657
Views
22
CrossRef citations to date
0
Altmetric
Review Article

Helicobacter pylori infection: A brief overview on alternative natural treatments to conventional therapy

, , &
Pages 94-105 | Received 12 Nov 2013, Accepted 04 Feb 2014, Published online: 10 Mar 2014

References

  • Algood HMS, Cover TL. (2006). Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin Microbiol Rev 19:597–613
  • Altiok D, Altiok E, Bayraktar O, et al. (2009). Stability of trans-resveratrol incorporated in chitosan microspheres. 14th National Biomedical Engineering Meeting.
  • Andersson AF, Lindberg M, Jakobsson H, et al. (2008). Comparative analysis of human gut microbiota by barcoded pyrosequencing. PloS One 3:e2836
  • American Cancer Society. Available from: http://www.cancer.org/cancer/stomachcancer/detailedguide/stomach-cancer-survival-rates [last accessed 12 Oct 2013]
  • Atherton JC. (2006). The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Ann Rev Pathol 1:63–96
  • Azevedo NF, Guimaraes N, Figueiredo C, et al. (2007). A new model for the transmission of Helicobacter pylori: role of environmental reservoirs as gene pools to increase strain diversity. Crit Rev Microbiol 33:157–69
  • Bik EM, Eckburg PB, Gill SR, et al. (2006). Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 103:732–7
  • Blaser MJ, Atherton JC. (2004). Helicobacter pylori persistence: biology and disease. J Clin Invest 113:321–33
  • Brogden KA. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–50
  • Brown LM. (2000). Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev 22:283–97
  • Burger O, Ofek I, Tabak M, et al. (2000). A high molecular mass constituent of cranberry juice inhibits Helicobacter pylori adhesion to human gastric mucus. FEMS Immunol Med Microbiol 29:295–301
  • Campo SMA, Zullo A, Hassan C, et al. (2007). Antibiotic treatment strategies for Helicobacter pylori infection. Recent Patents Anti-Infective Drug Discovery 2:11–17
  • Castro M, Romero C, de Castro A, et al. (2012). Assessment of Helicobacter pylori eradication by virgin olive oil. Helicobacter 17:305–11
  • Censini S, Lange C, Xiang Z, et al. (1996). CAG, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93:14648–53
  • Chang C-H, Huang W-Y, Lai C-H, et al. (2011). Development of novel nanoparticles shelled with heparin for berberine delivery to treat Helicobacter pylori. Acta Biomater 7:593–603
  • Chen L, Li Y, Li J, et al. (2007). An antimicrobial peptide with antimicrobial activity against Helicobacter pylori. Peptides 28:1527–31
  • Conway BR. (2005). Drug delivery strategies for the treatment of Helicobacter pylori infections. Curr Pharm Des 11:775–90
  • Correa P, Houghton J. (2007). Carcinogenesis of Helicobacter pylori. Gastroenterology 133:659–72
  • Correia M, Michel V, Matos A, et al. (2012). Docosahexaenoic acid inhibits Helicobacter pylori growth In vitro and mice gastric mucosa colonization. PloS One 7:e35072
  • Costa F, Carvalho IF, Montelaro RC, et al. (2011). Covalent immobilization of antimicrobial peptides (AMPs) onto biomaterial surfaces. Acta Biomater 7:1431–40
  • Cowan MM. (1999). Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–82
  • Daroch F, Hoeneisen M, Gonzalez C, et al. (2001). In vitro antibacterial activity of Chilean red wines against Helicobacter pylori. Microbios 104:79–85
  • Das UN, Ramadevi G, Rao KP, et al. (1989). Prostaglandins can modify gamma-radiation and chemical induced cytotoxicity and genetic damage In vitro and In vivo. Prostaglandins 38:689–716
  • Deacon MP, McGurk S, Roberts CJ, et al. (2000). Atomic force microscopy of gastric mucin and chitosan mucoadhesive systems. Biochem J 348:557–63
  • Ding S-Z, Minohara Y, Fan XJ, et al. (2007). Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 75:4030–9
  • Domínguez de María P, Maugeri Z. (2011). Ionic liquids in biotransformations: from proof-of-concept to emerging deep-eutectic-solvents. Curr Opin Chem Biol 15:220–5
  • Eaton KA, Brooks CL, Morgan DR, et al. (1991). Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun 59:2470–5
  • Eaton KA, Morgan DR, Krakowka S. (1992). Motility as a factor in the colonisation of gnotobiotic piglets by Helicobacter pylori. J Med Microbiol 37:123–7
  • Eaton KA, Suerbaum S, Josenhans C, et al. (1996). Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect Immun 64:2445–8
  • Engstrand L, Lindberg M. (2013). Helicobacter pylori and the gastric microbiota. Best Pract Res Clin Gastroenterol 27:39–45
  • Erah PO, Goddard AF, Barrett, DA, et al. (1997). The stability of amoxycillin, clarithromycin and metronidazole in gastric juice: relevance to the treatment of Helicobacter pylori infection. J Antimicrob Chemother 39:5–12
  • Ferlay J, Parkin DM, Steliarova-Foucher E. (2010). Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 1990 46:765–81
  • Fernandes J, Gomes F, Couto J, et al. (2007). The antimicrobial effect of wine on Listeria innocua in a model stomach system. Food Control 18:1477–83
  • Fernandes M, Gonçalves IC, Nardecchia S, et al. (2013). Modulation of stability and mucoadhesive properties of chitosan microspheres for therapeutic gastric application. Int J Pharm 454:116–24
  • Fernández-Bolaños JG, López O, López-García MA, et al. (2012). Biological properties of hydroxytyrosol and its derivatives, olive oil – constituents, quality, health properties and bioconversions, Dr. Dimitrios Boskou (Ed.), ISBN: 978-953-307-921-9, InTech
  • Frieri G, Pimpo M, Palombieri A. (2000). Polyunsaturated fatty acid dietary supplementation: an adjuvant approach to treatment of Helicobacter pylori infection. Nutr Res 20:907–16
  • Fuchs PC, Barry AL, Brown SD. (1998). In vitro antimicrobial activity of MSI-78, a magainin analog. Antimicrob Agents Chemother 42:1213–16
  • Gaby AR. (2001). Helicobacter pylori eradication: are there alternatives to antibiotics? Alter Med Rev 6:355–66
  • García-González DL, Aparicio-Ruiz R, Aparicio R. (2008). Virgin olive oil –chemical implications on quality and health. Eur J Lipid Sci Technol 110:602–7
  • Ge Y, MacDonald DL, Holroyd KJ, et al. (1999). In vitro antibacterial properties of pexiganan, an analog of magainin. Antimicrob Agents Chemother 43:782–8
  • Gisbert JP, Pajares JM. (2010). Treatment of Helicobacter pylori infection: the past and the future. Eur J Med 21:357–9
  • Goh K-L, Chan W-K, Shiota S, et al. (2010). Epidemiology of Helicobacter pylori Infection and public health implications. Helicobacter 16:1–7
  • Gonçalves IC, Magalhães A, Fernandes M, et al. (2013). Bacterial-binding chitosan microspheres for gastric infection treatment and prevention. Acta Biomater 9:9370–8
  • Gonzaga L, Coelho V, Margarida E, et al. (2007). Brazilian green propolis on Helicobacter pylori infection: a pilot clinical study. Helicobacter 12:572–4
  • Gottler LM, Ramamoorthy A. (2009). Structure, membrane orientation, mechanism, and function of pexiganan – a highly potent antimicrobial peptide designed from magainin. Biochim Biophys Acta 1788:1680–6
  • Goy RC, De Britto D, Assis OBG. (2009). A review of the antimicrobial activity of chitosan. Polimeros Ciencia Tecnologia. 19:241–7
  • Graham DY, Malaty HM, Evans DG, et al. (1991). Epidemiology of Helicobacter pyIori in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology 100:1491–501
  • Grant HW, Palmer KR, Riermesma R, et al. (1990). Duodenal ulcer is associated with low dietary linoleic acid intake. Gut 31:997–8
  • Graziani G, D’Argenio G, Tuccillo C, et al. (2005). Apple polyphenol extracts prevent damage to human gastric epithelial cells In vitro and to rat gastric mucosa In vivo. Gut 54:193–200
  • Greenway DL, Dyke, KG. (1960). Mechanism of the inhibitory action of linoleic acid on the growth of Staphylococcus aureus. J Gen Microbiol 115:179–96
  • Hejazi R, Amiji M. (2002). Stomach-specific anti-H. pylori therapy. I: preparation and characterization of tetracyline-loaded chitosan microspheres. Int J Pharma 235:87–94
  • Hejazi R, Amiji M. (2003). Stomach-specific anti-H. pylori therapy. II: gastric residence studies of tetracycline-loaded chitosan microspheres in gerbils. Pharma Dev Tech 8:253–62
  • Hejazi R, Amiji M. (2004). Stomach-specific anti-H. pylori therapy part III: effect of chitosan microspheres crosslinking on the gastric residence and local tetracycline concentrations in fasted gerbils. Int J Pharma 272:99–108
  • Higashi H, Tsutsumi R, Muto S, et al. (2002). SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295:683–6
  • Hollander D, Tarnawski A. (1991). Is there a role for dietary essential fatty acids in gastroduodenal mucosal protection? J Clin Gastroenterol 13:S72–4
  • Huang HW, Chen F-Y, Lee MT. (2004). Molecular mechanism of peptide-induced pores in membranes. Phys Rev Lett 92:198304-1–4
  • IARC. (1994). IARC Monographs on the evaluation of carcinogenic risks to humans. Schistosomes, liver flukes and Helicobacter pylori. IARC 61:177–240
  • Ilver D, Arnqvist A, Ogren J, et al. (1998). Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373–7
  • Iwahori A, Hirota Y, Sampe R, et al. (1997). On the antibacterial activity of normal and reversed magainin 2 analogs against Helicobacter pylori. Biol Pharma 20:805–8
  • Jäger S, Trojan H, Kopp T, et al. (2009). Pentacyclic triterpene distribution in various plants – rich sources for a new group of multi-potent plant extracts. Molecules 14:2016–31
  • Jang M, Cai L, Udeani G, et al. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 5297:218–20
  • Jemal A, Bray F, Center MM, et al. (2011). Global Cancer Statistics. CA Cancer J Clin 61:69–90
  • Khulusi S, Ahmed HA, Patel P, et al. (1995). The effects of unsaturated fatty acids on Helicobacter pylori In vitro. J Med Microbiol 42:276–82
  • Koivisto TT, Rautelin HI, Voutilainen ME, et al. (2005). First-line eradication therapy for Helicobacter pylori in primary health care based on antibiotic resistance: results of three eradication regimens. Aliment Pharmacol Ther 21:773–82
  • Kong M, Chen XG, Xing K, et al. (2010). Antimicrobial properties of chitosan and mode of action: a state of the art review. Int J Food Microbiol 144:51–63
  • Konturek JW. (2003). Discovery by Jaworski of Helicobacter pylori and its pathogenetic role in peptic ulcer, gastritis and gastric cancer. J Physiol Pharmacol 54:23–41
  • Lee JY, Hwang DH. (2006). The modulation of inflammatory gene expression by lipids: mediation through Toll-like receptors. Mol Cells 21:174–85
  • Lewis K. (2013). Platforms for antibiotic discovery. Nat Rev Drug Discov 12:371–87
  • Li Y, Xu C, Zhang Q, et al. (2005). In vitro anti-Helicobacter pylori action of 30 Chinese herbal medicines used to treat ulcer diseases. J Ethnopharmacol 98:329–33
  • Lin YT, Kwon YI, Labbe RG, et al. (2005). Inhibition of Helicobacter pylori and associated urease by oregano and cranberry phytochemical synergies. Appl Environ Microbiol 71:8558–64
  • Magalhães A, Ismail MN, Reis CA. (2010). Sweet receptors mediate the adhesion of the gastric pathogen Helicobacter pylori: glycoproteomic strategies. Expert Rev Proteomics 7:307–10
  • Mahady G, Pendland S. (2000). Resveratrol inhibits the growth of Helicobacter pylori In vitro. Am J Gastroenterol 96:1849
  • Mahady G, Pendland S, Chadwick LR. (2003). Resveratrol and red wine extracts inhibit the growth of CagA+ strains of Helicobacter pylori In vitro. Am J Gastroenterol 98:1440–1
  • Mahdavi J, Sondén B, Hurtig M, et al. (2002). Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573–8
  • Malfertheiner P, Megraud F, O’Morain CA, et al. (2012). Management of Helicobacter pylori infection-the Maastricht IV/Florence Consensus Report. Gut 61:646–64
  • Maloy WL, Kari UP. (1995). Structure-activity studies on magainins and other host defense peptides. Biopolymers 37:105–22
  • Manach C, Scalbert A, Morand C, et al. (2004). Polyphenols: food sources and bioavailability. Am J Clin Nutr 79:727–47
  • Manunza B, Deiana S, Pintore M, et al. (1999). The binding mechanism of urea, hydroxamic acid and N-(N-butyl)-phosphoric triamide to the urease active site: a comparative molecular dynamics study. Soil Biol Biochem 31:789–96
  • Matsuzaki K, Murase O, Fujii N, et al. (1995). Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 34:6521–6
  • McChesney JD, Venkataraman SK, Henri JT. (2007). Plant natural products: back to the future or into extinction? Phytochemistry 68:2015–22
  • McNulty CA, Wilson MP, Havinga W, et al. (2001). A pilot study to determine the effectiveness of garlic oil capsules in the treatment of dyspeptic patients with Helicobacter pylori. Helicobacter 6:249–53
  • Medina E, Brenes M, García A, et al. (2009). Bactericidal activity of glutaraldehyde-like compounds from olive products. J Food Prot 72:2611–14
  • Mégraud F. (2005). A humble bacterium sweeps this year’s Nobel Prize. Cell 123:975–6
  • Nakajima S, Fujita K, Inoue Y, et al. (2006). Effect of the folk remedy, Bainiku-ekisu, a concentrate of Prunus mume juice, on Helicobacter pylori infection in humans. Helicobacter 11:589–91
  • Nogueira F, Gonçalves IC, Martins MCL. (2012). Effect of gastric environment on Helicobacter pylori adhesion to a mucoadhesive polymer. Acta Biomater 9:5208–15
  • Nohynek LJ, Alakomi H-L, Kähkönen MP, et al. (2006). Berry phenolics: antimicrobial properties and mechanisms of action against severe human pathogens. Nutr Cancer 54:18–32
  • Nostro A, Cellini L, Di Bartolomeo S, et al. (2005). Antibacterial effect of plant extracts against Helicobacter pylori. Phytother Res 19:198–202
  • Oppenheim JJ, Biragyn A, Kwak LW, et al. (2003). Roles of antimicrobial peptides such as defensins in innate and adaptive immunity. Ann Rheum Dis 62:ii17–21
  • Oren Z, Shai Y. (1998). Mode of action of linear amphipathic alpha-helical antimicrobial peptides. Biopolymers 47:451–63
  • Pan-In P, Tachapruetinun A, Chaichanawongsaroj N, et al. (2013). Combating Helicobacter pylori infections with mucoadhesive nanoparticles loaded with Garcinia mangostana extract. Nanomedicine [Epub ahead of print]. doi:10.2217/NNM.13.30.
  • Paraschos S, Magiatis P, Mitakou S, et al. (2007). In vitro and In vivo activities of Chios mastic gum extracts and constituents against Helicobacter pylori. Antimicrob Agents Chemother 51:551–9
  • Parkin DM, Bray F, Ferlay J, et al. (2005). Global cancer statistics, 2002. CA Cancer J Clin 55:74–108
  • Pastene E, Speisky H, Troncoso M, et al. (2009a). In vitro inhibitory effect of apple peel extract on the growth of Helicobacter pylori and respiratory burst induced on human neutrophils. J Agric Food Chem 57:7743–9
  • Pastene E, Troncoso M, Figueroa G, et al. (2009b). Association between polymerization degree of apple peel polyphenols and inhibition of Helicobacter pylori urease. J Agric Food Chem 57:416–24
  • Pastene E, Speisky H, García A, et al. (2010). In vitro and in vivo effects of apple peel polyphenols against Helicobacter pylori. J Agric Food Chem 58:7172–9
  • Patel A, Shah N, Prajapati JB. (2013). Clinical appliance of probiotics in the treatment of Helicobacter pylori infection-a brief review. J Microbiol Immunol Infect [Epub ahead of print]. doi: 10.1016/j.jmii.2013.03.010
  • Paulo L, Oleastro M, Gallardo E, et al. (2011). Anti-Helicobacter pylori and urease inhibitory activities of resveratrol and red wine. Food Res Int 44:964–9
  • Peek RM, Blaser MJ. (2002). Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2:28–37
  • Perez-Perez GI, Rothenbacher D, Brenner H. (2004). Epidemiology of Helicobacter pylori infection. Helicobacter 9:1–6
  • Perry S, Sanchez ML, Yang S, et al. (2006). Gastroenteritis and transmission of Helicobacter pylori infection in households. Emerg Infect Dis 12:1701–8
  • Prabaharan M, Mano JF. (2005). Chitosan-based particles as controlled drug delivery systems. Drug Deliv 12:41–57
  • Raafat D, Von Bargen K, Haas A, et al. (2008). Insights into the mode of action of chitosan as an antibacterial compound. Appl Environ Microbiol 74:3764–73
  • Raafat D, Sahl H-G. (2009). Chitosan and its antimicrobial potential – a critical literature survey. Microb Biotechnol 2:186–201
  • Reddy KVR, Yedery RD, Aranha C. (2004). Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 24:536–47
  • Ricci V, Zarrilli R, Romano M. (2002). Voyage of Helicobacter pylori in human stomach: odyssey of a bacterium. Dig Liver Dis 3:42–8
  • Rohdewald P, Beil W. (2008). In vitro inhibition of Helicobacter pylori growth and adherence to gastric mucosal cells by Pycnogenol. Phytother Res 22:685–8
  • Romero C, Medina E, Vargas J, et al. (2007). In vitro activity of olive oil polyphenols against Helicobacter pylori. J Agricultural Food Chem 55:680–6
  • Rydning A, Børkje B, Lange O, et al. (1993). Effect of wheat fibre supplements on duodenal ulcer recurrence. Scand J Gastroenterol 28:1051–4
  • Samie A, Obi CL, Bessong PO, et al. (2005). Activity profiles of fourteen selected medicinal plants from Rural Venda communities in South Africa against fifteen clinical bacterial species. Afr J Biotechnol 4:1443–51
  • Sheu CW, Salomon D, Simmons JL, et al. (1975). Inhibitory effects of lipophilic acids and related compounds on bacteria and mammalian cells. Antimicrob Agents Chemother 7:349–63
  • Shin S-J, Park C-E, Baek N-I, et al. (2009). Betulinic and oleanolic acids isolated from Forsythia suspensa Vahl inhibit urease activity of Helicobacter pylori. Biotechnol Bioprocess Eng 14:140–5
  • Sogias I, Williams AC, Khutoryanskiy VV. (2008). Why is chitosan mucoadhesive? Biomacromolecules 9:1837–42
  • Solnick JV, Fong J, Hansen LM, et al. (2006). Acquisition of Helicobacter pylori infection in rhesus macaques is most consistent with oral-oral transmission. J Clin Microbiol 44:3799–803
  • Steer HW. (1975). Ultrastructure of cell migration throught the gastric epithelium and its relationship to bacteria. J Clin Pathol 28:639–46
  • Suerbaum S, Michetti P. (2002). Helicobacter pylori infection. N Engl J Med 347:1175–86
  • Sun CQ, O’Connor CJ, Roberton AM. (2003). Antibacterial actions of fatty acids and monoglycerides against Helicobacter pylori. FEMS Immun Med Microbiol 36:9–17
  • Suzuki T, Matsuo K, Ito H, et al. (2006). Smoking increases the treatment failure for Helicobacter pylori eradication. Am J Med 119:217–24
  • Thompson L, Cockayne A, Spiller RC. (1994a). Inhibitory effect of polyunsaturated fatty acids on the growth of Helicobacter pylori: a possible explanation of the effect of diet on peptic ulceration. Gut 35:1557–61
  • Vakil, N. (2006). Helicobacter pylori treatment: a practical approach. Am J Gastroenterol 101:497–9
  • Vaquero MJR, Alberto MR, Nadra MCM. (2007). Influence of phenolic compounds from wines on the growth of Listeria monocytogenes. Food Control 18:587–93
  • Waite JG, Daeschel MA. (2007). Contribution of wine components to inactivation of food-borne pathogens. J Food Sci 72:M286–91
  • Wang G, Tang W, Bidigare RR. (2005). Terpenoids as therapeutic drugs and pharmaceutical agents. In: Zhang L & Demain A eds. Natural Products Drug Discovery and Therapeutic Medicine. Totowa NJ: Humana Press, 197–227
  • Wang H-E, Chang C-H, Ker Y-B, et al. (2011). Fermented soybean liquid alleviated peptic ulcer through the destruction of acidic proton pump rather than suppression of urease of Helicobacter pylori: a kinetic analysis. J Agric Food Chem 59:6730–9
  • Waterman E, Lockwood B. (2007). Active components and clinical applications of olive oil. Altern Med 12:331–42
  • Wroblewski LE, Peek RM, Wilson KT. (2010). Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–39
  • Wu M, Maier E, Benz R et al. (1999). Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38:7235–42
  • Wu S, Chappell J. (2008). Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. Curr Opin Biotechnol 19:145–52
  • Yahiro K, Shirasaka D, Tagashira M, et al. (2005). Inhibitory effects of polyphenols on gastric injury by Helicobacter pylori VacA toxin. Helicobacter 10:231–9
  • Yeaman MR, Yount NY. (2003). Mechanisms of Antimicrobial Peptide Action and Resistance. Pharmacol Rev 55:27–55
  • Zaidi SFH, Ahmed K, Yamamoto T, et al. (2009). Effect of resveratrol on Helicobacter pylori-induced interleukin-8 secretion, reactive oxygen species generation and morphological changes in human gastric epithelial cells. Biol Pharma Bull 32:1931–5
  • Zasloff M. (1987). Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc Natl Acad Sci USA 84:5449–53
  • Zasloff M, Martin B, Chen HC. (1988). Antimicrobial activity of synthetic magainin peptides and several analogues. Proc Natl Acad Sci USA 85:910–13
  • Zheng CJ, Yoo J-S, Lee T-G, et al. (2005). Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Letters 579:5157–62
  • Zilberstein B, Quintanilha AG, Santos MAA, et al. (2007). Digestive tract microbiota in healthy volunteers. Clinics 62:47–54

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.