Wallace. (2012) Toxicological evaluation of ammonium perfluorobutyrate in rats: Twenty-eight-day and ninety-day oral gavage studies. Reproductive Toxicology 33:4, pages 513-530.
Crossref
Anne E. Loccisano, Jerry L. CampbellJr.Jr., John L. Butenhoff, Melvin E. Andersen & Harvey J. ClewellIIIIII. (2012) Evaluation of placental and lactational pharmacokinetics of PFOA and PFOS in the pregnant, lactating, fetal and neonatal rat using a physiologically based pharmacokinetic model. Reproductive Toxicology 33:4, pages 468-490.
Crossref
Anne E. Loccisano, Jerry L. CampbellJrJr, John L. Butenhoff, Melvin E. Andersen & Harvey J. ClewellIIIIII. (2012) Comparison and evaluation of pharmacokinetics of PFOA and PFOS in the adult rat using a physiologically based pharmacokinetic model. Reproductive Toxicology 33:4, pages 452-467.
Crossref
S. Weber, S. Halm, M. Du Vall, K. Whitney, G. Blaich & D. Bury. (2012) N-vinylpyrrolidone dimer (VPD), a novel excipient for oral drugs: Repeat-dose oral toxicity in Sprague–Dawley rats. Toxicology Letters 210:3, pages 324-331.
Crossref
Elsa Nielsen, Pia Nørhede, Julie Boberg, Louise Krag Isling, Stine Kroghsbo, Niels Hadrup, Lea Bredsdorff, Alicja Mortensen & John Christian Larsen. (2012) Identification of Cumulative Assessment Groups of Pesticides. EFSA Supporting Publications 9:4.
Crossref
Sebastian Greenhough & David C. Hay. (2012) Stem Cell-Based Toxicity Screening. Pharmaceutical Medicine 26:2, pages 85-89.
Crossref
John L. Butenhoff, Shu-Ching Chang, Geary W. Olsen & Peter J. Thomford. (2012) Chronic dietary toxicity and carcinogenicity study with potassium perfluorooctanesulfonate in Sprague Dawley rats. Toxicology 293:1-3, pages 1-15.
Crossref
Clifford R. Elcombe, Barbara M. Elcombe, John R. Foster, Shu-Ching Chang, David J. Ehresman, Patricia E. Noker & John L. Butenhoff. (2012) Evaluation of hepatic and thyroid responses in male Sprague Dawley rats for up to eighty-four days following seven days of dietary exposure to potassium perfluorooctanesulfonate. Toxicology 293:1-3, pages 30-40.
Crossref
Clifford R. Elcombe, Barbara M. Elcombe, John R. Foster, Shu-Ching Chang, David J. Ehresman & John L. Butenhoff. (2012) Hepatocellular hypertrophy and cell proliferation in Sprague–Dawley rats from dietary exposure to potassium perfluorooctanesulfonate results from increased expression of xenosensor nuclear receptors PPARα and CAR/PXR. Toxicology 293:1-3, pages 16-29.
Crossref
. 2002. The MAK-Collection for Occupational Health and Safety. The MAK-Collection for Occupational Health and Safety 1 42 .
Robert Roos, Patrik L. Andersson, Krister Halldin, Helen Hǻkansson, Emma Westerholm, Timo Hamers, Gerd Hamscher, Päivi Heikkinen, Merja Korkalainen, Heather A. Leslie, Marjo Niittynen, Satu Sankari, Hans-Joachim Schmitz, Leo T.M. van der Ven, Matti Viluksela & Dieter Schrenk. (2011) Hepatic effects of a highly purified 2,2′,3,4,4′,5,5′-heptachlorbiphenyl (PCB 180) in male and female rats. Toxicology 284:1-3, pages 42-53.
Crossref
Anne E. Loccisano, Jerry L. CampbellJr.Jr., Melvin E. Andersen & Harvey J. ClewellIIIIII. (2011) Evaluation and prediction of pharmacokinetics of PFOA and PFOS in the monkey and human using a PBPK model. Regulatory Toxicology and Pharmacology 59:1, pages 157-175.
Crossref
Sebastian Greenhough, Claire N. Medine & David C. Hay. (2010) Pluripotent stem cell derived hepatocyte like cells and their potential in toxicity screening. Toxicology 278:3, pages 250-255.
Crossref
Clifford R. Elcombe, Barbara M. Elcombe, John R. Foster, David G. Farrar, Reinhard Jung, Shu-Ching Chang, Gerald L. Kennedy & John L. Butenhoff. (2010) Hepatocellular hypertrophy and cell proliferation in Sprague–Dawley rats following dietary exposure to ammonium perfluorooctanoate occurs through increased activation of the xenosensor nuclear receptors PPARα and CAR/PXR. Archives of Toxicology 84:10, pages 787-798.
Crossref
Jillian Ross, Simon M. Plummer, Anja Rode, Nico Scheer, Conrad C. Bower, Ortwin Vogel, Colin J. Henderson, C. Roland Wolf & Clifford R. Elcombe. (2010) Human Constitutive Androstane Receptor (CAR) and Pregnane X Receptor (PXR) Support the Hypertrophic but not the Hyperplastic Response to the Murine Nongenotoxic Hepatocarcinogens Phenobarbital and Chlordane In Vivo. Toxicological Sciences 116:2, pages 452-466.
Crossref
Michael L. Cunningham, Bradley J. Collins, Milton R. Hejtmancik, Ronald A. Herbert, Gregory S. Travlos, Molly K. Vallant & Matthew D. Stout. (2010) Effects of the PPAR Agonist and Widely Used Antihyperlipidemic Drug Gemfibrozil on Hepatic Toxicity and Lipid Metabolism . PPAR Research 2010, pages 1-14.
Crossref

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.