Advanced search
Publication Cover
Pharmacogenomics Volume 10, 2009 - Issue 9
Submit an article Journal homepage
255
Views
0
CrossRef citations to date
0
Altmetric
Review

Genetic Polymorphisms Associated with Acute Lung Injury

Anita J Reddy1 Respiratory Institute, Cleveland Clinic Health System, OH, USAView further author information
&
Steven R Kleeberger2 Laboratory of Respiratory Biology, National Institute of Environmental Health Sciences, National Institutes of Health, 111 TW Alexander Drive, Building 101, Rm D240, Research Triangle Park, NC27709, USA Tel.: +1 919 541 3540; Fax: +1 919 541 4133; [email protected]View further author information
Pages 1527-1539 | Published online: 17 Sep 2009

Bibliography

  • Goss CH , BrowerRG, HudsonLD, RubenfeldGD, ARDS Network: Incidence of acute lung injury in the United States. Crit. Care Med.31 , 1607–1611 (2003).
  • Bernard GR , ArtigasA, BrighamKL et al.: The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination.Am. J. Respir. Crit. Care Med.149 , 818–824 (1994).
  • Hudson LD , MilbergJA, AnardiD, MaunderRJ: Clinical risks for development of the acute respiratory distress syndrome.Am. J. Respir. Crit. Care Med.151 , 293–301 (1995).
  • Piantadosi CA , SchwartzDA: The acute respiratory distress syndrome.Ann. Intern. Med.141 , 460–470 (2004).
  • ARDS Net: Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N. Engl. J. Med.342 , 1301–1308 (2000).
  • Bernard GR , PROWESS study group: Efficacy and safety of recombinant human activated protein C for severe sepsis. N. Engl. J. Med.344 , 699–709 (2001).
  • Meduri GU , HeadleyS, KohlerG et al.: Persistent elevation of inflammatory cytokines predicts a poor outcome in ARDS. Plasma IL-1β and IL-6 levels are consistent and efficient predictors of outcome over time.Chest107 , 1062–1073 (1995).
  • Donnelly TJ , MeadeP, JagelsM et al.: Cytokine, complement, and endotoxin profiles associated with the development of the adult respiratory distress syndrome after severe injury.Crit. Care Med.22 , 768–776 (1994).
  • Thickett DR , ArmstrongL, MillarAB: A role for vascular endothelial growth factor in acute and resolving lung injury.Am. J. Respir. Crit. Care Med.166 , 1332–1337 (2002).
  • Zhai R , GongMN, ZhouW et al.: Genotypes and haplotypes of the VEGF gene are associated with higher mortality and lower VEGF plasma levels in patients with ARDS.Thorax62 , 718–722 (2007).
  • Prabhakaran P , WareLB, WhiteKE et al.: Elevated levels of plasminogen activator inhibitor-1 in pulmonary edema fluid are associated with mortality in acute lung injury.Am. J. Physiol. Lung Cell. Mol. Physiol.285 , L20–L28 (2003).
  • Pan T , NielsenLD, AllenMJ et al.: Serum SP-D is a marker of lung injury in rats.Am. J. Physiol. Lung Cell. Mol. Physiol.282 , L284–L832 (2002).
  • Kawut SM , OkunJ, ShimboD et al.: Soluble P-selectin and the risk of primary graft dysfunction after lung transplantation.Chest (2009).
  • Bhandari V , Choo-WingR, LeeCG et al.: Hyperoxia causes angiopoietin 2-mediated acute lung injury and necrotic cell death.Nat. Med.12 , 1286–1293 (2006).
  • Wang Z , BeachD, SuL, ZhaiR, ChristianiDC: A genome-wide expression analysis in blood identifies pre-elafin as a biomarker in ARDS.Am. J. Respir. Cell Mol. Biol.38 , 724–732 (2008).
  • Wang Z , ChenF, Zhai et al.: Plasma neutrophil elastase and elafin imbalance is associated with acute respiratory distress syndrome (ARDS) development. PLoS ONE4 , 1–10 (2009).
  • Gong MN : Genetic epidemiology of acute respiratory distress syndrome: implications for future prevention and treatment.Clin. Chest Med.27 , 705–724 (2006).
  • Grigoryev DN , FiniganJH, HassounP, GarciaJG: Science review: Searching for gene candidates in acute lung injury.Crit. Care8 , 440–447 (2004).
  • Cho H -Y, Kleeberger SR: Genetic mechanisms of susceptibility to oxidative lung injury in mice. Free Radic. Biol. Med.42 , 433–445 (2007).
  • Fracica PJ , KnappMJ, PiantadosiCA et al.: Responses of baboons to prolonged hyperoxia: physiology and qualitative pathology.J. Appl. Physiol.71 , 2352–2362 (1991).
  • Sackner MA , LandaJ, HirschJ, ZapataA: Pulmonary effects of oxygen breathing. A 6-hour study in normal men.Ann. Intern. Med.82 , 40–43 (1975).
  • Erzurum SC , DanelC, GillissenA, Chu C-S, Trapnell BC, Crystal RG: In vivo antioxidant gene expression in human airway epithelium of normal individuals exposed to 100% O2. J. Appl. Physiol.75 , 1256–1262 (1993).
  • Waring WS , ThomsonAJ, AdwaniSH et al.: Cardiovascular effects of acute oxygen administration in healthy adults.J. Cardiovasc. Pharmacol.42 , 245–250 (2003).
  • Rossi P , TauzinL, WeissM, Rostain J-C, Sainty J-M, Boussuges A: Could hyperoxic ventilation impair oxygen delivery in septic patients? Clin. Physiol. Funct. Imaging27 , 180–184 (2007).
  • Matute-Bello G , FrevertCW, MartinTR: Animal models of acute lung injury.Am. J. Physiol. Lung Cell Mol. Physiol.295 , L379–L399 (2008).
  • Hudak BB , ZhangLY, KleebergerSR: Inter-strain variation in susceptibility to hyperoxic injury of the murine lung.Pharmacogenetics3 , 135–143 (1993).
  • Cho HY , JedlickaAE, ReddySP, ZhangLY, KenslerTW, KleebergerSR: Linkage analysis of susceptibility to hyperoxia: Nrf2 is a candidate gene.Am. J. Respir. Cell Mol. Biol.26 , 42–51 (2002).
  • Cho HY , JedlickaAE, ReddySPM et al.: Role of NRF2 in protection against hyperoxic lung injury in mice.Am. J. Respir. Cell Mol. Biol.26 , 175–182 (2002).
  • Prows DR , LeikaufGD: Quantitative trait analysis of nickel-induced acute lung injury in mice.Am. J. Respir. Cell Mol. Biol.24 , 740–746 (2001).
  • Prows DR , ShertzerHG, DalyMJ, SidmanCL, LeikaufGD: Genetic analysis of ozone-induced acute lung injury in sensitive and resistant strains of mice.Nat. Genet.17 , 471–474 (1997).
  • Bein K , WesselkamperSC, LiuX et al.: Surfactant associated protein B is critical to survival in nickel-induced injury in mice.Am. J. Respir. Cell Mol. Biol.41(2) , 226–236 (2009).
  • Kleeberger SR , LevittRC, ZhangLY: Susceptibility to ozone induced inflammation: II. Separate loci control responses to acute and subacute exposures.Am. J. Physiol.264 , L21–L26 (1993).
  • Kleeberger SR , LevittRC, ZhangLY et al.: Linkage analysis of susceptibility to ozone-induced lung inflammation in inbred mice.Nat. Genet.17 , 475–478 (1997).
  • Cho HY , MorganDL, BauerAK, KleebergerSR: Signal transduction pathways of tumor necrosis factor-mediated lung injury induced by ozone in mice.Am. J. Respir. Crit. Care Med.175 , 829–839 (2007).
  • Johnson AD , O‘DonnellCJ: An open access database of genome-wide association results.BMC Med. Genet.10 , 6 (2009).
  • Gudmundsson J , SulemP, SteinthorsdottirV et al.: Two variants on chromosome 17 confer prostate cancer risk, and the one in TCF2 protects against type 2 diabetes.Nat. Genet.39 , 977–983 (2007).
  • Gudmundsson J , SulemP, ManolescuA et al.: Genome-wide association study identifies a second prostate cancer susceptibility variant at 8q24.Nat. Genet.39 , 631–637 (2007).
  • Hofmann S , FrankeA, FischerA et al.: Genome-wide association study identifies ANXA11 as a new susceptibility locus for sarcoidosis.Nat. Genet.40 , 1103–1106 (2008).
  • Weidinger S , GiegerC, RodriguezE et al.: Genome-wide scan on total serum IgE levels identifies FCER1A as novel susceptibility locus.PLoS Genet.4 , 8 (2008).
  • McCarthy MI , AbecasisGR, CardonLR et al.: Genome-wide association studies for complex traits: consensus, uncertainty and challenges.Nat. Rev. Genet.9 , 356–369 (2008).
  • Psychiatric GWAS Consortium Coordinating Committee: Genomewide association studies: history, rationale, and prospects for psychiatric disorders. Am. J. Psychiatry166 , 540–556 (2009).
  • Elbers CC , van Eijk KR, Franke L et al.: Using genome-wide pathway analysis to unravel the etiology of complex diseases. Genet. Epidemiol.33(5) , 419–431 (2009)
  • Pearson TA , ManolioTA: How to interpret a genome-wide association study.JAMA299 , 1335–1344 (2008).
  • Liao G , WangJ, GuoJ et al.: In silico genetics: identification of a functional element regulating H2-Ea gene expression.Science306 , 690–695 (2004).
  • Pletcher MT , McClurgP, BatalovS et al.: Use of a dense single nucleotide polymorphism map for in silico mapping in the mouse.PLoS Biol.2 , 2159–2169 (2004).
  • Complex Trait Consortium: The collaborative cross, a community resource for the genetic analysis of complex traits. Nat. Genet.36 , 1133–1137 (2004).
  • Grigoryev DN , MaSF, IrizarryRA, YeSQ, QuackenbushJ, GarciaJG: Orthologous gene-expression profiling in multi-species models: search for candidate genes.Genome Biol.5 , R34 (2004).
  • Perkowski S , SunJ, SinghalS et al.: Gene expression profiling of the early pulmonary response to hyperoxia in mice.Am. J. Respir. Cell Mol. Biol.28 , 682–696 (2003).
  • Cho HY , ReddySP, DebiaseA, YamamotoM, KleebergerSR: Gene expression profiling of NRF2-mediated protection against oxidative injury.Free Radic. Biol. Med.38 , 325–343 (2005).
  • Drake TA , SchadtEE, LusisAJ: Integrating genetic and gene expression data: application to cardiovascular and metabolic traits in mice.Mammal. Genome17 , 466–479 (2006).
  • Li J , BurmeisterM: Genetical genomics: combining genetics with gene expression analysis.Hum. Mol. Genet.14 , R163–R169 (2005).
  • Bystrykh L , WeersingE, DontjeB et al.: Uncovering regulatory pathways that affect hematopoietic stem cell function using ‘genetical genomics‘.Nat. Genet.37 , 225–232 (2005).
  • Mehrabian M , AllayeeH, StocktonJ et al.: Integrating genotypic and expression data in a segregating mouse population to identify 5-lipoxygenase as a susceptibility gene for obesity and bone traits.Nat. Genet.37 , 1224–1233 (2005).
  • Mozhui K , CiobanuDC, SchikorskiT, WangX, LuL, WilliamsRW: Dissection of a QTL hotspot on mouse distal chromosome 1 that modulates neurobehavioral phenotypes and gene expression.PLoS Genet.4(11) , E1000260 (2008).
  • Marshall RP , WebbS, BellinganGJ et al.: Angiotensin converting enzyme insertion/deletion polymorphism is associated with susceptibility and outcome in acute respiratory distress syndrome.Am. J. Respir. Crit. Care Med.166 , 646–650 (2002).
  • Casey L , KriegerB, KohlerJ, RiceC, OparilS, SzidonP: Decreased serum angiotensin converting enzyme in adult respiratory distress syndrome associated with sepsis: a preliminary report.Crit. Care Med.9 , 651–654 (1981).
  • Fourrier F , ChopinC, WallaertB et al.: Compared evolution of plasma fibronectin and angiotensin-converting enzyme levels in septic ARDS.Chest87 , 191–195 (1985).
  • Imai Y , KubaK, RaoS et al.: Angiotensin-converting enzyme 2 protects from severe acute lung failure.Nature436 , 112–116 (2005).
  • Arndt PG , YoungSK, PochKR et al.: Systemic inhibition of the angiotensin-converting enzyme limits lipopolysaccharide-induced lung neutrophils recruitment through both bradykinin and angiotensin II-regulated pathways.J. Immunol.177 , 7233–7241 (2006).
  • Rigat B , HubertC, Alhenc-GelasF et al.: An insertion/deletion polymorphism in the angiotensin-1-converting enzyme gene accounting for half the variance of serum enzyme levels.J. Clin. Invest.86 , 1343–1346 (1990).
  • Jerng JS , YuCJ, WangHC et al.: Polymorphism of the angiotensin-converting enzyme gene affects the outcome of acute respiratory distress syndrome.Crit. Care Med.34 , 1001–1006 (2006).
  • Villar J , FloresC, Perez-MendezL et al.: Angiotensin-converting enzyme insertion/deletion polymorphism is not associated with susceptibility and outcome in sepsis and acute respiratory distress syndrome.Intensive Care Med.34 , 488–495 (2008).
  • Bowler RP , NicksM, TranK et al.: Extracellular superoxide dismutase attenuates lipopolysaccharide-induced neutrophilic inflammation.Am. J. Respir. Cell Mol. Biol.31 , 432–439 (2004).
  • Arcaroli JJ , HokansonJE, AbrahamE et al.: Extracellular superoxide dismutase haplotypes are associated with acute lung injury and mortality.Am. J. Respir. Crit. Care Med.179 , 105–112 (2009).
  • Neidhardt R , KeelM, SteckholzerU et al.: Relationship of interleukin-10 plasma levels to severity of injury and clinical outcome in injured patients.J. Trauma42 , 863–871 (1997).
  • Crawley E , KayR, SillibourneJ et al.: Polymorphic haplotypes of the interleukin-10 5´ flanking region determine variable interleukin-10 transcription and are associated with particular phenotypes of juvenile arthritis.Arthritis Rheum.42 , 1101–1108 (1999).
  • Schroder O , LaunRA, HeldB, EkkernkampA, SchulteKM: Association of interleukin-10 promoter polymorphism with the incidence of multiple organ dysfunction following major trauma: results of a prospective pilot study.Shock21 , 306–310 (2004).
  • Armstrong L , MillarAB: Relative production of tumor necrosis factor a and interleukin-10 in adult respiratory distress syndrome.Thorax52 , 442–446 (1997).
  • Parson PE , MossM, VanniceJL et al.: Circulating IL-1ra and IL-10 levels are increased but do not predict the development of acute respiratory distress syndrome in at-risk patients.Am. J. Resp. Crit. Care Med.155 , 1469–1473 (1997).
  • Gong MN , ThompsonBT, WilliamsPL et al.: Interleukin-10 polymorphism in position -1082 and acute respiratory distress syndrome.Eur. Respir. J.27 , 674–681 (2006).
  • Summerfield JA , SumiyaM, LevinM, TurnerMW: Association of mutations in mannose binding protein gene with childhood infection in consecutive hospital series.BMJ314 , 1229–1232 (1997).
  • Fidler KJ , WilsonP, DaviesJC et al.: Increased incidence and severity of the systemic inflammatory response syndrome in patients deficient in mannose-binding lectin.Intensive Care Med.30 , 1438–1445 (2004).
  • Gong MN , ZhouW, WilliamsPL et al.: Polymorphisms in the mannose binding lectin-2 gene and acute respiratory distress syndrome.Crit. Care Med.35 , 48–56 (2007).
  • Goeckeler ZM , WysolmerskiRB: Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation.J. Cell Biol.130 , 613–627 (1995).
  • Wainwright MS , RossiJ, SchavockyJ et al.: Protein kinase involved in lung injury susceptibility: evidence from enzyme isoform genetic knockout and in vivo inhibitor treatment.Proc. Natl Acad. Sci. USA100 , 6233–6238 (2003).
  • Eutamene H , TheodorouV, SchmidlinF et al.: LPS-induced lung inflammation is linked to increased epithelial permeability: role of MLCK.Eur. Resp. J.25 , 789–796 (2005).
  • Gao L , GrantA, HalderI et al.: Novel polymorphisms in the myosin light chain kinase gene confer risk for acute lung injury.Am. J. Respir. Cell Mol. Biol.34 , 487–495 (2006).
  • Christie JD , MaSF, AplencR et al.: Variation in the myosin light chain kinase gene is associated with development of acute lung injury after major trauma.Crit. Care Med.36 , 2794–2800 (2008).
  • Itoh K , TongKI, YamamotoM: Molecular mechanism activating Nrf2–Keap1 pathway in regulation of adaptive response to electrophiles.Free Radic. Biol. Med.36 , 1208–1213 (2004).
  • Kensler TW , WakabayashiN, BiswalS: Cell survival responses to environmental stresses via the Keap1–Nrf2–ARE pathway.Annu. Rev. Pharmacol. Toxicol.47 , 89–116 (2007).
  • Marzec JM , ChristieJD, ReddySP et al.: Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury.FASEB J.21 , 2237–2246 (2007).
  • Ross D , BeallH, TraverRD, SiegelD, PhillipsRM, GibsonNW: Bioactivation of quinines by DT-diaphorase: molecular, biochemical, and chemical studies.Oncol. Res.6 , 493–500 (1994).
  • Lim JH , Kim K-M, Kim SW, Hwang O, Choi HJ: Bromocriptine activates NQO1 via Nrf2-PI3K/Akt signaling: novel cytoprotective mechanism against oxidative damage. Pharmacol. Res.57 , 325–331 (2008).
  • Jaiswal AK : Regulation of genes encoding NAD(P)H:quinone oxidoreductases.Free Radic. Biol. Med.29 , 254–262 (2000).
  • Korashy HM , BrocksDR, El-KadiAOS: Induction of the NAD(P)H:quinone oxidoreductase 1 by ketoconazole and itraconazole; a mechanism of cancer chemoprotection.Cancer Lett.258 , 135–143 (2007).
  • Reddy AJ , ChristieJD, AplencR, FuchsB, LankenPN, KleebergerSR: Association of human NAD(P)H:quinone oxidoreductase 1 (NQO1) polymorphism with development of acute lung injury.J. Cell. Mol. Med. (2009) (Epub ahead of print).
  • Nemeth E , MillarLK, Bryant-GreenwoodG: Fetal membrane distension:II. Differentially expressed genes regulated by acute distension in vitro.Am. J. Obstet. Gynecol.182 , 60–67 (2007).
  • Ognjanovic S , BaoS, YamamotoSY et al.: Genomic organization of the gene coding for human pre-B-cell colony enhancing factor and expression in human fetal membranes.J. Mol. Endocrinol.26 , 107–117 (2001).
  • Jia SH , LiY, ParodoJ et al.: Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis.J. Clin. Invest.113 , 1318–1327 (2004).
  • Ye SQ , SimonBA, MaloneyJP et al.: Pre-B-cell colony-enhancing factor as a potential novel biomarker in acute lung injury.Am. J. Respir. Crit. Care Med.171 , 361–370 (2005).
  • Bajwa EK , YuCL, GongMN et al.: Pre-B-cell colony-enhancing factor gene polymorphisms and risk of acute respiratory distress syndrome.Crit. Care Med.35 , 1290–1295 (2007).
  • Eisner MD , ParsonsPE, MatthayMA et al.: Plasma surfactant protein levels and clinical outcomes in patients with acute lung injury.Thorax58 , 983–988 (2003).
  • Doyle IR , BerstenAD, NicholasTE: Surfactant proteins-A and -B are elevated in plasma of patients with acute respiratory failure.Am. J. Respir. Crit. Care Med.156 , 1217–1229 (1997).
  • Floros J , VeletzaSV, KotikalapudiP et al.: Dinucleotide repeats in the human surfactant protein-B gene and respiratory-distress syndrome.Biochem. J.305 , 583–590 (1995).
  • Gong MN , WeiZ, Xu L-L et al.: Polymorphism in the surfactant protein-B gene, gender, and the risk of direct pulmonary injury and ARDS. Chest125 , 203–211 (2004).
  • Quasney MW , WatererGW, DahmerMK et al.: Association between surfactant protein-B +1580 polymorphism and the risk of respiratory failure in adults with community-acquired pneumonia.Crit. Care Med.32 , 1115–1119 (2004).
  • Currier PF , GongMN, ZhaiR et al.: Surfactant protein-B polymorphisms and mortality in the acute respiratory distress syndrome.Crit. Care Med.36 , 2511–2516 (2008).
  • Seybold J , ThomasD, WitzenrathM et al.: Tumor necrosis factor-α-dependent expression of phosphodiesterase 2: role in endothelial hyperpermeability.Blood105 , 3569–3576 (2005).
  • Gong MN , ZhouW, WilliamsPL et al.: -308GA and TNFB polymorphisms in acute respiratory distress syndrome.Eur. Resp. J.26 , 382–289 (2005).
  • Corne J , ChuppG, LeeCG et al.: IL-13 stimulates vascular endothelial growth factor and protects against hyperoxic lung injury.J. Clin. Invest.106 , 783–791 (2000).
  • Medford AR , KeenLJ, BidwellJL, MillarAB: Vascular endothelial growth factor gene polymorphism and acute respiratory distress syndrome.Thorax60 , 244–248 (2005).
  • Morgan TM , KrumholzHM, LiftonRP, SpertusJA: Nonvalidation of reported genetic risk factors for acute coronary syndrome in a large-scale replication study.JAMA297 , 1551–1561 (2007)
  • Daly AK : Candidate gene case-control studies.Pharmacogenomics4 , 127–139 (2003).
  • Keating BJ , TischfieldS, MurraySS et al.: Concept, design and implementation of a cardiovascular gene-centric 50 K SNP array for large-scale genomic association studies.PLoS ONE3 , 1–9 (2008).
  • Rao DC : An overview of the genetic dissection of complex traits.Adv. Genet.60 , 3–34 (2008).
  • Sheu CC , ZhaiR, SuL et al.: Sex-specific association of epidermal growth factor gene polymorphisms with acute respiratory distress syndrome.Eur. Respir. J.33 , 543–550 (2009).
  • Moradi M , MojtahedzadehM, MandegariA et al.: The role of glutathione-S-transferase polymorphisms on clinical outcome of ALI/ARDS patients treated with N-acetylcysteine.Respir. Med.103 , 434–441 (2009).
  • Zhai R , ZhouW, GongMN et al.: Inhibitor κB-α haplotype GTC is associated with susceptibility to acute respiratory distress syndrome in Caucasians.Crit. Care Med.35 , 893–898 (2007).
  • Flores C , MaSF, MaressoK, WadeMS, VillarJ, GarciaJG: IL6 gene-wide haplotype is associated with susceptibility to acute lung injury.Transl. Res.152 , 11–17 (2008).
  • Hildebrand F , StuhrmannM, van Giensven M et al.: Association of IL-8-251A/T polymorphism with incidence of acute respiratory distress syndrome (ARDS) and IL-8 synthesis after multiple trauma. Cytokine37 , 192–199 (2007).
  • Gao L , FloresC, Fan-MaS et al.: Macrophage migration inhibitory factor in acute lung injury: expression, biomarker, and associations.Transl. Res.150 , 18–29 (2007).
  • Adamzik M , FreyUH, RiemanK et al.: Insertion/deletion polymorphism in the promoter of NFKB1 influences severity but not mortality of acute respiratory distress syndrome.Intensive Care Med.33 , 1199–1203 (2007).
  • Sapru A , HansenH, AjayiT et al.: 4G/5G polymorphism of plasminogen activator inhibitor-1 gene is associated with mortality in intensive care unit patients with severe pneumonia.Anesthesiology110 , 1086–1091 (2009).
  • Wurfel MM , GordonAC, HoldenTD et al.: Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis.Am. J. Respir. Crit. Care Med.178 , 710–720 (2008).
  • Arcaroli J , SankoffJ, LiuN, AllisonDB, MaloneyJ, AbrahamE: Association between urokinase haplotypes and outcome from infection-associated acute lung injury.Intensive Care Med.34 , 300–307 (2008).

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.