221
Views
28
CrossRef citations to date
0
Altmetric
Review

Therapeutic drug monitoring of mycophenolic acid: does it improve patient outcome?

, , &
Pages 251-261 | Published online: 11 Apr 2007

Bibliography

  • COX VC, ENSOM MH: Mycophenolate mofetil for solid organ transplantation: does the evidence support the need for clinical pharmacokinetic monitoring? Ther. Drug Monit. (2003) 25(2):137-157.
  • HALLORAN P, MATHEW T, TOMLANOVICH S et al.: Mycophenolate mofetil in renal allograft recipients: a pooled efficacy analysis of three randomized, double-blind, clinical studies in prevention of rejection. The International Mycophenolate Mofetil Renal Transplant Study Groups. Transplantation (1997) 63(1):39-47.
  • KAUFMAN DB, SHAPIRO R, LUCEY MR et al.: Immunosuppression: practice and trends. Am. J. Transplant. (2004) 4(Suppl. 9):38-53.
  • SHIPKOVA M, ARMSTRONG VW, WIELAND E et al.: Identification of glucoside and carboxyl-linked glucuronide conjugates of mycophenolic acid in plasma of transplant recipients treated with mycophenolate mofetil. Br. J. Pharmacol. (1999) 126(5):1075-1082.
  • BULLINGHAM RE, NICHOLLS AJ, KAMM BR: Clinical pharmacokinetics of mycophenolate mofetil. Clin. Pharmacokinet. (1998) 34(6):429-455.
  • KAGAYA H, INOUE K, MIURA M et al.: Influence of UGT1A8 and UGT2B7 genetic polymorphisms on mycophenolic acid pharmacokinetics in Japanese renal transplant recipients. Eur. J. Clin. Pharmacol. (2007) 63(3):279-288.
  • NOWAK I, SHAW LM: Mycophenolic acid binding to human serum albumin: characterization and relation to pharmacodynamics. Clin. Chem. (1995) 41(7):1011-1017.
  • JOHNSTON A, HOLT DW: Therapeutic drug monitoring of immunosuppressant drugs. Br. J. Clin. Pharmacol. (1999) 47(4):339-350.
  • HALE MD, NICHOLLS AJ, BULLINGHAM RE et al.: The pharmacokinetic-pharmacodynamic relationship for mycophenolate mofetil in renal transplantation. Clin. Pharmacol. Ther. (1998) 64(6):672-683.
  • WEBER LT, SHIPKOVA M, ARMSTRONG VW et al.: The pharmacokinetic–pharmacodynamic relationship for total and free mycophenolic Acid in pediatric renal transplant recipients: a report of the german study group on mycophenolate mofetil therapy. J. Am. Soc. Nephrol. (2002) 13(3):759-768.
  • KIBERD BA, LAWEN J, FRASER AD, KEOUGH-RYAN T, BELITSKY P: Early adequate mycophenolic acid exposure is associated with less rejection in kidney transplantation. Am. J. Transplant. (2004) 4(7):1079-1083.
  • BENNETT WM: Immunosuppression with mycophenolic acid: one size does not fit all. J. Am. Soc. Nephrol. (2003) 14(9):2414-2416.
  • CATTANEO D, GASPARI F, FERRARI S et al.: Pharmacokinetics help optimizing mycophenolate mofetil dosing in kidney transplant patients. Clin. Transplant. (2001) 15(6):402-409.
  • VAN HEST RM, HESSELINK DA, VULTO AG, MATHOT RA, VAN GELDER T: Individualization of mycophenolate mofetil dose in renal transplant recipients. Expert Opin. Pharmacother. (2006) 7(4):361-376.
  • KUYPERS DR, CLAES K, EVENEPOEL P, MAES B, VANRENTERGHEM Y: Clinical efficacy and toxicity profile of tacrolimus and mycophenolic acid in relation to combined long-term pharmacokinetics in de novo renal allograft recipients. Clin. Pharmacol. Ther. (2004) 75(5):434-447.
  • FILLER G, ZIMMERING M, MAI I: Pharmacokinetics of mycophenolate mofetil are influenced by concomitant immunosuppression. Pediatr. Nephrol. (2000) 14(2):100-104.
  • ZUCKER K, TSAROUCHA A, OLSON L et al.: Evidence that tacrolimus augments the bioavailability of mycophenolate mofetil through the inhibition of mycophenolic acid glucuronidation. Ther. Drug Monit. (1999) 21(1):35-43.
  • ATCHESON BA, TAYLOR PJ, MUDGE DW et al.: Mycophenolic acid pharmacokinetics and related outcomes early after renal transplant. Br. J. Clin. Pharmacol. (2005) 59(3):271-280.
  • HUBNER GI, EISMANN R, SZIEGOLEIT W: Drug interaction between mycophenolate mofetil and tacrolimus detectable within therapeutic mycophenolic acid monitoring in renal transplant patients. Ther. Drug Monit. (1999) 21(5):536-539.
  • LIPSKY JJ: Mycophenolate mofetil. Lancet (1996) 348(9038):1357-1359.
  • VAN GELDER T, HILBRANDS LB, VANRENTERGHEM Y et al.: A randomized double-blind, multicenter plasma concentration controlled study of the safety and efficacy of oral mycophenolate mofetil for the prevention of acute rejection after kidney transplantation. Transplantation (1999) 68(2):261-266.
  • MOURAD M, MALAISE J, CHAIB EDDOUR D et al.: Correlation of mycophenolic acid pharmacokinetic parameters with side effects in kidney transplant patients treated with mycophenolate mofetil. Clin. Chem. (2001) 47(1):88-94.
  • MOURAD M, MALAISE J, CHAIB EDDOUR D et al.: Pharmacokinetic basis for the efficient and safe use of low-dose mycophenolate mofetil in combination with tacrolimus in kidney transplantation. Clin. Chem. (2001) 47(7):1241-1248.
  • BORROWS R, CHUSNEY G, LOUCAIDOU M et al.: Mycophenolic acid 12-h trough level monitoring in renal transplantation: association with acute rejection and toxicity. Am. J. Transplant. (2006) 6(1):121-128.
  • ATCHESON BA, TAYLOR PJ, KIRKPATRICK CM et al.: Free mycophenolic acid should be monitored in renal transplant recipients with hypoalbuminemia. Ther. Drug Monit. (2004) 26(3):284-286.
  • SHAW LM, HOLT DW, OELLERICH M, MEISER B, VAN GELDER T: Current issues in therapeutic drug monitoring of mycophenolic acid: report of a roundtable discussion. Ther. Drug Monit. (2001) 23(4):305-315.
  • SHAW LM, KORECKA M, VENKATARAMANAN R et al.: Mycophenolic acid pharmacodynamics and pharmacokinetics provide a basis for rational monitoring strategies. Am. J. Transplant. (2003) 3(5):534-542.
  • VAN HEST RM, MATHOT RA, VULTO AG, IJZERMANS JN, VAN GELDER T: Within-patient variability of mycophenolic acid exposure: therapeutic drug monitoring from a clinical point of view. Ther. Drug Monit. (2006) 28(1):31-34.
  • VAN HEST R, MATHOT R, VULTO A, WEIMAR W, VAN GELDER T: Predicting the usefulness of therapeutic drug monitoring of mycophenolic acid: a computer simulation. Ther. Drug Monit. (2005) 27(2):163-167.
  • BUDDE K, GLANDER P, BAUER S et al.: Pharmacodynamic monitoring of mycophenolate mofetil. Clin. Chem. Lab. Med. (2000) 38(11):1213-1216.
  • GLANDER P, HAMBACH P, BRAUN KP et al.: Pre-transplant inosine monophosphate dehydrogenase activity is associated with clinical outcome after renal transplantation. Am. J. Transplant. (2004) 4(12):2045-2051.
  • MILLAN O, OPPENHEIMER F, BRUNET M et al.: Assessment of mycophenolic acid-induced immunosuppression: a new approach. Clin. Chem. (2000) 46(9):1376-1383.
  • VETHE NT, MANDLA R, LINE PD et al.: Inosine monophosphate dehydrogenase activity in renal allograft recipients during mycophenolate treatment. Scand. J. Clin. Lab. Invest. (2006) 66(1):31-44.
  • BUDDE K, BRAUN KP, GLANDER P et al.: Pharmacodynamic monitoring of mycophenolate mofetil in stable renal allograft recipients. Transplant. Proc. (2002) 34(5):1748-1750.
  • VAN GELDER T: Mycophenolate mofetil: how to further improve using an already successful drug? Am. J. Transplant. (2005) 5(2):199-200.
  • MORISSETTE P, ALBERT C, BUSQUE S, ST-LOUIS G, VINET B: In vivo higher glucuronidation of mycophenolic acid in male than in female recipients of a cadaveric kidney allograft and under immunosuppressive therapy with mycophenolate mofetil. Ther. Drug Monit. (2001) 23(5):520-525.
  • BORROWS R, CHUSNEY G, JAMES A et al.: Determinants of mycophenolic acid levels after renal transplantation. Ther. Drug Monit. (2005) 27(4):442-450.
  • VAN HEST RM, VAN GELDER T, VULTO AG, MATHOT RA: Population pharmacokinetics of mycophenolic acid in renal transplant recipients. Clin. Pharmacokinet. (2005) 44(10):1083-1096.
  • PESCOVITZ MD, GUASCH A, GASTON R et al.: Equivalent pharmacokinetics of mycophenolate mofetil in African-American and Caucasian male and female stable renal allograft recipients. Am. J. Transplant. (2003) 3(12):1581-1586.
  • VAN HEST RM, MATHOT RA, PESCOVITZ MD et al.: Explaining variability in mycophenolic acid exposure to optimize mycophenolate mofetil dosing: a population pharmacokinetic meta-analysis of mycophenolic acid in renal transplant recipients. J. Am. Soc. Nephrol. (2006) 17(3):871-880.
  • KUYPERS DR, CLAES K, EVENEPOEL P et al.: Long-term changes in mycophenolic acid exposure in combination with tacrolimus and corticosteroids are dose dependent and not reflected by trough plasma concentration: a prospective study in 100 de novo renal allograft recipients. J. Clin. Pharmacol. (2003) 43(8):866-880.
  • NEYLAN JF: Immunosuppressive therapy in high-risk transplant patients: dose-dependent efficacy of mycophenolate mofetil in African-American renal allograft recipients. US Renal Transplant Mycophenolate Mofetil Study Group. Transplantation (1997) 64(9):1277-1282.
  • SCHWEITZER EJ, YOON S, FINK J et al.: Mycophenolate mofetil reduces the risk of acute rejection less in African-American than in Caucasian kidney recipients. Transplantation (1998) 65(2):242-248.
  • MEIER-KRIESCHE HU, OJO AO, LEICHTMAN AB et al.: Effect of mycophenolate mofetil on long-term outcomes in African american renal transplant recipients. J. Am. Soc. Nephrol. (2000) 11(12):2366-2370.
  • SHAW LM, KORECKA M, ARADHYE S et al.: Mycophenolic acid area under the curve values in African American and Caucasian renal transplant patients are comparable. J. Clin. Pharmacol. (2000) 40(6):624-633.
  • SHAW LM, NAWROCKI A, KORECKA M, SOLARI S, KANG J: Using established immunosuppressant therapy effectively: lessons from the measurement of mycophenolic acid plasma concentrations. Ther. Drug Monit. (2004) 26(4):347-351.
  • CHEN H, PENG C, YU Z et al.: Pharmacokinetics of mycophenolic Acid and determination of area under the curve by abbreviated sampling strategy in chinese liver transplant recipients. Clin. Pharmacokinet. (2007) 46(2):175-185.
  • LE GUELLEC C, BOURGOIN H, BUCHLER M et al.: Population pharmacokinetics and Bayesian estimation of mycophenolic acid concentrations in stable renal transplant patients. Clin. Pharmacokinet. (2004) 43(4):253-266.
  • STAATZ CE, DUFFULL SB, KIBERD B, FRASER AD, TETT SE: Population pharmacokinetics of mycophenolic acid during the first week after renal transplantation. Eur. J. Clin. Pharmacol. (2005) 61(7):507-516.
  • VAN HEST RM, MATHOT RA, VULTO AG, LE MEUR Y, VAN GELDER T: Mycophenolic acid in diabetic renal transplant recipients: pharmacokinetics and application of a limited sampling strategy. Ther. Drug Monit. (2004) 26(6):620-625.
  • SHAW LM, MICK R, NOWAK I, KORECKA M, BRAYMAN KL: Pharmacokinetics of mycophenolic acid in renal transplant patients with delayed graft function. J. Clin. Pharmacol. (1998) 38(3):268-275.
  • WEBER LT, SHIPKOVA M, LAMERSDORF T et al.: Pharmacokinetics of mycophenolic acid (MPA) and determinants of MPA free fraction in pediatric and adult renal transplant recipients. German Study group on Mycophenolate Mofetil Therapy in Pediatric Renal Transplant Recipients. J. Am. Soc. Nephrol. (1998) 9(8):1511-1520.
  • VAN GELDER T, SHAW LM: The rationale for and limitations of therapeutic drug monitoring for mycophenolate mofetil in transplantation. Transplantation (2005) 80(Suppl. 2):S244-S253.
  • VAN HEST R, VAN GELDER T, BOUW R et al.: Time-dependent clearance of mycophenolic acid in renal transplant recipients. Br. J. Clin. Pharmacol. (2007) (In Press).
  • NAITO T, SHINNO K, MAEDA T et al.: Effects of calcineurin inhibitors on pharmacokinetics of mycophenolic acid and its glucuronide metabolite during the maintenance period following renal transplantation. Biol. Pharm. Bull. (2006) 29(2):275-280.
  • GREGOOR PJ, DE SEVAUX RG, HENE RJ et al.: Effect of cyclosporine on mycophenolic acid trough levels in kidney transplant recipients. Transplantation (1999) 68(10):1603-1606.
  • SMAK GREGOOR PJ, VAN GELDER T, HESSE CJ et al.: Mycophenolic acid plasma concentrations in kidney allograft recipients with or without cyclosporin: a cross-sectional study. Nephrol. Dial. Transplant. (1999) 14(3):706-708.
  • VAN GELDER T, KLUPP J, BARTEN MJ, CHRISTIANS U, MORRIS RE: Comparison of the effects of tacrolimus and cyclosporine on the pharmacokinetics of mycophenolic acid. Ther. Drug Monit. (2001) 23(2):119-128.
  • CREMERS S, SCHOEMAKER R, SCHOLTEN E et al.: Characterizing the role of enterohepatic recycling in the interactions between mycophenolate mofetil and calcineurin inhibitors in renal transplant patients by pharmacokinetic modelling. Br. J. Clin. Pharmacol. (2005) 60(3):249-256.
  • KOBAYASHI M, SAITOH H, TADANO K, TAKAHASHI Y, HIRANO T: Cyclosporin A, but not tacrolimus, inhibits the biliary excretion of mycophenolic acid glucuronide possibly mediated by multidrug resistance-associated protein 2 in rats. J. Pharmacol. Exp. Ther. (2004) 309(3):1029-1035.
  • HESSELINK DA, VAN HEST RM, MATHOT RA et al.: Cyclosporine interacts with mycophenolic acid by inhibiting the multidrug resistance-associated protein 2. Am. J. Transplant. (2005) 5(5):987-994.
  • PICARD N, PREMAUD A, ROUSSEAU A, LE MEUR Y, MARQUET P: A comparison of the effect of ciclosporin and sirolimus on the pharmokinetics of mycophenolate in renal transplant patients. Br. J. Clin. Pharmacol. (2006) 62(4):477-484.
  • BUCHLER M, LEBRANCHU Y, BENETON M et al.: Higher exposure to mycophenolic acid with sirolimus than with cyclosporine cotreatment. Clin. Pharmacol. Ther. (2005) 78(1):34-42.
  • GRINYO J, EKBERG H, OPPENHEIMER F et al.: Pharmacokinetics of total and free mycophenolic acid (MPA) when mycophenolate mofetil (MMF) is administered with low-dose tacrolimus, low-dose cyclosporine, low-dose sirolimus or standard-dose dyclosporine in renal transplantation. Results of the Symphony PK substudy. [abstract]. Transplantation (2006) 82(1 Suppl. 2):345.
  • CATTANEO D, PERICO N, GASPARI F, GOTTI E, REMUZZI G: Glucocorticoids interfere with mycophenolate mofetil bioavailability in kidney transplantation. Kidney Int. (2002) 62(3):1060-1067.
  • MORII M, UENO K, OGAWA A et al.: Impairment of mycophenolate mofetil absorption by iron ion. Clin. Pharmacol. Ther. (2000) 68(6):613-616.
  • MUDGE DW, ATCHESON B, TAYLOR PJ et al.: The effect of oral iron admiinistration on mycophenolate mofetil absorption in renal transplant recipients: a randomized, controlled trial. Transplantation (2004) 77(2):206-209.
  • LIDGATE D, BRANDL M, HOLPER M, ABUBAKARI A, WU X: Influence of ferrous sulfate on the solubility, partition coefficient, and stability of mycophenolic acid and the ester mycophenolate mofetil. Drug Dev. Ind. Pharm. (2002) 28(10):1275-1283.
  • PIEPER AK, BUHLE F, BAUER S et al.: The effect of sevelamer on the pharmacokinetics of cyclosporin A and mycophenolate mofetil after renal transplantation. Nephrol. Dial. Transplant. (2004) 19(10):2630-2633.
  • KUYPERS DR, VERLEDEN G, NAESENS M, VANRENTERGHEM Y: Drug interaction between mycophenolate mofetil and rifampin: possible induction of uridine diphosphate- glucuronosyltransferase. Clin. Pharmacol. Ther. (2005) 78(1):81-88.
  • HESSELINK DA, VAN GELDER T: Genetic and nongenetic determinants of between-patient variability in the pharmacokinetics of mycophenolic acid. Clin. Pharmacol. Ther. (2005) 78(4):317-321.
  • BERNARD O, GUILLEMETTE C: The main role of UGT1A9 in the hepatic metabolism of mycophenolic acid and the effects of naturally occurring variants. Drug Metab. Dispos. (2004) 32(8):775-778.
  • GIRARD H, COURT MH, BERNARD O et al.: Identification of common polymorphisms in the promoter of the UGT1A9 gene: evidence that UGT1A9 protein and activity levels are strongly genetically controlled in the liver. Pharmacogenetics (2004) 14(8):501-515.
  • VAN AGTEREN M, VAN SCHAIK R, DE FIJTER H et al.: Polymorphisms in the uridine diphosphate (UDP)-glucuronosyltransferases (UGT) gene explain part of the inter-individual variability in mycophenolate mofetil (MMF) pharmacokinetics [abstract]. Transplantation (2006) 82(1 Suppl. 2):478.
  • KUYPERS DR, NAESENS M, VERMEIRE S, VANRENTERGHEM Y: The impact of uridine diphosphate-glucuronosyltransferase 1A9 (UGT1A9) gene promoter region single-nucleotide polymorphisms T-275A and C-2152T on early mycophenolic acid dose-interval exposure in de novo renal allograft recipients. Clin. Pharmacol. Ther. (2005) 78(4):351-361.
  • MARQUET P, DJEBLI N, PICARD N et al.: Influence of metabolic enzymes and efflux transporter polymorphisms on the plasma concentrations of mpa metabolites in renal transplant recipients [abstract]. Am. J. Transplant. (2005) 5(Suppl. 11):391.
  • VAN AGTEREN M, VAN SCHAIK R, DE FIJTER H et al.: The impact of MRP2 gene polymorphism on mycophenolic acid exposure in renal transplant patients [abstract]. Transplantation (2006) 82(1 Suppl. 2):478.
  • NAESENS M, KUYPERS DR, VERBEKE K, VANRENTERGHEM Y: Multidrug resistance protein 2 genetic polymorphisms influence mycophenolic acid exposure in renal allograft recipients. Transplantation (2006) 82(8):1074-1084.
  • CARR SF, PAPP E, WU JC, NATSUMEDA Y: Characterization of human type I and type II IMP dehydrogenases. J. Biol. Chem. (1993) 268(36):27286-27290.
  • VANNOZZI F, FILIPPONI F, DI PAOLO A et al.: An exploratory study on pharmacogenetics of inosine-monophosphate dehydrogenase II in peripheral mononuclear cells from liver-transplant recipients. Transplant. Proc. (2004) 36(9):2787-2790.
  • VAN AGTEREN M, VAN GELDER T: Incidence of acute rejection after kidney transplantation and the correlation with polymorphisms in the inosine monophosphate dehydrogenase (IMPDH) gene [abstract]. Transplantation (2006) 82(1 Suppl. 2):478.
  • BAZRAFSHANI MR, POULTON KV, QASIM FJ, DYER PA: Genetic polymorphism of non-synonymous amino acid change of the IMPDH-1 gene in renal patients. Hum. Immunol. (2003) 64(10):S70.
  • ROBERTS RL, GEARRY RB, BARCLAY ML, KENNEDY MA: IMPDH1 promoter mutations in a patient exhibiting azathioprine resistance. Pharmacogenomics J. (2006) (In Press).
  • GRINYO J, VANRENTERGHEM Y, NASHAN B et al.: Association of three polymorphisms with acute rejection after kidney transplantation: an exploratory pharmacogenetic analysis of a randomized multicenter clinical trial (the caesar study) [abstract]. Transplantation (2006) 82(1 Suppl. 2):410-411.
  • WEBER LT, LAMERSDORF T, SHIPKOVA M et al.: Area under the plasma concentration–time curve for total, but not for free, mycophenolic acid increases in the stable phase after renal transplantation: a longitudinal study in pediatric patients. German Study Group on Mycophenolate Mofetil Therapy in Pediatric Renal Transplant Recipients. Ther. Drug Monit. (1999) 21(5):498-506.
  • KUYPERS DR, VANRENTERGHEM Y, SQUIFFLET JP et al.: Twelve-month evaluation of the clinical pharmacokinetics of total and free mycophenolic acid and its glucuronide metabolites in renal allograft recipients on low dose tacrolimus in combination with mycophenolate mofetil. Ther. Drug Monit. (2003) 25(5):609-622.
  • NICHOLLS AJ: Opportunities for therapeutic monitoring of mycophenolate mofetil dose in renal transplantation suggested by the pharmacokinetic/pharmacodynamic relationship for mycophenolic acid and suppression of rejection. Clin. Biochem. (1998) 31(5):329-333.
  • ROUSSEAU A, MARQUET P: Application of pharmacokinetic modelling to the routine therapeutic drug monitoring of anticancer drugs. Fundam. Clin. Pharmacol. (2002) 16(4):253-262.
  • TING LS, VILLENEUVE E, ENSOM MH: Beyond cyclosporine: a systematic review of limited sampling strategies for other immunosuppressants. Ther. Drug Monit. (2006) 28(3):419-430.
  • PAWINSKI T, HALE M, KORECKA M, FITZSIMMONS WE, SHAW LM: Limited sampling strategy for the estimation of mycophenolic acid area under the curve in adult renal transplant patients treated with concomitant tacrolimus. Clin. Chem. (2002) 48(9):1497-1504.
  • VAN GELDER T, MEUR YL, SHAW LM et al.: Therapeutic drug monitoring of mycophenolate mofetil in transplantation. Ther. Drug Monit. (2006) 28(2):145-154.
  • LE GUELLEC C, BUCHLER M, GIRAUDEAU B et al.: Simultaneous estimation of cyclosporin and mycophenolic acid areas under the curve in stable renal transplant patients using a limited sampling strategy. Eur. J. Clin. Pharmacol. (2002) 57(11):805-811.
  • PREMAUD A, LE MEUR Y, DEBORD J et al.: Maximum a posteriori bayesian estimation of mycophenolic acid pharmacokinetics in renal transplant recipients at different postgrafting periods. Ther. Drug Monit. (2005) 27(3):354-361.
  • MARQUET P: Clinical application of population pharmacokinetic methods developed for immunosuppressive drugs. Ther. Drug Monit. (2005) 27(6):727-732.
  • VAN GELDER T, SILVA HT, DE FIJTER H et al.: A prospective, randomised study comparing fixed dose versus concentration controlled MMF regimens for de novo patients following renal transplantation (the FDCC trial) [abstract]. Transplantation (2006) 82(1 Suppl. 2):343.
  • LE MEUR Y, BUCHLER M, LAVAUD S et al.: Therapeutic drug monitoring of MMF: a randomized multicenter study comparing concentration controlled versus fixed dose in kidney transplant recipients [abstract]. Transplantation (2006) 82(1 Suppl. 2):343-344.
  • BLOOM R, NARAGHI R, CIBRIK DM et al.: Opticept trial: interim results of 6-month efficacy and safety of monitored mycophenolate mofetil (MMF) in combination with CNI in renal transplantation [abstract]. Transplantation (2006) 82(1 Suppl. 2):344.

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.