476
Views
52
CrossRef citations to date
0
Altmetric
Review

Systems for region selective drug delivery in the gastrointestinal tract: biopharmaceutical considerations

, MSc Clin Pharm &
Pages 681-692 | Published online: 05 Jun 2008

Bibliography

  • Washington N, Washington C, Wilson CG. Physiological pharmaceutics. Barriers to drug absorption. 2nd edition. New York: Taylor and Francis, Inc.; 2001
  • Davis SS, Wilding EA, Wilding IR. Gastrointestinal transit of a matrix tablet formulation: comparison of canine and human data. Int J Pharm 1993;94(1-3):235-8
  • Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos 1995;16(5):351-80
  • Wilding I. Site-specific drug delivery in the gastrointestinal tract. Crit Rev Ther Drug Carrier Syst 2000;17(6):557-620
  • Timmermans J, Moes AJ. Factors controlling the buoyancy and gastric retention capabilities of floating matrix capsules: new data for reconsidering the controversy. J Pharm Sci 1994;83(1):18-24
  • Klausner EA, Lavy E, Friedman M, Hoffman A. Expandable gastroretentive dosage forms. J Control Release 2003;90(2):143-62
  • Streubel A, Siepmann J, Bodmeier R. Gastroretentive drug delivery systems. Exp Opin Drug Deliv 2006;3(2):217-33
  • Moes AJ. Gastroretentive dosage forms. Crit Rev Ther Drug Carrier Syst 1993;10(2):143-95
  • Reddy LH, Murthy RS. Floating dosage systems in drug delivery. Crit Rev Ther Drug Carrier Syst 2002;19(6):553-85
  • Hou SY, Cowles VE, Berner B. Gastric retentive dosage forms: a review. Crit Rev Ther Drug Carrier Syst 2003;20(6):459-97
  • Gusler G, Gorsline J, Levy G, et al. Pharmacokinetics of metformin gastric-retentive tablets in healthy volunteers. J Clin Pharmacol 2001;41(6):655-61
  • Gusler G, Hou SYE, Berner B, et al. Single dose pharmacokinetics of gabapentin Gastric Retentive (GRTM) tablets in healthy volunteers. Controlled Release Society 31st Annual Meeting; 12 – 16 June 2004; Honolulu, Hawaii, USA
  • Agyilirah GA, Green M, duCret R, Banker GS. Evaluation of the gastric retention properties of a cross-linked polymer coated tablet versus those of a non-disintegrating tablet. Int J Pharm 1991;75(2-3):241-7
  • Oth M, Franz M, Timmermans J, Moes A. The bilayer floating capsule: a stomach-directed drug delivery system for misoprostol. Pharm Res 1992;9(3):298-302
  • Whitehead L, Fell JT, Collett JH, et al. Floating dosage forms: an in vivo study demonstrating prolonged gastric retention. J Control Release 1998;55(1):3-12
  • Davis SS, Hardy JG, Taylor MJ, et al. The effect of food on the gastrointestinal transit of pellets and an osmotic device (Osmet). Int J Pharm 1984;21(3):331-40
  • Wilding IR, Coupe AJ, Davis SS. The role of gamma-scintigraphy in oral drug delivery. Adv Drug Deliv Rev 2001;46(1-3):103-24
  • Davis SS, Hardy JG, Newman SP, Wilding IR. Gamma-scintigraphy in the evaluation of pharmaceutical dosage forms. Eur J Nucl Med 1992;19(11):971-86
  • Afargan M, Kagan L, Kirmayer D, et al. Gastroretentive Accordion pill: Unaltered food transit and enhanced riboflavin bioavailability. Controlled Release Society 33rd Annual Meeting; 22 – 26 July 2006; Vienna, Austria
  • Kagan L, Lapidot N, Afargan M, et al. Gastroretentive Accordion Pill: enhancement of riboflavin bioavailability in humans. J Control Release 2006;113(3):208-15
  • Steingoetter A, Weishaupt D, Kunz P, et al. Magnetic resonance imaging for the in vivo evaluation of gastric-retentive tablets. Pharm Res 2003;20(12):2001-7
  • Arora S, Ali J, Ahuja A, et al. Floating drug delivery systems: a review. AAPS PharmSciTech 2005;6(3):E372-90
  • Singh BN, Kim KH. Floating drug delivery systems: an approach to oral controlled drug delivery via gastric retention. J Control Release 2000;63(3):235-59
  • Ozdemir N, Ordu S, Ozkan Y. Studies of floating dosage forms of furosemide: in vitro and in vivo evaluations of bilayer tablet formulations. Drug Dev Ind Pharm 2000;26(8):857-66
  • Bennett CE, Hardy JG, Wilson CG. The influence of posture on the gastric emptying of antacids. Int J Pharm 1984;21(3):341-7
  • Klausner EA, Lavy E, Barta M, et al. Novel gastroretentive dosage forms: evaluation of gastroretentivity and its effect on levodopa absorption in humans. Pharm Res 2003;20(9):1466-73
  • Klausner EA, Lavy E, Stepensky D, et al. Novel gastroretentive dosage forms: evaluation of gastroretentivity and its effect on riboflavin absorption in dogs. Pharm Res 2002;19(10):1516-23
  • Noonan B, Alm RA. Novel Intervention strategies for Helicobacter pylori treatment. Curr Drug Targets Infect Disord 2002;2(4):331
  • Conway BR. Drug delivery strategies for the treatment of Helicobacter pylori infections. Curr Pharm Des 2005;11(6):775-90
  • Peterson WL. Helicobacter pylori and peptic ulcer disease. N Engl J Med 1991;324(15):1043-8
  • Cooreman MP, Krausgrill P, Hengels KJ. Local gastric and serum amoxicillin concentrations after different oral application forms. Antimicrob Agents Chemother 1993;37(7):1506-9
  • Lozniewski A, de Korwin JD, Muhale F, Jehl F. Gastric diffusion of antibiotics used against Helicobacter pylori. Int J Antimicrob Agents 1998;9(3):181-93
  • Goddard AF, Jessa MJ, Barrett DA, et al. Effect of omeprazole on the distribution of metronidazole, amoxicillin, and clarithromycin in human gastric juice. Gastroenterology 1996;111(2):358-67
  • Shah S, Qaqish R, Patel V, Amiji M. Evaluation of the factors influencing stomach-specific delivery of antibacterial agents for Helicobacter pylori infection. J Pharm Pharmacol 1999;51(6):667-72
  • Wang J, Tauchi Y, Deguchi Y, et al. Positively charged gelatin microspheres as gastric mucoadhesive drug delivery system for eradication of H. pylori. Drug Deliv 2000;7(4):237-43
  • Murata Y, Sasaki N, Miyamoto E, Kawashima S. Use of floating alginate gel beads for stomach-specific drug delivery. Eur J Pharm Biopharm 2000;50(2):221-6
  • Rajinikanth PS, Mishra B. Floating in situ gelling system for stomach site-specific delivery of clarithromycin to eradicate H. pylori. J Control Release 2008;125(1):33-41
  • Bardonnet PL, Faivre V, Pugh WJ, et al. Gastroretentive dosage forms: overview and special case of Helicobacter pylori. J Control Release 2006;111(1-2):1-18
  • Davis SS. Formulation strategies for absorption windows. Drug Discov Today 2005;10(4):249-57
  • Rojanasakul Y, Wang LY, Bhat M, et al. The transport barrier of epithelia a comparative study on membrane permeability and charge selectivity in the rabbit. Pharm Res 1992;9(8):1029-34
  • Mummaneni V, Dressman JB. Intestinal uptake of cimetidine and ranitidine in rats. Pharm Res 1994;11(11):1599-604
  • Rouge N, Buri P, Doelker E. Drug absorption sites in the gastrointestinal tract and dosage forms for site-specific delivery. Int J Pharm 1996;136(1-2):117-39
  • Ungell AL, Nylander S, Bergstrand S, et al. Membrane transport of drugs in different regions of the intestinal tract of the rat. J Pharm Sci 1998;87(3):360-6
  • Groning R, Berntgen M, Georgarakis M. Acyclovir serum concentrations following peroral administration of magnetic depot tablets and the influence of extracorporal magnets to control gastrointestinal transit. Eur J Pharm Biopharm 1998;46(3):285-91
  • Kagan L, Hoffman A. Selection of drug candidates for gastroretentive dosage forms: pharmacokinetics following continuous intragastric mode of administration in a rat model. Eur J Pharm Biopharm 2008;69:238-46
  • Tamai I, Tsuji A. Carrier-mediated approaches for oral drug delivery. Adv Drug Deliv Rev 1996;20(1):5-32
  • Sai Y, Tsuji A. Transporter-mediated drug delivery: recent progress and experimental approaches. Drug Discov Today 2004;9(16):712-20
  • Steffansen B, Nielsen CU, Brodin B, et al. Intestinal solute carriers: an overview of trends and strategies for improving oral drug absorption. Eur J Pharm Sci 2004;21(1):3-16
  • Englund G, Rorsman F, Ronnblom A, et al. Regional levels of drug transporters along the human intestinal tract: co-expression of ABC and SLC transporters and comparison with Caco-2 cells. Eur J Pharm Sci 2006;29(3-4):269-77
  • Ngo LY, Patil SD, Unadkat JD. Ontogenic and longitudinal activity of Na+-nucleoside transporters in the human intestine. Am J Physiol Gastrointest Liver Physiol 2001;280(3):G475-81
  • Jusko WJ, Levy G. Absorption, metabolism, and excretion of riboflavin-5′-phosphate in man. J Pharm Sci 1967;56(1):58-62
  • Levy G, Jusko WJ. Factors affecting the absorption of riboflavin in man. J Pharm Sci 1966;55(3):285-9
  • Ahmed IS, Ayres JW. Bioavailability of riboflavin from a gastric retention formulation. Int J Pharm 2007;330(1-2):146-54
  • Groning R, Cloer C, Georgarakis M, Muller RS. Compressed collagen sponges as gastroretentive dosage forms: in vitro and in vivo studies. Eur J Pharm Sci 2007;30(1):1-6
  • Berry DJ, Beran RG, Plunkeft MJ, et al. The absorption of gabapentin following high dose escalation. Seizure 2003;12(1):28-36
  • Gidal BE, DeCerce J, Bockbrader HN, et al. Gabapentin bioavailability: effect of dose and frequency of administration in adult patients with epilepsy. Epilepsy Res 1998;31(2):91-99
  • Stewart BH, Kugler AR, Thompson PR, Bockbrader HN. A saturable transport mechanism in the intestinal absorption of gabapentin is the underlying cause of the lack of proportionality between increasing dose and drug levels in plasma. Pharm Res 1993;10(2):276-81
  • Cowles VE, Gusler G, Gu R, et al. Dose proportionality of gabapentin gastric retentive extended release tablets in beagle dog [abstract T3201]. AAPS J 2006;8(S2)
  • Gabapentin extended release – Depomed: gabapentin ER, gabapentin gastric retention, gabapentin GR. Drugs R&D 2007;8(5):317-20
  • Cundy KC, Annamalai T, Bu L, et al. XP13512 [(+/–)-1-([(alpha-isobutanoyloxyethoxy)carbonyl] aminomethyl)-1-cyclohexane acetic acid], a novel gabapentin prodrug: II. Improved oral bioavailability, dose proportionality, and colonic absorption compared with gabapentin in rats and monkeys. J Pharmacol Exp Ther 2004;311(1):324-33
  • Friend DR. Drug delivery to the small intestine. Curr Gastroenterol Rep 2004;6(5):371-6
  • Gramatte T, Oertel R, Terhaag B, Kirch W. Direct demonstration of small intestinal secretion and site-dependent absorption of the beta-blocker talinolol in humans. Clin Pharmacol Ther 1996;59(5):541-9
  • Mouly S, Paine MF. P-glycoprotein increases from proximal to distal regions of human small intestine. Pharm Res 2003;20(10):1595-9
  • Yumoto R, Murakami T, Nakamoto Y, et al. Transport of rhodamine 123, a P-glycoprotein substrate, across rat intestine and Caco-2 cell monolayers in the presence of cytochrome P-450 3A-related compounds. J Pharmacol Exp Ther 1999;289(1):149-55
  • Tian R, Koyabu N, Takanaga H, et al. Effects of grapefruit juice and orange juice on the intestinal efflux of P-glycoprotein substrates. Pharm Res 2002;19(6):802-9
  • Fojo AT, Ueda K, Slamon DJ, et al. Expression of a Multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci USA 1987;84(1):265-9
  • Fricker G, Drewe J, Huwyler J, et al. Relevance of p-glycoprotein for the enteral absorption of cyclosporin A: in vitro in vivo correlation. Br J Pharmacol 1996;118(7):1841-7
  • Berggren S, Gall C, Wollnitz N, et al. Gene and protein expression of P-glycoprotein, MRP1, MRP2, and CYP3A4 in the small and large human intestine. Mol Pharm 2007;4(2):252-7
  • Nakayama A, Saitoh H, Oda M, et al. Region-dependent disappearance of vinblastine in rat small intestine and characterization of its P-glycoprotein-mediated efflux system. Eur J Pharm Sci 2000;11(4):317-24
  • Klausner EA, Lavy E, Stepensky D, et al. Furosemide pharmacokinetics and pharmacodynamics following gastroretentive dosage form administration to healthy volunteers. J Clin Pharmacol 2003;43(7):711-20
  • Washington CB, Hou SYE, Campanella C, et al. Pharmacokinetics and pharmacodynamics of a novel extended-release ciprofloxacin in healthy volunteers. J Clin Pharmacol 2005;45(11):1236-44
  • Hoffman A, Horwitz E, Hess S, et al. Implications on emergence of antimicrobial resistance as a critical aspect in the design of oral sustained release delivery systems of antimicrobials. Pharm Res 2007 [Epub ahead of print]
  • Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001;46(1-3):3-26
  • Palin KJ, Wilson CG. The effect of different oils on the absorption of probucol in the rat. J Pharm Pharmacol 1984;36(9):641-3
  • Dahan A, Hoffman A. The effect of different lipid based formulations on the oral absorption of lipophilic drugs: the ability of in vitro lipolysis and consecutive ex vivo intestinal permeability data to predict in vivo bioavailability in rats. Eur J Pharm Biopharm 2007;67(1):96-105
  • Fatouros DG, Mullertz A. In vitro lipid digestion models in design of drug delivery systems for enhancing oral bioavailability. Expert Opin Drug Metab Toxicol 2008;4(1):65-76
  • Porter CJH, Charman WN. Intestinal lymphatic drug transport: an update. Adv Drug Deliv Rev 2001;50(1-2):61-80
  • O'Driscoll CM. Lipid-based formulations for intestinal lymphatic delivery. Eur J Pharm Sci 2002;15(5):405-15
  • Porter CJ. Drug delivery to the lymphatic system. Crit Rev Ther Drug Carrier Syst 1997;14(4):333-93
  • Gershkovich P, Hoffman A. Uptake of lipophilic drugs by plasma derived isolated chylomicrons: linear correlation with intestinal lymphatic bioavailability. Eur J Pharm Sci 2005;26(5):394-404
  • Gershkovich P, Qadri B, Yacovan A, et al. Different impacts of intestinal lymphatic transport on the oral bioavailability of structurally similar synthetic lipophilic cannabinoids: dexanabinol and PRS-211,220. Eur J Pharm Sci 2007;31(5):298-305
  • Caliph SM, Charman WN, Porter CJH. Effect of short-, medium-, and long-chain fatty acid-based vehicles on the absolute oral bioavailability and intestinal lymphatic transport of halofantrine and assessment of mass balance in lymph-cannulated and non-cannulated rats. J Pharm Sci 2000;89(8):1073-84
  • Dahan A, Duvdevani R, Shapiro I, et al. The oral absorption of phospholipid prodrugs: in vivo and in vitro mechanistic investigation of trafficking of a lecithin–valproic acid conjugate following oral administration. J Control Release 2008;126(1):1-9
  • Dahan A, Hoffman A. Enhanced gastrointestinal absorption of lipophilic drugs. In: Touitou E, Barry BW, editors, Enhancment in drug delivery: CRC Press; 2007. p. 111-31
  • Dahan A, Hoffman A. Evaluation of a chylomicron flow blocking approach to investigate the intestinal lymphatic transport of lipophilic drugs. Eur J Pharm Sci 2005;24(4):381-8
  • Dahan A, Mendelman A, Amsili S, et al. The effect of general anesthesia on the intestinal lymphatic transport of lipophilic drugs: comparison between anesthetized and freely moving conscious rat models. Eur J Pharm Sci 2007;32(4-5):367-74
  • Gershkovich P, Elgart A, Hoffman A. Prediction of lymphatic absorption transport: in-Vivo, ex vivo, in vitro, and in silico models. 6th Annual Meeting of Israeli Chapter of Controlled Release Society; 5 – 6 September 2007; Caesarea, Israel
  • Adkin DA, Davis SS, Sparrow RA, Wilding IR. Colonic transit of different sized tablets in healthy subjects. J Control Release 1993;23(2):147-56
  • Dobson CL, Davis SS, Chauhan S, et al. The effect of oleic acid on the human ileal brake and its implications for small intestinal transit of tablet formulations. Pharm Res 1999;16(1):92-6
  • Dobson CL, Davis SS, Chauhan S, et al. The effect of ileal brake activators on the oral bioavailability of atenolol in man. Int J Pharm 2002;248(1-2):61-70
  • Godbillon J, Evard D, Vidon N, et al. Investigation of drug absorption from the gastrointestinal tract of man. 3. Metoprolol in the colon. Br J Clin Pharmacol 1985;19:S113-8
  • Basit AW. Advances in colonic drug delivery. Drugs 2005;65(14):1991-2007
  • Chourasia MK, Jain SK. Polysaccharides for colon targeted drug delivery. Drug Deliv 2004;11(2):129-48
  • Jain A, Gupta Y, Jain SK. Azo chemistry and its potential for colonic delivery. Crit Rev Therap Drug Carrier Syst 2006;23(5):349-400
  • Nugent SG, Kumar D, Rampton DS, Evans DF. Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut 2001;48(4):571-7
  • Carrette O, Favier C, Mizon C, et al. Bacterial enzymes used for colon-specific drug delivery are decreased in active Crohn's disease. Dig Dis Sci 1995;40(12):2641-6
  • Reddy SN, Bazzocchi G, Chan S, et al. Colonic motility and transit in health and ulcerative colitis. Gastroenterology 1991;101(5):1289-97
  • Rubinstein A. Colonic drug delivery. Drug Discov Today Technol 2005;2(1):33-7
  • Asghar LFA, Chandran S. Multiparticulate formulation approach to colon specific drug delivery: current perspectives. J Pharm Pharmaceut Sci 2006;9(3):327-38
  • Haupt S, Rubinstein A. The colon as a possible target for orally administered peptide and protein drugs. Crit Rev Therap Drug Carrier Syst 2002;19(6):499-551
  • Sinha V, Singh A, Kumar RV, et al. Oral colon-specific drug delivery of protein and peptide drugs. Crit Rev Therap Drug Carrier Syst 2007;24(1):63-92
  • Patel M, Shah T, Amin A. Therapeutic opportunities in colon-specific drug-delivery systems. Crit Rev Therap Drug Carrier Syst 2007;24(2):147-202
  • Miura S, Song IS, Morita A, et al. Distribution and biosynthesis of aminopeptidase N and dipeptidyl aminopeptidase-IV in rat small intestine. Biochim Biophys Acta 1983;761(1):66-75
  • Ikesue K, Kopeckova P, Kopecek J. Degradation of proteins by guinea pig intestinal enzymes. Int J Pharm 1993;95(1-3):171-9
  • Bai JPF. Distribution of brush-border membrane peptidases along the rat intestine. Pharm Res 1994;11(6):897-900
  • Ishizawa T, Hayashi M, Awazu S. Enhancement of jejunal and colonic absorption of fosfomycin by promoters in the rat. J Pharm Pharmacol 1987;39(11):892-5
  • Sutton SC, Lecluyse EL, Cammack L, Fix JA. Enhanced bioavailability of cefoxitin using palmitoyl L-carnitine. 1. Enhancer activity in different intestinal regions. Pharm Res 1992;9(2):191-4
  • Prueksaritanont T, Gorham LM, Hochman JH, et al. Comparative studies of drug-metabolizing enzymes in dog, monkey, and human small intestines, and in Caco-2 cells. Drug Metab Dispos 1996;24(6):634-42
  • Inoue M, Morikawa M, Tsuboi M, et al. Comparative study of human intestinal and hepatic esterases as related to enzymatic properties and hydrolyzing activity for ester-type drugs. Jpn J Pharmacol 1980;30(4):529-35
  • Inoue M, Morikawa M, Yamada T, et al. Hydrolysis of ester-type drugs by the purified esterase from human intestinal mucosa. Jpn J Pharmacol 1979;29(1):17-25
  • Van Gelder J, Shafiee M, De Clercq E, et al. Species-dependent and site-specific intestinal metabolism of ester prodrugs. Int J Pharm 2000;205(1-2):93-100
  • Gershkovich P, Hoffman A. Effect of a high-fat meal on absorption and disposition of lipophilic compounds: the importance of degree of association with triglyceride-rich lipoproteins. Eur J Pharm Sci 2007;32(1):24-32
  • DeSesso JM, Jacobson CF. Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem Toxicol 2001;39(3):209-28
  • Nur AO, Zhang JS. Captopril floating and/or bioadhesive tablets: design and release kinetics. Drug Dev Ind Pharm 2000;26(9):965-9
  • Rouge N, Allemann E, Gex-Fabry M, et al. Comparative pharmacokinetic study of a floating multiple-unit capsule, a high-density multiple-unit capsule and an immediate release tablet containing 25 mg atenolol. Pharm Acta Helv 1998;73(2):81-7
  • Machida Y, Inouye K, Tokumura T, et al. Preparation and evaluation of intragastric buoyant preparations. Drug Des Deliv 1989;4(2):155-61
  • Wei ZP, Yu ZF, Bi DZ. Design and evaluation of a two-layer floating tablet for gastric retention using cisapride as a model drug. Drug Dev Ind Pharm 2001;27(5):469-74
  • Li S, Lin S, Chien YW, et al. Statistical optimization of gastric floating system for oral controlled delivery of calcium. AAPS PharmSciTech 2001;2(1):E1
  • Menon A, Ritschel WA, Sakr A. Development and evaluation of a monolithic floating dosage form for furosemide. J Pharm Sci 1994;83(2):239-45
  • El-Kamel AH, Sokar MS, Al Gamal SS, Naggar VF. Preparation and evaluation of ketoprofen floating oral delivery system. Int J Pharm 2001;220(1-2):13-21
  • Erni W, Held K. The hydrodynamically balanced system: a novel principle of controlled drug release. Eur Neurol 1987;27(Suppl 1):21-7
  • Stepensky D, Friedman M, Srour W, et al. Preclinical evaluation of pharmacokinetic–pharmacodynamic rationale for oral CR metformin formulation. J Control Release 2001;71(1):107-15
  • Chueh HR, Zia H, Rhodes CT. Optimization of sotalol floating and bioadhesive extended release tablet formulations. Drug Dev Ind Pharm 1995;21(15):1725-47
  • Hejazi R, Amiji M. Stomach-specific anti-H. pylori therapy. II. Gastric residence studies of tetracycline-loaded chitosan microspheres in gerbils. Pharm Dev Technol 2003;8(3):253-62
  • Sawicki W. Pharmacokinetics of verapamil and norverapamil from controlled release floating pellets in humans. Eur J Pharm Biopharm 2002;53(1):29-35
  • Gambhire MN, Ambade KW, Kurmi SD, et al. Development and in vitro evaluation of an oral floating matrix tablet formulation of diltiazem hydrochloride. AAPS Pharm Sci Tech 2007;8(3):E1-E9
  • Chavanpatil M, Jain P, Chaudhari S, et al. Development of sustained release gastroretentive drug delivery system for ofloxacin: in vitro and in vivo evaluation. Int J Pharm 2005;304(1-2):178-84
  • Chauhan H, Shimpi S, Mahadik KR, Paradkar A. Preparation and evaluation of floating risedronate sodium-Gelucire (R) 43/01 formulations. Drug Dev Ind Pharm 2005;31(9):851-60

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.