Publication Cover
Journal of Environmental Science and Health, Part B
Pesticides, Food Contaminants, and Agricultural Wastes
Volume 57, 2022 - Issue 10
384
Views
4
CrossRef citations to date
0
Altmetric
Research Article

Transcriptomic signaling in zebrafish (Danio rerio) embryos exposed to environmental concentrations of glyphosate

, , , , & ORCID Icon

References

  • Landrigan, P. J.; Belpoggi, F. The Need for Independent Research on the Health Effects of Glyphosate-Based Herbicides. Environ. Health. 2018, 17, 51. DOI: 10.1186/s12940-018-0392-z.
  • Benbrook, C. M. Trends in Glyphosate Herbicide Use in the United States and Globally. Environ. Sci. Eur. 2016, 28, 3. DOI: 10.1186/s12302-016-0070-0.
  • Moraes, J. S.; Silva Nornberg, B. d.; Castro, M. d.; Vaz, BdS.; Mizuschima, C. W.; Marins, L. F. F.; Martins, CdM. Zebrafish (Danio rerio) Ability to Activate ABCC Transporters after Exposure to Glyphosate and Its Formulation Roundup Transorb®. Chemosphere. 2020, 248, 125959. DOI: 10.1016/j.chemosphere.2020.125959.
  • Vandenberg, L. N.; Blumberg, B.; Antoniou, M. N.; Benbrook, C. M.; Carroll, L.; Colborn, T.; Everett, L. G.; Hansen, M.; Landrigan, P. J.; Lanphear, B. P.; et al. Is it Time to Reassess Current Safety Standards for Glyphosate-Based Herbicides? J. Epidemiol. Commun. Health. 2017, 71, 613–618. DOI: 10.1136/jech-2016-208463.
  • Rendon-von Osten, J.; Dzul-Caamal, R. Glyphosate Residues in Groundwater, Drinking Water and Urine of Subsistence Farmers from Intensive Agriculture Localities: A Survey in Hopelchén, Campeche, Mexico. IJERPH. 2017, 14, 595. DOI: 10.3390/ijerph14060595.
  • Van Stempvoort, D. R.; Spoelstra, J.; Senger, N. D.; Brown, S. J.; Post, R.; Struger, J. Glyphosate Residues in Rural Groundwater, Nottawasaga River Watershed, Ontario, Canada: Glyphosate Residues in Rural Groundwater and Transmission to Surface Waters. Pest. Manag. Sci. 2016, 72, 1862–1872. DOI: 10.1002/ps.4218.
  • Peruzzo, P. J.; Porta, A. A.; Ronco, A. E. Levels of Glyphosate in Surface Waters, Sediments and Soils Associated with Direct Sowing Soybean Cultivation in North Pampasic Region of Argentina. Environ. Pollut. 2008, 156, 61–66. DOI: 10.1016/j.envpol.2008.01.015.
  • Mörtl, M.; Németh, G.; Juracsek, J.; Darvas, B.; Kamp, L.; Rubio, F.; Székács, A. Determination of Glyphosate Residues in Hungarian Water Samples by Immunoassay. Microchem. J. 2013, 107, 143–151. DOI: 10.1016/j.microc.2012.05.021.
  • Kaiser, K. Preliminary Study of Pesticide Drift into the Maya Mountain Protected Areas of Belize. Bull. Environ. Contam. Toxicol. 2011, 86, 56–59. DOI: 10.1007/s00128-010-0167-x.
  • Struger, J.; Thompson, D.; Staznik, B.; Martin, P.; McDaniel, T.; Marvin, C. Occurrence of Glyphosate in Surface Waters of Southern Ontario. Bull. Environ. Contam. Toxicol. 2008, 80, 378–384. DOI: 10.1007/s00128-008-9373-1.
  • Byer, J. D.; Struger, J.; Klawunn, P.; Todd, A.; Sverko, E. Low Cost Monitoring of Glyphosate in Surface Waters Using the ELISA Method: An Evaluation. Environ. Sci. Technol. 2008, 42, 6052–6057.
  • Van Stempvoort, D. R.; Roy, J. W.; Brown, S. J.; Bickerton, G. Residues of the Herbicide Glyphosate in Riparian Groundwater in Urban Catchments. Chemosphere. 2014, 95, 455–463. DOI: 10.1016/j.chemosphere.2013.09.095.
  • Ruiz-Toledo, J.; Castro, R.; Rivero-Pérez, N.; Bello-Mendoza, R.; Sánchez, D. Occurrence of Glyphosate in Water Bodies Derived from Intensive Agriculture in a Tropical Region of Southern Mexico. Bull. Environ. Contam. Toxicol. 2014, 93, 289–293. DOI: 10.1007/s00128-014-1328-0.
  • Gonçalves, B. B.; Nascimento, N. F.; Santos, M. P.; Bertolini, R. M.; Yasui, G. S.; Giaquinto, P. C. Low Concentrations of Glyphosate-Based Herbicide Cause Complete Loss of Sperm Motility of Yellowtail Tetra Fish Astyanax Lacustris: Herbicide Kills A. Lacustris Sperm Cells. J. Fish Biol. 2018, 92, 1218–1224. DOI: 10.1111/jfb.13571.
  • Fiorino, E.; Sehonova, P.; Plhalova, L.; Blahova, J.; Svobodova, Z.; Faggio, C. Effects of Glyphosate on Early Life Stages: comparison between Cyprinus Carpio and Danio rerio. Environ. Sci. Pollut. Res. Int. 2018, 25, 8542–8549. DOI: 10.1007/s11356-017-1141-5.
  • Terrazas-Salgado, L.; García-Gasca, A.; Betancourt-Lozano, M.; Llera-Herrera, R.; Alvarado-Cruz, I.; Yáñez-Rivera, B. Epigenetic Transgenerational Modifications Induced by Xenobiotic Exposure in. Front Cell Dev. Biol. 2022, 10, 832982.
  • Horzmann, K. A.; Freeman, J. L. Toxicogenomic Evaluation Using the Zebrafish Model System. In Encyclopedia of Analytical Chemistry; Meyers, R. A., Ed.; John Wiley & Sons, Ltd: Chichester, UK, 2017; pp 1–19.
  • Horzmann, K. A.; Freeman, J. L. Making Waves: New Developments in Toxicology with the Zebrafish. Toxicol. Sci. 2018, 163, 5–12. DOI: 10.1093/toxsci/kfy044.
  • Lai, K. P.; Gong, Z.; Tse, W. K. F. Zebrafish as the Toxicant Screening Model: Transgenic and Omics Approaches. Aquat. Toxicol. 2021, 234, 105813. DOI: 10.1016/j.aquatox.2021.105813.
  • Pereira, A. C.; Gomes, T.; Ferreira Machado, M. R.; Rocha, T. L. The Zebrafish Embryotoxicity Test (ZET) for Nanotoxicity Assessment: From Morphological to Molecular Approach. Environ. Pollut. 2019, 252, 1841–1853. DOI: 10.1016/j.envpol.2019.06.100.
  • OECD. Test No. 236: Fish Embryo Acute Toxicity (FET) Test. OECD:, 2013. https://www.oecd-ilibrary.org/environment/test-no-236-fish-embryo-acute-toxicity-fet-test_9789264203709-en
  • Wang, W.-Q.; Chen, H.-H.; Zhao, W.-J.; Fang, K.-M.; Sun, H.-J.; Zhu, F.-Y. Ecotoxicological Assessment of Spent Battery Extract Using Zebrafish Embryotoxicity Test: A Multi-Biomarker Approach. Chemosphere 2022, 287, 132120. DOI: 10.1016/j.chemosphere.2021.132120.
  • Wlodkowic, D.; Campana, O. Toward High-Throughput Fish Embryo Toxicity Tests in Aquatic Toxicology. Environ. Sci. Technol. 2021, 55, 3505–3513.
  • Ribeiro, R. X.; Silva Brito, R. d.; Pereira, A. C.; Monteiro, KeS.; Gonçalves, B. B.; Rocha, T. L. Ecotoxicological Assessment of Effluents from Brazilian Wastewater Treatment Plants Using Zebrafish Embryotoxicity Test: A Multi-Biomarker Approach. Sci. Total. Environ. 2020, 735, 139036. DOI: 10.1016/j.scitotenv.2020.139036.
  • Cassar, S.; Adatto, I.; Freeman, J. L.; Gamse, J. T.; Iturria, I.; Lawrence, C.; Muriana, A.; Peterson, R. T.; Van Cruchten, S.; Zon, L. I. Use of Zebrafish in Drug Discovery Toxicology. Chem. Res. Toxicol. 2020, 33, 95–118.
  • Uren Webster, T. M.; Laing, L. V.; Florance, H.; Santos, E. M. Effects of Glyphosate and Its Formulation, Roundup, on Reproduction in Zebrafish (Danio rerio). Environ. Sci. Technol. 2014, 48, 1271–1279.
  • Lopes, F. M.; Varela Junior, A. S.; Corcini, C. D.; Silva, A. d.; Guazzelli, V. G.; Tavares, G.; Rosa, C. d Effect of Glyphosate on the Sperm Quality of Zebrafish Danio rerio. Aquat. Toxicol. 2014, 155, 322–326. DOI: 10.1016/j.aquatox.2014.07.006.
  • Díaz-Martín, R. D.; Carvajal-Peraza, A.; Yáñez-Rivera, B.; Betancourt-Lozano, M. Short Exposure to Glyphosate Induces Locomotor, Craniofacial, and Bone Disorders in Zebrafish (Danio rerio) Embryos. Environ. Toxicol. Pharmacol. 2021, 87, 103700. DOI: 10.1016/j.etap.2021.103700.
  • Gaur, H.; Bhargava, A. Glyphosate Induces Toxicity and Modulates Calcium and NO Signaling in Zebrafish Embryos. Biochem. Biophys. Res. Commun. 2019, 513, 1070–1075. DOI: 10.1016/j.bbrc.2019.04.074.
  • Roy, N. M.; Ochs, J.; Zambrzycka, E.; Anderson, A. Glyphosate Induces Cardiovascular Toxicity in Danio rerio. Environ. Toxicol. Pharmacol. 2016, 46, 292–300. DOI: 10.1016/j.etap.2016.08.010.
  • Zhang, S.; Xu, J.; Kuang, X.; Li, S.; Li, X.; Chen, D.; Zhao, X.; Feng, X. Biological Impacts of Glyphosate on Morphology, Embryo Biomechanics and Larval Behavior in Zebrafish (Danio rerio). Chemosphere. 2017, 181, 270–280. DOI: 10.1016/j.chemosphere.2017.04.094.
  • Forner-Piquer, I.; Faucherre, A.; Byram, J.; Blaquiere, M.; Bock, F. d.; Gamet-Payrastre, L.; Ellero-Simatos, S.; Audinat, E.; Jopling, C.; Marchi, N. Differential Impact of Dose-Range Glyphosate on Locomotor Behavior, Neuronal Activity, Glio-Cerebrovascular Structures, and Transcript Regulations in Zebrafish Larvae. Chemosphere. 2021, 267, 128986. DOI: 10.1016/j.chemosphere.2020.128986.
  • Bridi, D.; Altenhofen, S.; Gonzalez, J. B.; Reolon, G. K.; Bonan, C. D. Glyphosate and Roundup® Alter Morphology and Behavior in Zebrafish. Toxicology. 2017, 392, 32–39. DOI: 10.1016/j.tox.2017.10.007.
  • Lanzarin, G. A. B.; Venâncio, C. A. S.; Monteiro, S. M.; Félix, L. M. Behavioural Toxicity of Environmental Relevant Concentrations of a Glyphosate Commercial formulation – RoundUp® UltraMax - during Zebrafish Embryogenesis. Chemosphere. 2020, 253, 126636. DOI: 10.1016/j.chemosphere.2020.126636.
  • Lawrence, C. The Husbandry of Zebrafish (Danio rerio): A Review. Aquaculture. 2007, 269, 1–20. DOI: 10.1016/j.aquaculture.2007.04.077.
  • OECD. Test No. 229: Fish Short Term Reproduction Assay. OECD:, 2012. https://www.oecd-ilibrary.org/environment/test-no-229-fish-short-term-reproduction-assay_9789264185265-en
  • Collymore, C. Anesthesia, Analgesia, and Euthanasia of the Laboratory Zebrafish. In The Zebrafish in Biomedical Research; Elsevier, 2020; pp 403–413. DOI: 10.1016/B978-0-12-812431-4.00034-8.
  • Jensen, P. K.; Wujcik, C. E.; McGuire, M. K.; McGuire, M. A. Validation of Reliable and Selective Methods for Direct Determination of Glyphosate and Aminomethylphosphonic Acid in Milk and Urine Using LC-MS/MS. J. Environ. Sci. Health. B. 2016, 51, 254–259. DOI: 10.1080/03601234.2015.1120619.
  • Martin, M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnet J. 2011, 17, 10. DOI: 10.14806/ej.17.1.200.
  • Grabherr, M. G.; Haas, B. J.; Yassour, M.; Levin, J. Z.; Thompson, D. A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome. Nat. Biotechnol. 2011, 29, 644–652. DOI: 10.1038/nbt.1883.
  • Bray, N. L.; Pimentel, H.; Melsted, P.; Pachter, L. Near-Optimal Probabilistic RNA-Seq Quantification. Nat. Biotechnol. 2016, 34, 525–527. DOI: 10.1038/nbt.3519.
  • Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. EdgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data. Bioinformatics. 2010, 26, 139–140. DOI: 10.1093/bioinformatics/btp616.
  • Lawson, J. Design and Analysis of Experiments with R. CRC Press, Taylor & Francis Group: Boca Raton, 2015; pp 596.
  • Brito Rodrigues, L. d.; Oliveira, R. d.; Abe, F. R.; Brito, L. B.; Moura, D. S.; Valadares, M. C.; Grisolia, C. K.; Oliveira, D. d.; Oliveira, G. d Ecotoxicological Assessment of Glyphosate-Based Herbicides: Effects on Different Organisms: Ecotoxicity of Glyphosate-Based Herbicides. Environ. Toxicol. Chem. 2017, 36, 1755–1763. DOI: 10.1002/etc.3580.
  • Sulukan, E.; Köktürk, M.; Ceylan, H.; Beydemir, Ş.; Işik, M.; Atamanalp, M.; Ceyhun, S. B. An Approach to Clarify the Effect Mechanism of Glyphosate on Body Malformations during Embryonic Development of Zebrafish (Daino Rerio). Chemosphere. 2017, 180, 77–85. DOI: 10.1016/j.chemosphere.2017.04.018.
  • Pereira, A. G.; Jaramillo, M. L.; Remor, A. P.; Latini, A.; Davico, C. E.; Silva, M. L.; da; Müller, Y. M. R.; Ammar, D.; Nazari, E. M. Low-Concentration Exposure to Glyphosate-Based Herbicide Modulates the Complexes of the Mitochondrial Respiratory Chain and Induces Mitochondrial Hyperpolarization in the Danio rerio Brain. Chemosphere. 2018, 209, 353–362. DOI: 10.1016/j.chemosphere.2018.06.075.
  • Costas-Ferreira, C.; Durán, R.; Faro, L. R. F. Toxic Effects of Glyphosate on the Nervous System: A Systematic Review. IJMS. 2022, 23, 4605. DOI: 10.3390/ijms23094605.
  • Costa, M. J.; Monteiro, D. A.; Oliveira-Neto, A. L.; Rantin, F. T.; Kalinin, A. L. Oxidative Stress Biomarkers and Heart Function in Bullfrog Tadpoles Exposed to Roundup Original®. Ecotoxicology. 2008, 17, 153–163. DOI: 10.1007/s10646-007-0178-5.
  • Sandrini, J. Z.; Rola, R. C.; Lopes, F. M.; Buffon, H. F.; Freitas, M. M.; Martins, CdM.; Rosa, C. d Effects of Glyphosate on Cholinesterase Activity of the Mussel Perna Perna and the Fish Danio rerio and Jenynsia Multidentata: In Vitro Studies. Aquat. Toxicol. 2013, 130–131, 171–173. DOI: 10.1016/j.aquatox.2013.01.006.
  • Uren Webster, T. M.; Santos, E. M. Global Transcriptomic Profiling Demonstrates Induction of Oxidative Stress and of Compensatory Cellular Stress Responses in Brown Trout Exposed to Glyphosate and Roundup. BMC Genomics. 2015, 16, 32. DOI: 10.1186/s12864-015-1254-5.
  • Babalola, O. O.; Truter, J. C.; Wyk, J. H. Mortality, Teratogenicity and Growth Inhibition of Three Glyphosate Formulations Using Frog Embryo Teratogenesis Assay‐Xenopus. J. Appl. Toxicol. 2019, 39, 1257–1266. DOI: 10.1002/jat.3811.
  • Giaquinto, P. C.; Sá, M. d.; Sugihara, V. S.; Gonçalves, B. B.; Delício, H. C.; Barki, A. Effects of Glyphosate-Based Herbicide Sub-Lethal Concentrations on Fish Feeding Behavior. Bull. Environ. Contam. Toxicol. 2017, 98, 460–464. DOI: 10.1007/s00128-017-2037-2.
  • Howe, K.; Clark, M. D.; Torroja, C. F.; Torrance, J.; Berthelot, C.; Muffato, M.; Collins, J. E.; Humphray, S.; McLaren, K.; Matthews, L.; et al. The Zebrafish Reference Genome Sequence and Its Relationship to the Human Genome. Nature. 2013, 496, 498–503. DOI: 10.1038/nature12111.
  • Blanc, M.; Antczak, P.; Cousin, X.; Grunau, C.; Scherbak, N.; Rüegg, J.; Keiter, S. H. The Insecticide Permethrin Induces Transgenerational Behavioral Changes Linked to Transcriptomic and Epigenetic Alterations in Zebrafish (Danio rerio). Sci. Total Environ. 2021, 779, 146404. DOI: 10.1016/j.scitotenv.2021.146404.
  • Rusconi, M.; Bettinetti, R.; Polesello, S.; Stefani, F. Evolutionary Toxicology as a Tool to Assess the Ecotoxicological Risk in Freshwater Ecosystems. Water. 2018, 10, 490. DOI: 10.3390/w10040490.
  • Denslow, N. D.; Garcia-Reyero, N.; Barber, D. S. Fish ‘n’ Chips: The Use of Microarrays for Aquatic Toxicology. Mol. Biosyst. 2007, 3, 172–177.
  • Qian, L.; Qi, S.; Wang, Z.; Magnuson, J. T.; Volz, D. C.; Schlenk, D.; Jiang, J.; Wang, C. Environmentally Relevant Concentrations of Boscalid Exposure Affects the Neurobehavioral Response of Zebrafish by Disrupting Visual and Nervous Systems. J. Hazard. Mater. 2021, 404, 124083. DOI: 10.1016/j.jhazmat.2020.124083.
  • Klein, C.; Mikutta, J.; Krueger, J.; Scholz, K.; Brinkmann, J.; Liu, D.; Veerkamp, J.; Siegel, D.; Abdelilah-Seyfried, S.; Noble, F. l Neuron Navigator 3a Regulates Liver Organogenesis During Zebrafish Embryogenesis. Development. 2011, 138, 1935–1945. DOI: 10.1242/dev.056861.
  • Stringham, E. G.; Schmidt, K. L. Navigating the Cell: UNC-53 and the Navigators, a Family of Cytoskeletal Regulators with Multiple Roles in Cell Migration, Outgrowth and Trafficking. Cell Adh. Migr. 2009, 3, 342–346. DOI: 10.4161/cam.3.4.9451.
  • Martínez-López, M. J.; Alcántara, S.; Mascaró, C.; Pérez-Brangulí, F.; Ruiz-Lozano, P.; Maes, T.; Soriano, E.; Buesa, C. Mouse Neuron Navigator 1, a Novel Microtubule-Associated Protein Involved in Neuronal Migration. Mol. Cell Neurosci. 2005, 28, 599–612. DOI: 10.1016/j.mcn.2004.09.016.
  • Larrivee, B.; Freitas, C.; Trombe, M.; Lv, X.; DeLafarge, B.; Yuan, L.; Bouvree, K.; Breant, C.; Del Toro, R.; Brechot, N.; et al. Activation of the UNC5B Receptor by Netrin-1 Inhibits Sprouting Angiogenesis. Genes Dev. 2007, 21, 2433–2447. DOI: 10.1101/gad.437807.
  • Muley, P. D.; McNeill, E. M.; Marzinke, M. A.; Knobel, K. M.; Barr, M. M.; Clagett-Dame, M. The atRA-Responsive Gene Neuron Navigator 2 Functions in Neurite Outgrowth and Axonal Elongation. Dev. Neurobiol. 2008, 68, 1441–1453. DOI: 10.1002/dneu.20670.
  • Olivari, S.; Molinari, M. Glycoprotein Folding and the Role of EDEM1, EDEM2 and EDEM3 in Degradation of Folding-Defective Glycoproteins. FEBS Lett. 2007, 581, 3658–3664. DOI: 10.1016/j.febslet.2007.04.070.
  • Bar-Peled, L.; Chantranupong, L.; Cherniack, A. D.; Chen, W. W.; Ottina, K. A.; Grabiner, B. C.; Spear, E. D.; Carter, S. L.; Sabatini, D. M. A Tumor Suppressor Complex with GAP Activity for the Rag GTPases That Signal Amino Acid Sufficiency to mTORC, 2013, p 11. DOI: 10.1126/science.123204.
  • Hallett, J. E. H.; Manning, B. D. CASTORing New Light on Amino Acid Sensing. Cell. 2016, 165, 15–17. DOI: 10.1016/j.cell.2016.03.002.
  • Faria, M.; Bedrossiantz, J.; Ramírez, J. R. R.; Mayol, M.; García, G. H.; Bellot, M.; Prats, E.; Garcia-Reyero, N.; Gómez-Canela, C.; Gómez-Oliván, L. M.; et al. Glyphosate Targets Fish Monoaminergic Systems Leading to Oxidative Stress and Anxiety. Environ. Int. 2021, 146, 106253. DOI: 10.1016/j.envint.2020.106253.
  • Pereiro, P.; Librán-Pérez, M.; Figueras, A.; Novoa, B. Conserved Function of Zebrafish (Danio rerio) Gdf15 as a Sepsis Tolerance Mediator. Dev. Comp. Immunol. 2020, 109, 103698. DOI: 10.1016/j.dci.2020.103698.
  • Zhang, D.; Lin, W.; Liu, Y.; Guo, H.; Wang, L.; Yang, L.; Li, L.; Li, D.; Tang, R. Chronic Microcystin-LR Exposure Induces Abnormal Lipid Metabolism via Endoplasmic Reticulum Stress in Male Zebrafish. Toxins. 2020, 12, 107. DOI: 10.3390/toxins12020107.
  • Pruvot, B.; Curé, Y.; Djiotsa, J.; Voncken, A.; Muller, M. Developmental Defects in Zebrafish for Classification of EGF Pathway Inhibitors. Toxicol. Appl. Pharmacol. 2014, 274, 339–349. DOI: 10.1016/j.taap.2013.11.006.
  • Chen, Y. Y.; Zhu, J. Y.; Chan, K. M. Effects of Cadmium on Cell Proliferation, Apoptosis, and Proto-Oncogene Expression in Zebrafish Liver Cells. Aquat. Toxicol. 2014, 157, 196–206. DOI: 10.1016/j.aquatox.2014.10.018.
  • Kang, J. W.; Kim, Y.; Lee, Y.; Myung, K.; Kim, Y. H.; Oh, C. AML Poor Prognosis Factor, TPD52, is Associated with the Maintenance of Haematopoietic Stem Cells through Regulation of Cell Proliferation. J. Cell Biochem. 2021, 122, 403–412. DOI: 10.1002/jcb.29869.
  • Strähle, U.; Scholz, S.; Geisler, R.; Greiner, P.; Hollert, H.; Rastegar, S.; Schumacher, A.; Selderslaghs, I.; Weiss, C.; Witters, H.; Braunbeck, T. Zebrafish Embryos as an Alternative to Animal Experiments—a Commentary on the Definition of the Onset of Protected Life Stages in Animal Welfare Regulations. Reprod. Toxicol. 2012, 33, 128–132. DOI: 10.1016/j.reprotox.2011.06.121.
  • Ashley, P. J. Fish Welfare: Current Issues in Aquaculture. Appl. Anim. Behav. Sci. 2007, 104, 199–235. DOI: 10.1016/j.applanim.2006.09.001.

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.