229
Views
14
CrossRef citations to date
0
Altmetric
Review

Role of oxidative stress and antioxidant therapy in acute and chronic phases of sulfur mustard injuries: a review

, , , , &
Pages 9-17 | Received 23 Mar 2018, Accepted 26 Jun 2018, Published online: 10 Sep 2018

References

  • Paromov V, Suntres Z, Smith M, et al. Sulfur mustard toxicity following dermal exposure: role of oxidative stress, and antioxidant therapy. J Burns Wounds 2007;7:e7.
  • Namazi S, Niknahad H, Razmkhah H. Long-term complications of sulphur mustard poisoning in intoxicated Iranian veterans. J Med Toxicol 2009;5:191–195.
  • Kehe K, Szinicz L. Medical aspects of sulphur mustard poisoning. Toxicology 2005;214:198–209.
  • Balali M. Clinical and laboratory findings in Iranian fighters with chemical gas poisoning. Archiv Belges 1984;(Suppl):254–259.
  • Vijayaraghavan R. Modifications of breathing pattern induced by inhaled sulphur mustard in mice. Arch Toxicol 1997;71:157–164.
  • Khateri S, Ghanei M, Keshavarz S, et al. Incidence of lung, eye, and skin lesions as late complications in 34,000 Iranians with wartime exposure to mustard agent. J Occup Environ Med 2003;45:1136–1143.
  • Rowell M, Kehe K, Balszuweit F, et al. The chronic effects of sulfur mustard exposure. Toxicology 2009;263:9–11.
  • Ghanei M, Harandi AA. Molecular and cellular mechanism of lung injuries due to exposure to sulfur mustard: a review. Inhal Toxicol 2011;23:363–371.
  • Ghabili K, Agutter PS, Ghanei M, et al. Mustard gas toxicity: the acute and chronic pathological effects. J Appl Toxicol 2010;30:627–643.
  • Shohrati M, Peyman M, Peyman A, et al. Cutaneous and ocular late complications of sulfur mustard in Iranian veterans. Cutan Ocul Toxicol 2007;26:73–81.
  • Emadi S, Kaffashi M, Poursaleh Z, et al. Sulfur mustard-induced poikiloderma: a case report. Cutan Ocul Toxicol 2011;30:170–174.
  • Mahmoudi M, Hefazi M, Rastin M, et al. Long-term hematological and immunological complications of sulfur mustard poisoning in Iranian veterans. Int Immunopharmacol 2005;5:1479–1485.
  • Balali-Mood M, Hefazi M. Comparison of early and late toxic effects of sulfur mustard in Iranian veterans. Basic Clin Pharmacol Toxicol 2006;99:273–282.
  • Firooz A, Sadr B, Davoudi SM, et al. Long-term skin damage due to chemical weapon exposure. Cutan Ocul Toxicol 2011;30:64–68.
  • Zafarghandi MR, Soroush MR, Mahmoodi M, et al. Incidence of cancer in Iranian sulfur mustard exposed veterans: a long-term follow-up cohort study. Cancer Causes Control 2013;24:99–105.
  • Hefazi M, Maleki M, Mahmoudi M, et al. Delayed complications of sulfur mustard poisoning in the skin and the immune system of Iranian veterans 16-20 years after exposure. Int J Dermatol 2006;45:1025–1031.
  • Shahriary A, Mehrani H, Ghanei M, et al. Comparative proteome analysis of peripheral neutrophils from sulfur mustard-exposed and COPD patients. J Immunotoxicol 2015;12:132–139.
  • Balali-Mood M, Hefazi M. The clinical toxicology of sulfur mustard. Prehosp Disaster Med 2005;8:162–179.
  • Akhlaghpoor S, Ahari AA, Shabestari AA, et al. Comparison of virtual bronchoscopy with fiberoptic bronchoscopy findings in patients exposed to sulfur mustard gas. Acta Radiol 2011;52:1095–1100.
  • Shohrati M, Ghanei M, Shamspour N, et al. Activity and function in lung injuries due to sulphur mustard. Biomarkers 2008;13:728–733.
  • Mirbagheri L, Habibi Roudkenar M, Imani Fooladi AA, et al. Downregulation of super oxide dismutase level in protein might be due to sulfur mustard induced toxicity in lung. Iran J Allergy Asthma Immunol 2013;12:153–160.
  • Tahmasbpour E, Ghanei M, Khor A, et al. Altered expression of cyclooxygenase-2, 12-lipoxygenase, inducible nitric oxide synthase-2 and surfactant protein D in lungs of patients with pulmonary injury caused by sulfur mustard. Drug Chem Toxicol 2018;1–7.
  • Tahmasbpour E, Ghanei M, Qazvini A, et al. Gene expression profile of oxidative stress and antioxidant defense in lung tissue of patients exposed to sulfur mustard. Mutat Res Genet Toxicol Environ Mutagen 2016;800:12–21.
  • Ghanei M, Mokhtari M, Mohammad MM, et al. Bronchiolitis obliterans following exposure to sulfur mustard: chest high resolution computed tomography. Eur J Radiol 2004;52:164–169.
  • Ghanei M, Eshraghi M, Jalali AR, et al. Evaluation of latent hemoptysis in Sulfur Mustard injured patients. Environ Toxicol Pharmacol 2006;22:128–130.
  • Pishgoo B, Ghanei M, Harandi AA, et al. Long term cardiac abnormality after single high dose exposure to sulfur mustard? Indian Heart J 2007;59:181–184.
  • Ghanei M, Adibi I, Farhat F, et al. Late respiratory effects of sulfur mustard: how is the early symptoms severity involved? Chron Respir Dis 2008;5:95–100.
  • Ghanei M, Harandi AA. Lung carcinogenicity of sulfur mustard. Clin Lung Cancer 2010;11:13–17.
  • Ghabili K, Agutter PS, Ghanei M, et al. Sulfur mustard toxicity: history, chemistry, pharmacokinetics, and pharmacodynamics. Crit Rev Toxicol 2011;41:384–403.
  • Panahi Y, Roshandel D, Sadoughi MM, et al. Sulfur mustard-induced ocular injuries: update on mechanisms and management. Curr Pharm Des 2017;23:1589–1597.
  • Ghanei M, Poursaleh Z, Harandi AA, et al. Acute and chronic effects of sulfur mustard on the skin: a comprehensive review. Cutan Ocul Toxicol 2010;29:269–277.
  • Emadi S, Aslani J, Poursaleh Z, et al. Comparison late cutaneous complications between exposure to sulfur mustard and nerve agents. Cutan Ocul Toxicol 2012;31:214–219.
  • Emadi S, Moeineddin F, Sorush M. Urinary and cutaneous complications of sulphur mustard poisoning preceding pulmonary and ocular involvement: an unusual sequence of symptoms. Clin Exp Dermatol 2009;34:e7–e10.
  • Panahi Y, Ghanei M, Ghabili K, et al. Acute and chronic pathological effects of sulfur mustard on genitourinary system and male fertility. Urol J 2013;10:837–846.
  • Tahmasbpour Marzony E, Ghanei M, Panahi Y. Relationship of oxidative stress with male infertility in sulfur mustard-exposed injuries. Asian Pac J Reprod 2016;5:1–9.
  • Saber H, Saburi A, Ghanei M. Clinical and paraclinical guidelines for management of sulfur mustard induced bronchiolitis obliterans; from bench to bedside. Inhal Toxicol 2012;24:900–906.
  • Iravani S, Rahnavardi M, Gorouhi F, et al. Repeated gastrointestinal malignancies in a victim of sulfur mustard gas attack. Indian J Gastroenterol 2007;26:102.
  • Hassan ZM, Ebtekar M, Ghanei M, et al. Immunobiological consequences of sulfur mustard contamination. Iran J Allergy Asthma Immunol 2006;5:101–108.
  • Panahi Y, Jadidi-Niaragh F, Jamalkandi SA, et al. Immunology of chronic obstructive pulmonary disease and sulfur mustard induced airway injuries: implications for immunotherapeutic interventions. Curr Pharm Des 2016;22:2975–2996.
  • Jafari M, Ghanei M. Evaluation of plasma, erythrocytes, and bronchoalveolar lavage fluid antioxidant defense system in sulfur mustard-injured patients. Clin Toxicol 2010;48:184–192.
  • Ghanei M, Harandi AA. Long term consequences from exposure to sulfur mustard: a review. Inhal Toxicol 2007;19:451–456.
  • Najafi A, Masoudi-Nejad A, Imani Fooladi AA, et al. Microarray gene expression analysis of the human airway in patients exposed to sulfur mustard. J Recept Signal Transduct Res 2014;34:283–289.
  • Gerecke DR, Chen M, Isukapalli SS, et al. Differential gene expression profiling of mouse skin after sulfur mustard exposure: extended time response and inhibitor effect. Toxicol Appl Pharmacol 2009;234:156–165.
  • Brimfield AA, Zweig LM, Novak MJ, et al. In vitro oxidation of the hydrolysis product of sulfur mustard, 2,2'-thiobis-ethanol, by mammalian alcohol dehydrogenase. J Biochem Mol Toxicol 1998;12:361–369.
  • Balali-Mood M, Hefazi M, Mahmoudi M, et al. Long-term complications of sulphur mustard poisoning in severely intoxicated Iranian veterans. Fundam Clin Pharmacol 2005;19:713–721.
  • Tahmasbpour E, Reza Emami S, Ghanei M, et al. Role of oxidative stress in sulfur mustard-induced pulmonary injury and antioxidant protection. Inhal Toxicol 2015;27:659–672.
  • Jowsey PA, Williams FM, Blain PG. DNA damage responses in cells exposed to sulphur mustard. Toxicol Lett 2012;209:1–10.
  • Moser J, Levine CF, Thomas-Dunmeyer DR, et al. Cross-linking interferes with assessing sulfur mustard-induced DNA damage in human peripheral blood lymphocytes using the comet assay. Toxicol Mech Methods 2004;14:195–202.
  • Gross CL, Meier HL, Papirmeister B, et al. Sulfur mustard lowers nicotinamide adenine dinucleotide concentrations in human skin grafted to athymic nude mice. Toxicol Appl Pharmacol 1985;81:85–90.
  • Papirmeister B, Gross CL, Meier HL, et al. Molecular basis for mustard-induced vesication. Fundam Appl Toxicol 1985;5:S134–S149.
  • Ray R, Legere RH, Majerus BJ, et al. Sulfur mustard-induced increase in intracellular free calcium level and arachidonic acid release from cell membrane. Toxicol Appl Pharmacol 1995;131:44–52.
  • Orrenius S, McConkey DJ, Bellomo G, et al. Role of Ca2+ in toxic cell killing. Trends Pharmacol Sci 1989;10:281–285.
  • Nicotera P, Bellomo G, Orrenius S. Calcium-mediated mechanisms in chemically induced cell death. Annu Rev Pharmacol Toxicol 1992;32:449–470.
  • Pounds JG. The role of cell calcium in current approaches to toxicology. Environ Health Perspect 1990;84:7–15.
  • Pirzad G, Jafari M, Tavana S, et al. The role of Fas-FasL signaling pathway in induction of apoptosis in patients with sulfur mustard-induced chronic bronchiolitis. J Toxicol 2010;2010:373612.
  • Korkmaz A, Tan DX, Reiter RJ. Acute and delayed sulfur mustard toxicity; novel mechanisms and future studies. Interdiscip Toxicol 2008;1:22–26.
  • Simons T, Steinritz D, Bolck B, et al. Sulfur mustard-induced epigenetic modifications over time – a pilot study. Toxicol Lett 2018;293:45–50.
  • Tahmasbpour E, Balasubramanian D, Agarwal A. A multi-faceted approach to understanding male infertility: gene mutations, molecular defects and assisted reproductive techniques (ART). J Assist Reprod Genet 2014;31:1115–1137.
  • Steinritz D, Schmidt A, Balszuweit F, et al. Epigenetic modulations in early endothelial cells and DNA hypermethylation in human skin after sulfur mustard exposure. Toxicol Lett 2016;244:95–102.
  • Colagar AH, Marzony ET. Ascorbic Acid in human seminal plasma: determination and its relationship to sperm quality. J Clin Biochem Nutr 2009;45:144–149.
  • Aliev G, Obrenovich ME, Reddy VP, et al. Antioxidant therapy in Alzheimer's disease: theory and practice. Mini Rev Med Chem 2008;8:1395–1406.
  • Colagar AH, Marzony ET, Chaichi MJ. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009;29:82–88.
  • Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes 2015;6:456–480.
  • Mota SI, Costa RO, Ferreira IL, et al. Oxidative stress involving changes in Nrf2 and ER stress in early stages of Alzheimer's disease. Biochim Biophys Acta 2015;1852:1428–1441.
  • Yen CY, Hou MF, Yang ZW, et al. Concentration effects of grape seed extracts in anti-oral cancer cells involving differential apoptosis, oxidative stress, and DNA damage. BMC Complement Altern Med 2015;15:94.
  • Kumar D, Tewari-Singh N, Agarwal C, et al. Nitrogen mustard exposure of murine skin induces DNA damage, oxidative stress and activation of MAPK/Akt-AP1 pathway leading to induction of inflammatory and proteolytic mediators. Toxicol Lett 2015;235:161–171.
  • Pohanka M, Sobotka J, Svobodova H, et al. Sulfur mustard induced oxidative stress and its alteration using asoxime (HI-6). Interdiscip Toxicol 2013;6:198–202.
  • Jain AK, Tewari-Singh N, Gu M, et al. Sulfur mustard analog, 2-chloroethyl ethyl sulfide-induced skin injury involves DNA damage and induction of inflammatory mediators, in part via oxidative stress, in SKH-1 hairless mouse skin. Toxicol Lett 2011;205:293–301.
  • Gould NS, White CW, Day BJ. A role for mitochondrial oxidative stress in sulfur mustard analog 2-chloroethyl ethyl sulfide-induced lung cell injury and antioxidant protection. J Pharmacol Exp Ther 2009;328:732–739.
  • Brimfield AA, Soni SD, Trimmer KA, et al. Metabolic activation of sulfur mustard leads to oxygen free radical formation. Free Radic Biol Med 2012;52:811–817.
  • Inturi S, Tewari-Singh N, Gu M, et al. Mechanisms of sulfur mustard analog 2-chloroethyl ethyl sulfide-induced DNA damage in skin epidermal cells and fibroblasts. Free Radic Biol Med 2011;51:2272–2280.
  • Cook JR, Van Buskirk RG. A double-label technique that monitors sulfur mustard damage to nuclei and mitochondria of normal human epidermal keratinocytes in vitro. Toxicol Pathol 1997;25:481–486.
  • Ray R, Keyser B, Benton B, et al. Sulfur mustard induces apoptosis in cultured normal human airway epithelial cells: evidence of a dominant caspase-8-mediated pathway and differential cellular responses. Drug Chem Toxicol 2008;31:137–148.
  • Panahi Y, Davoudi SM, Beiraghdar F, et al. Serum levels of interleukins 2, 4, 6, and 10 in veterans with chronic sulfur mustard-induced pruritus: a cross-sectional study. Skinmed 2013;11:205–209.
  • Khaheshi I, Keshavarz S, Imani Fooladi AA, et al. Loss of expression of TGF-betas and their receptors in chronic skin lesions induced by sulfur mustard as compared with chronic contact dermatitis patients. BMC Dermatol 2011;11:2.
  • Shohrati M, Amini-Harandi A, Najafian B, et al. The role of serum level of interleukin-6 in severity of pulmonary complications of sulfur mustard injuries. Iran J Med Sci 2014;39:382–386.
  • Tahmasbpour Marzony E, Nejad-Moghadam A, Ghanei M, et al. Sulfur mustard causes oxidants/antioxidants imbalance through the overexpression of free radical producing-related genes in human mustard lungs. Environ Toxicol Pharmacol 2016;45:187–192.
  • Nourani MR, Azimzadeh S, Ghanei M, et al. Expression of glutathione S-transferase variants in human airway wall after long-term response to sulfur mustard. J Recept Signal Transduct Res 2014;34:125–130.
  • Dudek H, Farbiszewski R, Michno T, et al. [Activity of glutathione peroxidase (GSH-Px), glutathione reductase (GSSG-R) and superoxide dismutase (SOD-1) in single brain metastasis]. Wiad Lek 2002;55:252–256.
  • Batal M, Rebelo-Moreira S, Hamon N, et al. A guanine-ethylthioethyl-glutathione adduct as a major DNA lesion in the skin and in organs of mice exposed to sulfur mustard. Toxicol Lett 2015;233:1–7.
  • Escribano A, Amor M, Pastor S, et al. Decreased glutathione and low catalase activity contribute to oxidative stress in children with alpha-1 antitrypsin deficiency. Thorax 2015;70:82–83.
  • Sawyer TW, Lundy PM, Weiss MT. Protective effect of an inhibitor of nitric oxide synthase on sulphur mustard toxicity in vitro. Toxicol Appl Pharmacol 1996;141:138–144.
  • Korkmaz A, Kunak ZI, Paredes SD, et al. The use of melatonin to combat mustard toxicity. REVIEW. Neuro Endocrinol Lett 2008;29:614–619.
  • Weinberger B, Laskin JD, Sunil VR, et al. Sulfur mustard-induced pulmonary injury: therapeutic approaches to mitigating toxicity. Pulm Pharmacol Ther 2011;24:92–99.
  • Ishida H, Ray R, Amnuaysirikul J, et al. Nitric oxide synthase gene transfer overcomes the inhibition of wound healing by sulfur mustard in a human keratinocyte in vitro model. ISRN Toxicol 2012;2012:190429.
  • Rappeneau S, Baeza SA, Marano F, et al. Efficient protection of human bronchial epithelial cells against sulfur and nitrogen mustard cytotoxicity using drug combinations. Toxicol Sci 2000;58:153–160.
  • Tewari-Singh N, Inturi S, Jain AK, et al. Catalytic antioxidant AEOL 10150 treatment ameliorates sulfur mustard analog 2-chloroethyl ethyl sulfide-associated cutaneous toxic effects. Free Radic Biol Med 2014;72:285–295.
  • Sunil VR, Patel-Vayas K, Shen J, et al. Role of TNFR1 in lung injury and altered lung function induced by the model sulfur mustard vesicant, 2-chloroethyl ethyl sulfide. Toxicol Appl Pharmacol 2011;250:245–255.
  • Gautam A, Vijayaraghavan R. Prophylactic effect of gossypin against percutaneously administered sulfur mustard. Biomed Environ Sci 2007;20:250–259.
  • Shohrati M, Karimzadeh I, Saburi A, et al. The role of N-acetylcysteine in the management of acute and chronic pulmonary complications of sulfur mustard: a literature review. Inhal Toxicol 2014;26:507–523.
  • Anderson DR, Taylor SL, Fetterer DP, et al. Evaluation of protease inhibitors and an antioxidant for treatment of sulfur mustard-induced toxic lung injury. Toxicology 2009;263:41–46.
  • O'Neill HC, White CW, Veress LA, et al. Treatment with the catalytic metalloporphyrin AEOL 10150 reduces inflammation and oxidative stress due to inhalation of the sulfur mustard analog 2-chloroethyl ethyl sulfide. Free Radic Biol Med 2010;48:1188–1196.
  • Pohanka M. Antioxidants countermeasures against sulfur mustard. Mini Rev Med Chem 2012;12:742–748.
  • Panahi Y, Ghanei M, Bashiri S, et al. Short-term curcuminoid supplementation for chronic pulmonary complications due to sulfur mustard intoxication: positive results of a randomized double-blind placebo-controlled trial. Drug Res (Stuttg) 2015;65:567–573.
  • Panahi Y, Ghanei M, Hajhashemi A, et al. Effects of curcuminoids-piperine combination on systemic oxidative stress, clinical symptoms and quality of life in subjects with chronic pulmonary complications due to sulfur mustard: a randomized controlled trial. J Diet Suppl 2016;13:93–105.
  • Ghanei M, Shohrati M, Jafari M, et al. N-Acetylcysteine improves the clinical conditions of mustard gas-exposed patients with normal pulmonary function test. Basic Clin Pharmacol Toxicol 2008;103:428–432.
  • Panahi Y, Ghanei M, Vahedi E, et al. Efficacy of probiotic supplementation on quality of life and pulmonary symptoms due to sulfur mustard exposure: a randomized double-blind placebo-controlled trial. Drug Chem Toxicol 2017;40:24–29.
  • Nejad-Moghaddam A, Ajdary S, Tahmasbpour E, et al. Immunomodulatory properties of mesenchymal stem cells can mitigate oxidative stress and inflammation process in human mustard lung. Biochem Genet 2016;54:769–783.
  • Mousavi S, Shohrati M, Vahedi E, et al. Effect of melatonin administration on sleep quality in sulfur mustard exposed patients with sleep disorders. Iran J Pharm Res 2018;17:136–144.
  • Panahi Y, Ghanei M, Vahedi E, et al. Effect of recombinant human IFNgamma in the treatment of chronic pulmonary complications due to sulfur mustard intoxication. J Immunotoxicol 2014;11:72–77.
  • Gholamnezhad Z, Boskabady MH, Amery S, et al. The effect of vitamin E on lung pathology in sulfur mustard-exposed guinea pigs. Toxicol Ind Health 2016;32:1971–1977.
  • Boskabady MH, Amery S, Vahedi N, et al. The effect of vitamin E on tracheal responsiveness and lung inflammation in sulfur mustard exposed guinea pigs. Inhal Toxicol 2011;23:157–165.
  • Ucar M, Korkmaz A, Reiter RJ, et al. Melatonin alleviates lung damage induced by the chemical warfare agent nitrogen mustard. Toxicol Lett 2007;173:124–131.
  • Pohanka M, Sobotka J, Jilkova M, et al. Oxidative stress after sulfur mustard intoxication and its reduction by melatonin: efficacy of antioxidant therapy during serious intoxication. Drug Chem Toxicol 2011;34:85–91.
  • Balszuweit F, Menacher G, Schmidt A, et al. Protective effects of the thiol compounds GSH and NAC against sulfur mustard toxicity in a human keratinocyte cell line. Toxicol Lett 2016;244:35–43.
  • Steinritz D, Bolck B, Schwarz J, et al. Effect of N-acetyl cysteine and alpha-linolenic acid on sulfur mustard caused impairment of in vitro endothelial tube formation. Toxicol Sci 2010;118:521–529.
  • Saberi M, Zaree Mahmodabady A. The protective effects of N-acetyl-cysteine, oxo-thiazolidine-carboxylate, acetaminophen and their combinations against sulfur mustard cytotoxicity on human skin fibroblast cell line (HF2FF). Iran Biomed J 2009;13:215–221.
  • Tewari-Singh N, Agarwal C, Huang J, et al. Efficacy of glutathione in ameliorating sulfur mustard analog-induced toxicity in cultured skin epidermal cells and in SKH-1 mouse skin in vivo. J Pharmacol Exp Ther 2011;336:450–459.
  • Hoesel LM, Flierl MA, Niederbichler AD, et al. Ability of antioxidant liposomes to prevent acute and progressive pulmonary injury. Antioxid Redox Signal 2008;10:973–981.
  • Mukherjee S, Stone WL, Yang H, et al. Protection of half sulfur mustard gas-induced lung injury in guinea pigs by antioxidant liposomes. J Biochem Mol Toxicol 2009;23:143–153.
  • Panahi Y, Rajaee SM, Sahebkar A. Ocular effects of sulfur mustard and therapeutic approaches. J Cell Biochem 2017;118:3549–3560.
  • Jugg B, Fairhall S, Smith A, et al. N-Acetyl-l-cysteine protects against inhaled sulfur mustard poisoning in the large swine. Clin Toxicol 2013;51:216–224.
  • Siegert M, Kranawetvogl A, Thiermann H, et al. N-Acetylcysteine as a chemical scavenger for sulfur mustard: new insights by mass spectrometry. Drug Test Anal 2018;10:243–253.
  • Wigenstam E, Rocksen D, Ekstrand-Hammarstrom B, et al. Treatment with dexamethasone or liposome-encapsuled vitamin E provides beneficial effects after chemical-induced lung injury. Inhal Toxicol 2009;21:958–964.
  • Naghii MR. Sulfur mustard intoxication, oxidative stress, and antioxidants. Military Med 2002;167:573–575.
  • Kim S, Jeong KJ, Cho SK, et al. Caffeic acid, morin hydrate and quercetin partially attenuate sulfur mustard-induced cell death by inhibiting the lipoxygenase pathway. Mol Med Rep 2016;14:4454–4460.

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.