417
Views
3
CrossRef citations to date
0
Altmetric
Special Report

Considerations for mass spectrometry-based multi-omic analysis of clinical samples

, &
Pages 99-107 | Received 05 Nov 2019, Accepted 29 Jan 2020, Published online: 07 Feb 2020

References

  • Hasin Y, Seldin M, Lusis A. Multi-omics approaches to disease. Genome Biol. 2017;18(1):83.
  • Kopczynski D, Coman C, Zahedi RP, et al. Multi-OMICS: a critical technical perspective on integrative lipidomics approaches. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862(8):808–811.
  • Tebani A, Afonso C, Marret S, et al. Omics-based strategies in precision medicine: toward a paradigm shift in inborn errors of metabolism investigations. Int J Mol Sci. 2016;17(9):1555.
  • Pappireddi N, Martin L, Wuhr M. A review on quantitative multiplexed proteomics. Chembiochem. 2019;20(10):1210–1224.
  • Beale DJ, Pinu FR, Kouremenos KA, et al. Review of recent developments in GC-MS approaches to metabolomics-based research. Metabolomics. 2018;14(11):152.
  • Benton HP, Wong DM, Trauger SA, et al. XCMS2: processing tandem mass spectrometry data for metabolite identification and structural characterization. Anal Chem. 2008;80(16):6382–6389.
  • Marco-Ramell A, Palau-Rodriguez M, Alay A, et al. Evaluation and comparison of bioinformatic tools for the enrichment analysis of metabolomics data. BMC Bioinformatics. 2018;19(1):1.
  • Wang M, Carver JJ, Phelan VV, et al. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat Biotechnol. 2016;34(8):828–837.
  • Thomas MC, Mitchell TW, Blanksby SJ. Ozonolysis of phospholipid double bonds during electrospray ionization: a new tool for structure determination. J Am Chem Soc. 2006;128(1):58–59.
  • Ellis SR, Hughes JR, Mitchell TW, et al. Using ambient ozone for assignment of double bond position in unsaturated lipids. Analyst. 2012;137(5):1100–1110.
  • Tang S, Cheng H, Yan X. On-demand electrochemical epoxidation in nano-electrospray ionization mass spectrometry to locate carbon-carbon double bonds. Angew Chem Int Ed Engl. 2019 Jan 2;59(1):209–214.
  • Leaptrot KL, May JC, Dodds JN, et al. Ion mobility conformational lipid atlas for high confidence lipidomics. Nat Commun. 2019;10(1):985.
  • Nichols CM, Dodds JN, Rose BS, et al. Untargeted molecular discovery in primary metabolism: collision cross section as a molecular descriptor in ion mobility-mass spectrometry. Anal Chem. 2018;90(24):14484–14492.
  • Stevens VL, Hoover E, Wang Y, et al. Pre-analytical factors that affect metabolite stability in human urine, plasma, and serum: a review. Metabolites. 2019;9(8):156.
  • Wang Z, Zolnik CP, Qiu Y, et al. Comparison of fecal collection methods for microbiome and metabolomics studies. Front Cell Infect Microbiol. 2018;8:301.
  • Hogue SR, Gomez MF, da Silva WV, et al. A customized at-home stool collection protocol for use in microbiome studies conducted in cancer patient populations. Microb Ecol. 2019;78:1030–1034.
  • Beretov J, Wasinger VC, Schwartz P, et al. A standardized and reproducible urine preparation protocol for cancer biomarkers discovery. Biomark Cancer. 2014;6:21–27.
  • Olszowy P, Buszewski B. Urine sample preparation for proteomic analysis. J Sep Sci. 2014;37(20):2920–2928.
  • Ranganathan S, Polshyna A, Nicholl G, et al. Assessment of protein stability in cerebrospinal fluid using surface-enhanced laser desorption/ionization time-of-flight mass spectrometry protein profiling. Clin Proteomics. 2006;2(1–2):91–101.
  • Rosenling T, Slim CL, Christin C, et al. The effect of preanalytical factors on stability of the proteome and selected metabolites in cerebrospinal fluid (CSF). J Proteome Res. 2009;8(12):5511–5522.
  • Wuolikainen A, Hedenstrom M, Moritz T, et al. Optimization of procedures for collecting and storing of CSF for studying the metabolome in ALS. Amyotroph Lateral Scler. 2009;10(4):229–236.
  • Kamlage B, Neuber S, Bethan B, et al. Impact of prolonged blood incubation and extended serum storage at room temperature on the human serum metabolome. Metabolites. 2018;8(1):6.
  • Anton G, Wilson R, Yu ZH, et al. Pre-analytical sample quality: metabolite ratios as an intrinsic marker for prolonged room temperature exposure of serum samples. PLoS One. 2015;10(3):e0121495.
  • Kaisar M, van Dullemen LFA, Thezenas ML, et al. Plasma degradome affected by variable storage of human blood. Clin Proteomics. 2016;13:26.
  • Hebels DG, Georgiadis P, Keun HC, et al. Performance in omics analyses of blood samples in long-term storage: opportunities for the exploitation of existing biobanks in environmental health research. Environ Health Perspect. 2013;121(4):480–487.
  • Ignjatovic V, Geyer PE, Palaniappan KK, et al. Mass spectrometry-based plasma proteomics: considerations from sample collection to achieving translational data. J Proteome Res. 2019;18:4085–4097.
  • Lygirou V, Makridakis M, Vlahou A. Biological sample collection for clinical proteomics: existing SOPs. Methods Mol Biol. 2015;1243:3–27.
  • Eisenbeiss L, Steuer AE, Binz TM, et al. (Un)targeted hair metabolomics: first considerations and systematic evaluation on the impact of sample preparation. Anal Bioanal Chem. 2019;411(17):3963–3977.
  • Rupasinghe TW. Lipidomics: extraction protocols for biological matrices. Methods Mol Biol. 2013;1055:71–80.
  • Hayton S, Trengove RD, Maker GL. Sample preparation and reporting standards for metabolomics of adherent mammalian cells. Methods Mol Biol. 2019;1978:3–12.
  • Lindahl A, Saaf S, Lehtio J, et al. Tuning metabolome coverage in reversed phase LC-MS metabolomics of MeOH extracted samples using the reconstitution solvent composition. Anal Chem. 2017;89(14):7356–7364.
  • Ulmer CZ, Yost RA, Chen J, et al. Liquid chromatography-mass spectrometry metabolic and lipidomic sample preparation workflow for suspension-cultured mammalian cells using Jurkat T lymphocyte cells. J Proteomics Bioinform. 2015;8(6):126–132.
  • Ulmer CZ, Jones CM, Yost RA, et al. Optimization of Folch, Bligh-Dyer, and Matyash sample-to-extraction solvent ratios for human plasma-based lipidomics studies. Anal Chim Acta. 2018;1037:351–357.
  • Gil A, Zhang W, Wolters JC, et al. One- vs two-phase extraction: re-evaluation of sample preparation procedures for untargeted lipidomics in plasma samples. Anal Bioanal Chem. 2018;410(23):5859–5870.
  • Duan X, Yarmush D, Berthiaume F, et al. Immunodepletion of albumin for two-dimensional gel detection of new mouse acute-phase protein and other plasma proteins. Proteomics. 2005;5(15):3991–4000.
  • Brand J, Haslberger T, Zolg W, et al. Depletion efficiency and recovery of trace markers from a multiparameter immunodepletion column. Proteomics. 2006;6(11):3236–3242.
  • Shores KS, Knapp DR. Assessment approach for evaluating high abundance protein depletion methods for cerebrospinal fluid (CSF) proteomic analysis. J Proteome Res. 2007;6(9):3739–3751.
  • Heller M, Michel PE, Morier P, et al. Two-stage Off-Gel isoelectric focusing: protein followed by peptide fractionation and application to proteome analysis of human plasma. Electrophoresis. 2005;26(6):1174–1188.
  • Cologna SM, Russell WK, Lim PJ, et al. Combining isoelectric point-based fractionation, liquid chromatography and mass spectrometry to improve peptide detection and protein identification. J Am Soc Mass Spectrom. 2010;21(9):1612–1619.
  • Tran JC, Doucette AA. Gel-eluted liquid fraction entrapment electrophoresis: an electrophoretic method for broad molecular weight range proteome separation. Anal Chem. 2008;80(5):1568–1573.
  • Ten-Domenech I, Simo-Alfonso EF, Herrero-Martinez JM. Improving fractionation of human milk proteins through calcium phosphate coprecipitation and their rapid characterization by capillary electrophoresis. J Proteome Res. 2018;17(10):3557–3564.
  • Deng N, Chen Y, Jiang B, et al. A robust and effective intact protein fractionation strategy by GO/PEI/Au/PEG nanocomposites for human plasma proteome analysis. Talanta. 2018;178:49–56.
  • Washburn MP, Wolters D, Yates JR 3rd. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol. 2001;19(3):242–247.
  • Waas M, Bhattacharya S, Chuppa S, et al. Combine and conquer: surfactants, solvents, and chaotropes for robust mass spectrometry based analyses of membrane proteins. Anal Chem. 2014;86(3):1551–1559.
  • Proc JL, Kuzyk MA, Hardie DB, et al. A quantitative study of the effects of chaotropic agents, surfactants, and solvents on the digestion efficiency of human plasma proteins by trypsin. J Proteome Res. 2010;9(10):5422–5437.
  • Verdoliva V, Senatore C, Polci ML, et al. Differential denaturation of serum proteome reveals a significant amount of hidden information in complex mixtures of proteins. PLoS One. 2013;8(3):e57104.
  • Josic D, Kovac S. reversed-phase high performance liquid chromatography of proteins. Curr Protoc Protein Sci. 2010;61. Chapter 8, Unit 8 7.
  • Chen TH, Yang Y, Zhang Z, et al. Native reversed-phase liquid chromatography: a technique for LCMS of intact antibody-drug conjugates. Anal Chem. 2019;91(4):2805–2812.
  • Richard VR, Domanski D, Percy AJ, et al. An online 2D-reversed-phase - Reversed-phase chromatographic method for sensitive and robust plasma protein quantitation. J Proteomics. 2017;168:28–36.
  • Pergande MR, Zarate E, Haney-Ball C, et al. Standard-flow LC and thermal focusing ESI elucidates altered liver proteins in late stage Niemann-Pick, type C1 disease. Bioanalysis. 2019;11(11):1067–1083.
  • Pergande MR, Nguyen TTA, Haney-Ball C, et al. Quantitative, label-free proteomics in the symptomatic Niemann-Pick, type C1 mouse model using standard flow liquid chromatography and thermal focusing electrospray ionization. Proteomics. 2019;19(9):e1800432.
  • Bird SS, Marur VR, Sniatynski MJ, et al. Serum lipidomics profiling using LC-MS and high-energy collisional dissociation fragmentation: focus on triglyceride detection and characterization. Anal Chem. 2011;83(17):6648–6657.
  • Morin-Rivron D, Christinat N, Masoodi M. Lipidomics analysis of long-chain fatty acyl-coenzyme as in liver, brain, muscle and adipose tissue by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom. 2017;31(4):344–350.
  • Pergande MR, Serna-Perez F, Mohsin SB, et al. Lipidomic analysis reveals altered fatty acid metabolism in the liver of the symptomatic Niemann-Pick, type C1 mouse model. Proteomics. 2019;19(18):e1800285.
  • Naser FJ, Mahieu NG, Wang L, et al. Two complementary reversed-phase separations for comprehensive coverage of the semipolar and nonpolar metabolome. Anal Bioanal Chem. 2018;410(4):1287–1297.
  • Chan W, Zhao Y, Zhang J. Evaluating the performance of sample preparation methods for ultra-performance liquid chromatography/mass spectrometry based serum metabonomics. Rapid Commun Mass Spectrom. 2019;33(6):561–568.
  • Wang S, Shi X, Xu G. Online three dimensional liquid chromatography/mass spectrometry method for the separation of complex samples. Anal Chem. 2017;89(3):1433–1438.
  • Schwaiger M, Schoeny H, El Abiead Y, et al. Merging metabolomics and lipidomics into one analytical run. Analyst. 2018;144(1):220–229.
  • Zhao Z, Xu Y. An extremely simple method for extraction of lysophospholipids and phospholipids from blood samples. J Lipid Res. 2010;51(3):652–659.
  • McCalley DV. Understanding and manipulating the separation in hydrophilic interaction liquid chromatography. J Chromatogr A. 2017;1523:49–71.
  • Hook V, Kind T, Podvin S, et al. Metabolomics analyses of 14 classical neurotransmitters by GC-TOF with LC-MS illustrates secretion of 9 cell-cell signaling molecules from sympathoadrenal chromaffin cells in the presence of lithium. ACS Chem Neurosci. 2019;10(3):1369–1379.
  • Ribbenstedt A, Ziarrusta H, Benskin JP. Development, characterization and comparisons of targeted and non-targeted metabolomics methods. PLoS One. 2018;13(11):e0207082.
  • Liu W, Song Q, Cao Y, et al. Advanced liquid chromatography-mass spectrometry enables merging widely targeted metabolomics and proteomics. Anal Chim Acta. 2019;1069:89–97.
  • Sun Z, Ji F, Jiang Z, et al. Improving deep proteome and PTMome coverage using tandem HILIC-HPRP peptide fractionation strategy. Anal Bioanal Chem. 2019;411(2):459–469.
  • Kozlik P, Goldman R, Sanda M. Hydrophilic interaction liquid chromatography in the separation of glycopeptides and their isomers. Anal Bioanal Chem. 2018;410(20):5001–5008.
  • Sasaki K, Sagawa H, Suzuki M, et al. Metabolomics platform with capillary electrophoresis coupled with high-resolution mass spectrometry for plasma analysis. Anal Chem. 2019;91(2):1295–1301.
  • MacLennan MS, Kok MGM, Soliman L, et al. Capillary electrophoresis-mass spectrometry for targeted and untargeted analysis of the sub-5kDa urine metabolome of patients with prostate or bladder cancer: a feasibility study. J Chromatogr B Analyt Technol Biomed Life Sci. 2018;1074–1075:79–85.
  • Yang Z, Shen X, Chen D, et al. Microscale reversed-phase liquid chromatography/capillary zone electrophoresis-tandem mass spectrometry for deep and highly sensitive bottom-up proteomics: identification of 7500 proteins with five micrograms of an MCF7 proteome digest. Anal Chem. 2018;90(17):10479–10486.
  • Belov AM, Zang L, Sebastiano R, et al. Complementary middle-down and intact monoclonal antibody proteoform characterization by capillary zone electrophoresis - mass spectrometry. Electrophoresis. 2018;39(16):2069–2082.
  • Takeda H, Izumi Y, Takahashi M, et al. Widely-targeted quantitative lipidomics method by supercritical fluid chromatography triple quadrupole mass spectrometry. J Lipid Res. 2018;59(7):1283–1293.
  • Lisa M, Cifkova E, Khalikova M, et al. Lipidomic analysis of biological samples: comparison of liquid chromatography, supercritical fluid chromatography and direct infusion mass spectrometry methods. J Chromatogr A. 2017;1525:96–108.
  • Desfontaine V, Losacco GL, Gagnebin Y, et al. Applicability of supercritical fluid chromatography - mass spectrometry to metabolomics. I - optimization of separation conditions for the simultaneous analysis of hydrophilic and lipophilic substances. J Chromatogr A. 2018;1562:96–107.
  • Suzuki M, Nishiumi S, Kobayashi T, et al. Use of on-line supercritical fluid extraction-supercritical fluid chromatography/tandem mass spectrometry to analyze disease biomarkers in dried serum spots compared with serum analysis using liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom. 2017;31(10):886–894.
  • Hancock SE, Poad BLJ, Willcox MDP, et al. Analytical separations for lipids in complex, non-polar lipidomes using differential mobility spectrometry. J Lipid Res. 2019;60:1968–1978.
  • Wernisch S, Afshinnia F, Rajendiran T, et al. Probing the application range and selectivity of a differential mobility spectrometry-mass spectrometry platform for metabolomics. Anal Bioanal Chem. 2018;410(12):2865–2877.
  • Zhang X, Kew K, Reisdorph R, et al. Performance of a high-pressure liquid chromatography-ion mobility-mass spectrometry system for metabolic profiling. Anal Chem. 2017;89(12):6384–6391.
  • Schweppe DK, Prasad S, Belford MW, et al. Characterization and optimization of multiplexed quantitative analyses using high-field asymmetric-waveform ion mobility mass spectrometry. Anal Chem. 2019;91(6):4010–4016.
  • Nassar AF, Williams BJ, Yaworksy DC, et al. Rapid label-free profiling of oral cancer biomarker proteins using nano-UPLC-Q-TOF ion mobility mass spectrometry. Proteomics Clin Appl. 2016;10(3):280–289.
  • Newton BW, Cologna SM, Moya C, et al. Proteomic analysis of 3T3-L1 adipocyte mitochondria during differentiation and enlargement. J Proteome Res. 2011;10(10):4692–4702.
  • Tran JC, Doucette AA. Rapid and effective focusing in a carrier ampholyte solution isoelectric focusing system: a proteome prefractionation tool. J Proteome Res. 2008;7(4):1761–1766.
  • Zuo X, Speicher DW. Comprehensive analysis of complex proteomes using microscale solution isoelectrofocusing prior to narrow pH range two-dimensional electrophoresis. Proteomics. 2002;2(1):58–68.
  • Ros A, Faupel M, Mees H, et al. Protein purification by Off-Gel electrophoresis. Proteomics. 2002;2(2):151–156.
  • Wang W, Wu X, Xiong E, et al. Improving gel-based proteome analysis of soluble protein extracts by heat prefractionation. Proteomics. 2012;12(7):938–943.
  • Chiangjong W, Changtong C, Panachan J, et al. Optimization and standardization of thermal treatment as a plasma prefractionation method for proteomic analysis. Biomed Res Int. 2019;8646039:2019.
  • Simo C, Bachi A, Cattaneo A, et al. Performance of combinatorial peptide libraries in capturing the low-abundance proteome of red blood cells. 1. Behavior of mono- to hexapeptides. Anal Chem. 2008;80(10):3547–3556.
  • Guerrier L, Righetti PG, Boschetti E. Reduction of dynamic protein concentration range of biological extracts for the discovery of low-abundance proteins by means of hexapeptide ligand library. Nat Protoc. 2008;3(5):883–890.
  • Leipert J, Tholey A. Miniaturized sample preparation on a digital microfluidics device for sensitive bottom-up microproteomics of mammalian cells using magnetic beads and mass spectrometry-compatible surfactants. Lab Chip. 2019;19(20):3490–3498.
  • Li X, Wang W, Chen J. Recent progress in mass spectrometry proteomics for biomedical research. Sci China Life Sci. 2017;60(10):1093–1113.
  • Gowda GA, Djukovic D. Overview of mass spectrometry-based metabolomics: opportunities and challenges. Methods Mol Biol. 2014;1198:3–12.
  • Wood PL. Mass spectrometry strategies for clinical metabolomics and lipidomics in psychiatry, neurology, and neuro-oncology. Neuropsychopharmacology. 2014;39(1):24–33.
  • Hu T, Zhang JL. Mass-spectrometry-based lipidomics. J Sep Sci. 2018;41(1):351–372.
  • Rustam YH, Reid GE. Analytical challenges and recent advances in mass spectrometry based lipidomics. Anal Chem. 2018;90(1):374–397.
  • Parker CE, Pearson TW, Anderson NL, et al. Mass-spectrometry-based clinical proteomics–a review and prospective. Analyst. 2010;135(8):1830–1838.
  • Liu LY, Yang T, Ji J, et al. Integrating multiple ‘omics’ analyses identifies serological protein biomarkers for preeclampsia. BMC Med. 2013;11:236.
  • Yang L, Yang X, Kong X, et al. Covariation analysis of serumal and urinary metabolites suggests aberrant glycine and fatty acid metabolism in chronic hepatitis B. PLoS One. 2016;11(5):e0156166.
  • Schubert KO, Stacey D, Arentz G, et al. Targeted proteomic analysis of cognitive dysfunction in remitted major depressive disorder: opportunities of multi-omics approaches towards predictive, preventive, and personalized psychiatry. J Proteomics. 2018;188:63–70.
  • Xicota L, Ichou F, Lejeune FX, et al. Multi-omics signature of brain amyloid deposition in asymptomatic individuals at-risk for Alzheimer’s disease: the INSIGHT-preAD study. EBioMedicine. 2019;47:518–528.
  • Barkovits K, Linden A, Galozzi S, et al. Characterization of cerebrospinal fluid via data-independent acquisition mass spectrometry. J Proteome Res. 2018;17(10):3418–3430.
  • Blasco H, Veyrat-Durebex C, Bocca C, et al. Lipidomics reveals cerebrospinal-fluid signatures of ALS. Sci Rep. 2017;7(1):17652.
  • Pieragostino D, D’Alessandro M, Di Ioia M, et al. An integrated metabolomics approach for the research of new cerebrospinal fluid biomarkers of multiple sclerosis. Mol Biosyst. 2015;11(6):1563–1572.
  • Darst BF, Lu Q, Johnson SC, et al. Integrated analysis of genomics, longitudinal metabolomics, and Alzheimer’s risk factors among 1,111 cohort participants. Genet Epidemiol. 2019;43(6):657–674.
  • Krochmal M, Cisek K, Filip S, et al. Identification of novel molecular signatures of IgA nephropathy through an integrative -omics analysis. Sci Rep. 2017;7(1):9091.
  • Badoud F, Brewer D, Charchoglyan A, et al. Multi-omics integrative investigation of fatty acid metabolism in obese and lean subcutaneous tissue. OMICS. 2017;21(7):371–379.
  • Schlotter F, Halu A, Goto S, et al. Spatiotemporal multi-omics mapping generates a molecular atlas of the aortic valve and reveals networks driving disease. Circulation. 2018;138(4):377–393.
  • Bastarrachea RA, Laviada-Molina HA, Nava-Gonzalez EJ, et al. Deep multi-OMICs and multi-tissue characterization in a pre- and postprandial state in human volunteers: the GEMM family study research design. Genes (Basel). 2018;9(11):532.
  • Vantaku V, Dong J, Ambati CR, et al. Multi-omics integration analysis robustly predicts high-grade patient survival and identifies CPT1B effect on fatty acid metabolism in bladder cancer. Clin Cancer Res. 2019;25(12):3689–3701.
  • Khurshid Z, Zohaib S, Najeeb S, et al. Human saliva collection devices for proteomics: an update. Int J Mol Sci. 2016;17(6):846.
  • Tang ZZ, Chen G, Hong Q, et al. Multi-omic analysis of the microbiome and metabolome in healthy subjects reveals microbiome-dependent relationships between diet and metabolites. Front Genet. 2019;10:454.
  • Sugawara J, Ochi D, Yamashita R, et al. Maternity log study: a longitudinal lifelog monitoring and multiomics analysis for the early prediction of complicated pregnancy. BMJ Open. 2019;9(2):e025939.
  • Zhao Y, Shin DG. Deep pathway analysis V2.0: a pathway analysis framework incorporating multi-dimensional omics data. IEEE/ACM Trans Comput Biol Bioinform. 2019;1–1.
  • Altenbuchinger M, Zacharias HU, Solbrig S, et al. A multi-source data integration approach reveals novel associations between metabolites and renal outcomes in the German Chronic Kidney Disease study. Sci Rep. 2019;9(1):13954.
  • Argelaguet R, Velten B, Arnol D, et al. Multi-omics factor analysis-a framework for unsupervised integration of multi-omics data sets. Mol Syst Biol. 2018;14(6):e8124.
  • Meng C, Basunia A, Peters B, et al. Integrative single sample gene-set analysis of multiple omics data. Mol Cell Proteomics. 2019;18(8 suppl 1):S153–S168.
  • Singh A, Shannon CP, Gautier B, et al. DIABLO: an integrative approach for identifying key molecular drivers from multi-omics assays. Bioinformatics. 2019;35(17):3055–3062.
  • Csala A, Hof MH, Zwinderman AH. Multiset sparse redundancy analysis for high-dimensional omics data. Biom J. 2019;61(2):406–423.
  • Wang P, Gao L, Hu Y, et al. Feature related multi-view nonnegative matrix factorization for identifying conserved functional modules in multiple biological networks. BMC Bioinformatics. 2018;19(1):394.
  • Rappoport N, Shamir R. Multi-omic and multi-view clustering algorithms: review and cancer benchmark. Nucleic Acids Res. 2018;46(20):10546–10562.

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.