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Paraquat and Parkinson’s disease: a systematic review and meta-analysis of observational studies

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References

  • Adler, C. H., and T. G. Beach. 2016. Neuropathological basis of nonmotor manifestations of Parkinson’s disease. Mov. Disord. 31:1114–19. doi:10.1002/mds.16605.
  • Ali, K., and H. R. Morris. 2015. Parkinson’s disease: Chameleons and mimics. Pract. Neurol. 15:14–25. doi:10.1136/practneurol-2014-000849.
  • Allen, M. T., and L. S. Levy. 2013. Parkinson’s disease and pesticide exposure – A new assessment. Crit. Rev. Toxicol. 43:515–34. doi:10.3109/10408444.2013.798719.
  • Angerer, J., U. Ewers, and M. Wilhelm. 2007. Human biomonitoring: state of the art. Int. J. Hyg. Environ. Health 210:201–28. doi:10.1016/j.ijheh.2007.01.024.
  • ANVISA. Agência Nacional de Vigilância Sanitária. 2017. Analisa a reavaliação toxicológica do ingrediente ativo Paraquate [Analyzes the toxicological revaluation of the active ingredient Paraquat]. http://portal.anvisa.gov.br/documents/219201/2782895/Voto+Renato+Paraquate/fa409d90-a520-4302-9815-f39b683da509.
  • Bain, P., M. Brin, G. Deuschl, R. Elble, J. Jankovic, L. Findley, W. C. Koller, and R. Pahwa. 2000. Criteria for the diagnosis of essential tremor. Neurology 54:S7.
  • Balshem, H., M. Helfand, H. J. Schünemann, A. D. Oxman, R. Kunz, J. Brozek, G. E. Vist, Y. Falck-Ytter, J. Meerpohl, S. Norris, et al. 2011. GRADE guidelines: 3. Rating the quality of evidence. J. Clin. Epidemiol. 64:401–06. doi:10.1016/j.jclinepi.2010.07.015.
  • Barlow, B. K., M. J. Thiruchelvam, L. Bennice, D. A. Cory-Slechta, N. Ballatori, and E. K. Richfield. 2003. Increased synaptosomal dopamine content and brain concentration of paraquat produced by selective dithiocarbamates. J. Neurochem. 85:1075–86. doi:10.1046/j.1471-4159.2003.01773.x.
  • Bernheimer, H., W. Birkmayer, O. Hornykiewicz, K. Jellinger, and F. Seitelberger. 1973. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 20:415–55. doi:10.1016/0022-510x(73)90175-5.
  • Blesa, J., S. Phani, V. Jackson-Lewis, and S. Przedborski. 2012. Classic and new animal models of Parkinson's disease. J Biomed Biotechnol 2012:845618. doi:10.1155/2012/845618.
  • Blesa, J., I. Trigo-Damas, M. Dileone, N. L. Del Rey, L. F. Hernandez, and J. A. Obeso. 2017. Compensatory mechanisms in Parkinson’s disease: Circuits adaptations and role in disease modification. Exp. Neurol. 298:148–61. doi:10.1016/j.expneurol.2017.10.002.
  • Breckenridge, C. B., C. Berry, E. T. Chang, R. L. Sielken, and J. S. Mandel. 2016. Association between Parkinson’s disease and cigarette smoking, rural living, well-water consumption, farming and pesticide use: Systematic review and meta-analysis. PLoS ONE 11:e0151841. doi:10.1371/journal.pone.0151841.
  • Brent, J., and T. H. Schaeffer. 2011. Systematic review of Parkinsonian syndromes in short- and long-term survivors of paraquat poisoning. J. Occup. Environ. Med. 53:1332–36. doi:10.1097/JOM.0b013e318233775d.
  • Brouwer, M., A. Huss, M. van der Mark, P. C. G. Nijssen, W. M. Mulleners, A. M. G. Sas, T. van Laar, G. R. de Snoo, H. Kromhout, and R. C. H. Vermeulen. 2017. Environmental exposure to pesticides and the risk of Parkinson’s disease in the Netherlands. Environ. Int. 107:100–10. doi:10.1016/j.envint.2017.07.001.
  • Brown, T. P., P. C. Rumsby, A. C. Capleton, L. Rushton, and L. S. Levy. 2006. Pesticides and Parkinson’s disease - Is there a link? Environ. Health Perspect. 114:156–64. doi:10.1289/ehp.8095.
  • Cannon, J. R., and J. T. Greenamyre. 2013. Gene-environment interactions in Parkinson’s disease: Specific evidence in humans and mammalian models. Neurobiol. Dis. 57:38–46. doi:10.1016/j.nbd.2012.06.025.
  • Castello, P. R., D. A. Drechsel, and M. Patel. 2007. Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J. Biol. Chem. 282:14186–93. doi:10.1074/jbc.M700827200.
  • Chaudhuri, K. R., and P. Martinez-Martin. 2008. Quantitation of non-motor symptoms in Parkinson’s disease. Eur. J. Neurol. 15 (Suppl 2):2–7. doi:10.1111/j.1468-1331.2008.02212.x.
  • Cheng, H. C., C. M. Ulane, and R. E. Burke. 2010. Clinical progression in Parkinson disease and the neurobiology of axons. Ann. Neurol. 67:715–25. doi:10.1002/ana.21995.
  • Cheng, Y. H., W. C. Chou, Y. F. Yang, C. W. Huang, C. M. How, S. C. Chen, W. Y. Chen, N. H. Hsieh, Y. J. Lin, S. H. You, et al. 2018. PBPK/PD assessment for Parkinson’s disease risk posed by airborne pesticide paraquat exposure. Environ. Sci. Pollut. Res. Int. 25:5359–68. doi:10.1007/s11356-017-0875-4.
  • Chinta, S. J., G. Woods, M. Demaria, A. Rane, Y. Zou, A. McQuade, S. Rajagopalan, C. Limbad, D. T. Madden, J. Campisi, et al. 2018. Cellular senescence is induced by the environmental neurotoxin paraquat and contributes to neuropathology linked to Parkinson’s disease. Cell Rep. 22:930–40. doi:10.1016/j.celrep.2017.12.092.
  • Cicchetti, F., J. Drouin-Ouellet, and R. E. Gross. 2009. Environmental toxins and Parkinson’s disease: what have we learned from pesticide-induced animal models?. Trends Pharmacol. Sci. 30:475–83. doi:10.1016/j.tips.2009.06.005.
  • Costello, S., M. Cockburn, J. Bronstein, X. Zhang, and B. Ritz. 2009. Parkinson’s disease and residential exposure to maneb and paraquat from agricultural applications in the Central Valley of California. Am. J. Epidemiol. 169:919–26. doi:10.1093/aje/kwp006.
  • Dauer, W., and S. Przedborski. 2003. Parkinson’s disease: Mechanisms and models. Neuron 39:889–909. doi:10.1016/s0896-6273(03)00568-3.
  • de Rijk, M. C., L. J. Launer, K. Berger, M. M. Breteler, J. F. Dartigues, M. Baldereschi, L. Fratiglioni, A. Lobo, J. Martinez-Lage, C. Trenkwalder, et al. 2000. Prevalence of Parkinson’s disease in Europe: A collaborative study of population-based cohorts. Neurologic diseases in the Elderly research group. Neurology 54:S21–S23.
  • Dhillon, A. S., G. L. Tarbutton, J. L. Levin, G. M. Plotkin, L. K. Lowry, J. T. Nalbone, and S. Shepherd. 2008. Pesticide/environmental exposures and Parkinson’s disease in East Texas. J. Agromed. 13:37–48. doi:10.1080/10599240801986215.
  • Dick, F. D., G. De Palma, A. Ahmadi, N. W. Scott, G. J. Prescott, J. Bennett, S. Semple, S. Dick, C. Counsell, P. Mozzoni, et al. 2007. Environmental risk factors for Parkinson’s disease and parkinsonism: The Geoparkinson study. Occup. Environ. Med. 64:666–72. doi:10.1136/oem.2006.027003.
  • Dinis-Oliveira, R. J., F. Remião, H. Carmo, J. A. Duarte, A. S. Navarro, M. L. Bastos, and F. Carvalho. 2006. Paraquat exposure as an etiological factor of Parkinson’s disease. Neurotoxicol. 27:1110–22. doi:10.1016/j.neuro.2006.05.012.
  • Dorsey, E. R., R. Constantinescu, J. P. Thompson, K. M. Biglan, R. G. Holloway, K. Kieburtz, F. J. Marshall, B. M. Ravina, G. Schifitto, A. Siderowf, et al. 2007. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68:384–86. doi:10.1212/01.wnl.0000247740.47667.03.
  • Durrheim, D. N., and A. Reingold. 2010. Modifying the GRADE framework could benefit public health. J. Epidemiol. Community Health 64:387. doi:10.1136/jech.2009.103226.
  • Elbaz, A., J. Clavel, P. J. Rathouz, F. Moisan, J. P. Galanaud, B. Delemotte, A. Alpérovitch, and C. Tzourio. 2009. Professional exposure to pesticides and Parkinson disease. Ann. Neurol. 66:494–504. doi:10.1002/ana.21717.
  • Elble, R. J. 2000. Diagnostic criteria for essential tremor and differential diagnosis. Neurology 54:S2–S6.
  • Engel, L., H. Checkoway, M. Keifer, N. Seixas, W. Longstreth, K. Scott, K. Hudnellh, W. K. Angerf, and R. Camicioli. 2001. Parkinsonism and occupational exposure to pesticides. Occup. Environ. Med. 58:582–89. doi:10.1136/oem.58.9.582.
  • Fearnley, J. M., and A. J. Lees. 1991. Ageing and Parkinson’s disease: Substantia nigra regional selectivity. Brain 114:2283–301. doi:10.1093/brain/114.5.2283.
  • Fedak, K. M., A. Bernal, Z. A. Capshaw, and S. Gross. 2015. Applying the Bradford Hill criteria in the 21st century: How data integration has changed causal inference in molecular epidemiology. Emerg Themes Epidemiol 12:14. doi:10.1186/s12982-015-0037-4.
  • Fei, Q., and D. W. Ethell. 2008. Maneb potentiates paraquat neurotoxicity by inducing key Bcl-2 family members. J. Neurochem. 105:2091–97. doi:10.1111/j.1471-4159.2008.05293.x.
  • Feng, L. R., and K. A. Maguire-Zeiss. 2011. Dopamine and paraquat enhance alpha-synuclein-induced alterations in membrane conductance. Neurotox Res 20:387–401. doi:10.1007/s12640-011-9255-x.
  • Firestone, J. A., J. I. Lundin, K. M. Powers, T. Smith-Weller, G. M. Franklin, P. D. Swanson, W. T. Longstreth, and H. C. Jr. 2010. Occupational factors and risk of Parkinson’s disease: A population-based case–control study. Am. J. Ind. Med. 53:217–23. doi:10.1002/ajim.20788.
  • Firestone, J. A., T. Smith-Weller, G. Franklin, P. Swanson, W. T. Longstreth, and H. Checkoway. 2005. Pesticides and risk of Parkinson disease. A population-based case-control study. Arch. Neurol. 62:91–95. doi:10.1001/archneur.62.1.91.
  • Fleming, S. M. 2017. Mechanisms of gene-environment interactions in Parkinson’s disease. Curr. Environ. Health Rep. 4:192–99. doi:10.1007/s40572-017-0143-2.
  • Freire, C., and S. Koifman. 2012. Pesticide exposure and Parkinson’s disease: Epidemiological evidence of association. Neurotoxicol. 33:947–71. doi:10.1016/j.neuro.2012.05.011.
  • Furlong, M., C. M. Tanner, S. M. Goldman, G. S. Bhudhikanok, A. Blair, A. Chade, K. Comyns, J. A. Hoppin, M. Kasten, and M. Korell. 2015. Protective glove use and hygiene habits modify the associations of specific pesticides with Parkinson’s disease. Environ. Int. 75:144–50. doi:10.1016/j.envint.2014.11.002.
  • Gatto, N. M., M. Cockburn, J. Bronstein, A. D. Manthripragada, and B. Ritz. 2009. Well-water consumption and Parkinson’s disease in rural California. Environ. Health Perspect. 117:1912–18. doi:10.1289/ehp.0900852.
  • Gatto, N. M., S. L. Rhodes, A. D. Manthripragada, J. Bronstein, M. Cockburn, M. Farrer, and B. Ritz. 2010. Synuclein gene may interact with environmental factors in increasing risk of Parkinson’s disease. Neuroepidemiology 35:191–95. doi:10.1159/000315157.
  • Gelb, D. J., E. Oliver, and S. Gilman. 1999. Diagnostic criteria for Parkinson disease. Arch. Neurol. 56:33–39. doi:10.1001/archneur.56.1.33.
  • Giasson, B. I., J. E. Duda, I. V. Murray, Q. Chen, J. M. Souza, H. I. Hurtig, H. Ischiropoulos, J. Q. Trojanowski, and V. M. Lee. 2000. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Sci. 290:985–89. doi:10.1126/science.290.5493.985.
  • Goetz, C. G. 2011. The history of Parkinson’s disease: Early clinical descriptions and neurological therapies. Cold Spring Harb. Perspect. Med. 1:a008862. doi:10.1101/cshperspect.a008862.
  • Goldman, S. M., F. Kamel, G. W. Ross, G. S. Bhudhikanok, J. A. Hoppin, M. Korell, C. Marras, C. Meng, D. M. Umbach, and M. Kasten. 2012. Genetic modification of the association of paraquat and Parkinson’s disease. Mov. Disord. 27:1652–58. doi:10.1002/mds.25216.
  • Guyatt, G. H., A. D. Oxman, G. Vist, R. Kunz, J. Brozek, P. Alonso-Coello, V. Montori, E. A. Akl, B. Djulbegovic, Y. Falck-Ytter, et al. 2011a. GRADE guidelines: 4. Rating the quality of evidence - study limitations (risk of bias). J. Clin. Epidemiol. 64:407–15. doi:10.1016/j.jclinepi.2010.07.017.
  • Guyatt, G. H., A. D. Oxman, G. E. Vist, R. Kunz, Y. Falck-Ytter, P. Alonso-Coello, H. J. Schünemann, and GRADE Working Group. 2008. GRADE: An emerging consensus on rating quality of evidence and strength of recommendations. Br. Med. J. 336:924–26. doi:10.1136/bmj.39489.470347.AD.
  • Guyatt, G. H., A. D. Oxman, R. Kunz, J. Brozek, P. Alonso-Coello, D. Rind, P. J. Devereaux, V. M. Montori, B. Freyschuss, G. Vist, et al. 2011b. GRADE guidelines 6. Rating the quality of evidence—imprecision. J. Clin. Epidemiol. 64:1283–93. doi:10.1016/j.jclinepi.2011.01.012.
  • Guyatt, G. H., A. D. Oxman, R. Kunz, J. Woodcock, J. Brozek, M. Helfand, P. Alonso-Coello, P. Glasziou, R. Jaeschke, E. A. Akl, et al. 2011c. GRADE guidelines: 7. Rating the quality of evidence - inconsistency. J. Clin. Epidemiol. 64:1294–302. doi:10.1016/j.jclinepi.2011.03.017.
  • Guyatt, G. H., A. D. Oxman, R. Kunz, J. Woodcock, J. Brozek, M. Helfand, P. Alonso-Coello, Y. Falck-Ytter, R. Jaeschke, G. Vist, et al. 2011d. GRADE guidelines: 8. Rating the quality of evidence - indirectness. J. Clin. Epidemiol. 64:1303–10. doi:10.1016/j.jclinepi.2011.04.014.
  • Guyatt, G. H., A. D. Oxman, S. Sultan, P. Glasziou, E. A. Akl, P. Alonso-Coello, D. Atkins, R. Kunz, J. Brozek, V. Montori, et al. 2011f. GRADE guidelines: 9. Rating up the quality of evidence. J. Clin. Epidemiol. 64:1311–16. doi:10.1016/j.jclinepi.2011.06.004.
  • Guyatt, G. H., A. D. Oxman, V. Montori, G. Vist, R. Kunz, J. Brozek, P. Alonso-Coello, B. Djulbegovic, D. Atkins, Y. Falck-Ytter, et al. 2011e. GRADE guidelines: 5. Rating the quality of evidence - publication bias. J. Clin. Epidemiol. 64:1277–82. doi:10.1016/j.jclinepi.2011.01.011.
  • Guyatt, G. H., and J. W. Busse. 2019. Methods instrument: Tool to assess risk of bias in cohort studies and tool to assess risk of bias in case control studies. In: Evidence partners [Internet]. Accessed June 20, 2017. https://www.evidencepartners.com/resources/methodological-resources.
  • Hancock, D. B., E. R. Martin, G. M. Mayhew, J. M. Stajich, R. Jewett, M. A. Stacy, B. L. Scott, J. M. Vance, and W. K. Scott. 2008. Pesticide exposure and risk of Parkinson’s disease: A family-based case-control study. BMC Neurol. 8:6. doi:10.1186/1471-2377-8-6.
  • Hernandez, D. G., C. Paisan-Ruiz, A. McInerney-Leo, S. Jain, A. Meyer-Lindenberg, E. W. Evans, K. F. Berman, J. Johnson, G. Auburger, A. A. Schaffer, et al. 2005. Clinical and positron emission tomography of Parkinson’s disease caused by LRRK2. Ann. Neurol. 57:453–56. doi:10.1002/ana.20401.
  • Hertzman, C., M. Wiens, B. Snow, S. Kelly, and D. Calne. 1994. A case-control study of Parkinson’s disease in a horticultural region of British Columbia. Mov. Disord. 9:69–75. doi:10.1002/mds.870090111.
  • Hertzman, C., M. Wiens, and D. Bowering. 1990. Parkinson’s disease: A case-control study of occupational and environmental risk factors. Am. J. Indust. Med. 17:349–55. doi:10.1002/ajim.4700170307.
  • Higgins, J. P. T., D. G. Altman, and J. A. C. Sterne. 2011. Assessing risk of bias in included studies. In Cochrane handbook for systematic reviews of interventions Version 5.1.0, ed. J. P. T. Higgins, and S. Green, Chinchester: The Cochrane Collaboration. http://handbook.cochrane.org/.
  • Higgins, J. P. T., S. G. Thompson, J. J. Deeks, and D. G. Altman. 2003. Measuring inconsistency in meta-analyses. Br. Med. J. 327:557–60. doi:10.1136/bmj.327.7414.557.
  • Hill, A. B. 1965. The environment and disease: Association or causation? Proc. Roy Soc. Med. 58:295. doi:10.1177/003591576505800503.
  • Huang, D., J. Xu, J. Wang, J. Tong, X. Bai, H. Li, Z. Wang, Y. Huang, Y. Wu, M. Yu, et al. 2017. Dynamic changes in the nigrostriatal pathway in the MPTP mouse model of Parkinson’s disease. Parkinson’s Dis. 2017:9349487. doi:10.1155/2017/9349487.
  • Hughes, A. J., S. E. Daniel, L. Kilford, and A. J. Lees. 1992b. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease. A clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiat. 55:181–84. doi:10.1136/jnnp.55.3.181.
  • Kalia, L. V., and A. E. Lang. 2015. Parkinson’s disease. Lancet 386:896–912. doi:10.1016/S0140-6736(14)61393-3.
  • Kamel, F., C. Tanner, D. Umbach, J. A. Hoppin, M. C. R. Alavanja, A. Blair, K. Comyns, S. Goldman, M. Korell, J. Langston, et al. 2007. Pesticide exposure and self-reported Parkinson’s disease in the agricultural health study. Am. J. Epidemiol. 165:364–74. doi:10.1093/aje/kwk024.
  • Kamel, F., S. M. Goldman, D. M. Umbach, H. Chen, G. Richardson, M. R. Barber, C. Meng, C. Marras, M. Korell, M. Kasten, et al. 2014. Dietary fat intake, pesticide use, and Parkinson’s disease. Parkinsonism Relat. Disord. 20:82–87. doi:10.1016/j.parkreldis.2013.09.023.
  • Kosaka, K. 2014. Lewy body disease and dementia with Lewy bodies. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 90:301–06. doi:10.2183/pjab.90.301.
  • Kuopio, A. M., R. J. Marttila, H. Helenius, and U. K. Rinne. 1999. Environmental risk factors in Parkinson’s disease. Mov. Disord. 14:928–39.
  • Kuter, K., P. Nowak, K. Golembiowska, and K. Ossowska. 2010. Increased reactive oxygen species production in the brain after repeated low-dose pesticide paraquat exposure in rats: A comparison with peripheral tissues. Neurochem. Res. 35:1121–30. doi:10.1007/s11064-010-0163-x.
  • Lang, A. E., and A. M. Lozano, Parkinson’s disease. 1998. First of two parts. N. Engl. J. Med. 339: 1044–53. doi: 10.1056/NEJM199810083391506.
  • Langston, J. W. 2017. The MPTP story. J. Parkinsons Dis. 7:S11–S19. doi:10.3233/JPD-179006.
  • Lee, P. C., Y. Bordelon, J. Bronstein, and B. Ritz. 2012. Traumatic brain injury, paraquat exposure, and their relationship to Parkinson disease. Neurology 79:2061–66. doi:10.1212/WNL.0b013e3182749f28.
  • Li, A. A., P. J. Mink, L. J. McIntosh, M. J. Teta, and B. Finley. 2005. Evaluation of epidemiologic and animal data associating pesticides with Parkinson’s disease. J. Occup. Environ. Med. 47:1059–87.
  • Liou, H. H., M. C. Tsai, C. J. Chen, J. S. Jeng, Y. C. Chang, S. Y. Chen, and R. C. Chen. 1997. Environmental risk factors and Parkinson’s disease: A case-control study in Taiwan. Neurology 48:1583–88. doi:10.1212/wnl.48.6.1583.
  • Manning-Bog, A. B., A. L. McCormack, J. Li, V. N. Uversky, A. L. Fink, and D. A. Di Monte. 2002. The herbicide paraquat causes up-regulation and aggregation of alpha-synuclein in mice: Paraquat and alpha-synuclein. J. Biol. Chem. 277:1641–44. doi:10.1074/jbc.C100560200.
  • McCormack, A. L., M. Thiruchelvam, A. B. Manning-Bog, C. Thiffault, J. W. Langston, D. A. Cory-Slechta, and D. A. Di Monte. 2002. Environmental risk factors and Parkinson’s disease: Selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 10:119–27.
  • Meredith, G. E., and D. J. Rademacher. 2011. MPTP mouse models of Parkinson’s disease: An update. J. Parkinsons Dis. 1:19–33. doi:10.3233/JPD-2011-11023.
  • Miller, G. W. 2007. Paraquat: The red herring of Parkinson’s disease research. Toxicol. Sci. 100:1–2. doi:10.1093/toxsci/kfm223.
  • Moretto, A., and C. Colosio. 2013. The role of pesticide exposure in the genesis of Parkinson’s disease: Epidemiological studies and experimental data. Toxicol. 307:24–34. doi:10.1016/j.tox.2012.11.021.
  • Narayan, S., Z. Liew, J. M. Bronstein, and B. Ritz. 2017. Occupational pesticide use and Parkinson’s disease in the Parkinson environment gene (PEG) study. Environ. Int. 107:266–73. doi:10.1016/j.envint.2017.04.010.
  • NTP. National Toxicology Program. 2018. Protocol for scoping review of paraquat dichloride exposure and Parkinson’s disease. https://ntp.niehs.nih.gov/ntp/ohat/parkinson/parkinsons_protocol_508.pdf.
  • Ntzani, E. E., M. Chondrogiorgi, G. Nitritsos, and I. Tzoulaki. 2013. Literature review on epidemiological studies linking exposure to pesticides and health effects. EFSA Supp Publ 10:497EN. http://onlinelibrary.wiley.com/doi/10.2903/sp.efsa.2013.EN-497/abstract.
  • Ossowska, K., J. Wardas, M. Smialowska, K. Kuter, T. Lenda, J. M. Wieronska, B. Zieba, P. Nowak, J. Dabrowska, A. Bortel, et al. 2005. A slowly developing dysfunction of dopaminergic nigrostriatal neurons induced by long-term paraquat administration in rats: An animal model of preclinical stages of Parkinson’s disease? Eur. J. Neurosci. 22:1294–304. doi:10.1111/j.1460-9568.2005.04301.x.
  • Pesch, B., B. Kendzia, P. Gustavsson, K. H. Jöckel, G. Johnen, H. Pohlabeln, A. Olsson, W. Ahrens, I. M. Gross, I. Brüske, et al. 2012. Cigarette smoking and lung cancer – relative risk estimates for the major histological types from a pooled analysis of case-control studies. Int. J. Cancer 131:1210–19. doi:10.1002/ijc.27339.
  • Pezzoli, G., and E. Cereda. 2013. Exposure to pesticides or solvents and risk of Parkinson disease. Neurology 80:2035–41. doi:10.1212/WNL.0b013e318294b3c8.
  • Plato, N., and G. Steineck. 1993. Methodology and utility of a job-exposure matrix. Am. J. Ind. Med. 23:491–502.
  • Pouchieu, C., C. Piel, C. Carles, A. Gruber, C. Helmer, S. Tual, E. Marcotullio, P. Lebailly, and I. Baldi. 2018. Pesticide use in agriculture and Parkinson’s disease in the AGRICAN cohort study. Int. J. Epidemiol. 47:299–310. doi:10.1093/ije/dyx225.
  • Ribeiro, A. I., A. Olhero, H. Teixeira, A. Magalhães, and M. F. Pina. 2014. Tools for address georeferencing – limitations and opportunities every public health professional should be aware of. PLoS ONE 9:e114130. doi:10.1371/journal.pone.0114130.
  • Richardson, J. R. 2005. Paraquat neurotoxicity is distinct from that of MPTP and rotenone. Toxicol. Sci. 88:193–201. doi:10.1093/toxsci/kfi304.
  • Ritz, B. R., A. D. Manthripragada, S. Costello, S. J. Lincoln, M. J. Farrer, M. Cockburn, and J. Bronstein. 2009. Dopamine transporter genetic variants and pesticides in Parkinson’s disease. Environ. Health Perspect. 117:964–69. doi:10.1289/ehp.0800277.
  • Rugbjerg, K., M. A. Harris, H. Shen, S. A. Marion, J. K. Tsui, and K. Teschke. 2011. Pesticide exposure and risk of Parkinson’s disease – A population-based case–control study evaluating the potential for recall bias. Scand. J. Work Environ. Health 27:427–36. doi:10.5271/sjweh.3142.
  • Sanders, L. H., K. C. Paul, E. H. Howlett, H. Lawal, S. Boppana, J. M. Bronstein, B. Ritz, and J. T. Greenamyre. 2017. Editor’s highlight: Base excision repair variants and pesticide exposure increase Parkinson’s disease risk. Toxicol. Sci. 158:188–98. doi:10.1093/toxsci/kfx086.
  • Schünemann, H., S. Hill, G. Guyatt, E. A. Akl, and F. Ahmed. 2011. The GRADE approach and Bradford Hill’s criteria for causation. J. Epidemiol. Community Health 65:392–95. doi:10.1136/jech.2010.119933.
  • Seidler, A., W. Hellenbrand, B. P. Robra, P. Vieregge, P. Nischan, and J. Joerg. 1996. Possible environmental, occupational, and other etiologic factors for Parkinson’s disease: A case-control study in Germany. Neurology 46:1275–84. doi:10.1212/wnl.46.5.1275.
  • Semchuk, K. M., E. J. Love, and R. G. Lee. 1992. Parkinson’s disease and exposure to agricultural work and pesticide chemicals. Neurology 42:1328–35. doi:10.1212/wnl.42.7.1328.
  • Shichiri, M. 2014. The role of lipid peroxidation in neurological disorders. J. Clin. Biochem. Nutr. 54:151–60. doi:10.3164/jcbn.14-10.
  • Shimizu, K., K. Ohtaki, K. Matsubara, K. Aoyama, T. Uezono, O. Saito, M. Suno, K. Ogawa, N. Hayase, K. Kimura, et al. 2001. Carrier-mediated processes in blood–brain barrier penetration and neural uptake of paraquat. Brain Res. 906:135–42. doi:10.1016/s0006-8993(01)02577-x.
  • Singleton, A. B., M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, R. Nussbaum, et al. 2003. Alpha-synuclein locus triplication causes Parkinson’s disease. Sci. 302:841. doi:10.1126/science.1090278.
  • Smith, D. M. 2018. Could a common mechanism of protein degradation impairment underlie many neurodegenerative diseases? J. Exp. Neurosci. 12:1179069518794675. doi:10.1177/1179069518794675.
  • Stroup, D. F., J. A. Berlin, S. C. Morton, I. Olkin, G. D. Williamson, D. Rennie, D. Moher, B. J. Becker, T. A. Sipe, and S. B. Thacker. 2000. Meta-analysis of observational studies in epidemiology: a proposal for reporting. J. Am. Med. Assoc. 283:2008–12. doi:10.1001/jama.283.15.2008.
  • Sulzer, D., R. N. Alcalay, F. Garretti, L. Cote, E. Kanter, J. Agin-Liebes, C. Liong, C. McMurtrey, W. H. Hildebrand, X. Mao, et al. 2017. T cells from patients with Parkinson’s disease recognize α-synuclein peptides. Nature 546:656–61. doi:10.1038/nature22815.
  • Swaen, G., and L. van Amelsvoort. 2009. A weight of evidence approach to causal inference. J. Clin. Epidemiol. 62:270–77. doi:10.1016/j.jclinepi.2008.06.013.
  • Tanner, C. M., F. Kamel, G. W. Ross, J. A. Hoppin, S. M. Goldman, M. Korell, C. Marras, G. S. Bhudhikanok, M. Kasten, A. R. Chade, et al. 2011. Rotenone, paraquat, and Parkinson’s disease. Environ. Health Perspect. 119:866–72. doi:10.1289/ehp.1002839.
  • Tanner, C. M., G. W. Ross, S. A. Jewell, R. A. Hauser, J. Jankovic, S. A. Factor, S. Bressman, A. Deligtisch, C. Marras, K. E. Lyons, et al. 2009. Occupation and risk of parkinsonism. A multicenter case-control study. Arch. Neurol. 66:1106–13. doi:10.1001/archneurol.2009.195.
  • The Nordic Cochrane Centre. 2011. The cochrane collaboration. Review manager (RevMan). 5.3. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration.
  • Vaccari, C., R. El Dib, and J. L. V. de Camargo. 2017. Paraquat and Parkinson’s disease: A systematic review protocol according to the OHAT approach for hazard identification. Syst. Rev. 6:98. doi:10.1186/s13643-017-0491-x.
  • van der Mark, M., M. Brouwer, H. Kromhout, P. Nijssen, A. Huss, and R. Vermeulen. 2012.Is pesticide use related to Parkinson Disease? Some clues to heterogeneity in study results. Environ Health Perspect 120: 340–47. doi:10.1289/ehp.1103881.
  • van Der Mark, M., R. Vermeulen, P. C. Nijssen, W. M. Mulleners, A. M. Sas, T. Van Laar, M. Brouwer, A. Huss, and H. Kromhout. 2014. Occupational exposure to pesticides and endotoxin and Parkinson disease in the Netherlands. Occup. Environ. Med. 71:757–64. doi:10.1136/oemed-2014-102170.
  • Van Maele-Fabry, G., P. Hoet, F. Vilain, and D. Lison. 2012. Occupational exposure to pesticides and Parkinson’s disease: A systematic review and meta-analysis of cohort studies. Environ. Int. 46:30–43. doi:10.1016/j.envint.2012.05.004.
  • Wakabayashi, K., K. Tanji, F. Mori, and H. Takahashi. 2007. The Lewy body in Parkinson’s disease: Molecules implicated in the formation and degradation of α-synuclein aggregates. Neuropathology 27:494–506.
  • Wang, A., S. Costello, M. Cockburn, X. Zhang, J. Bronstein, and B. Ritz. 2011. Parkinson’s disease risk from ambient exposure to pesticides. Eur. J. Epidemiol. 26:547–55. doi:10.1007/s10654-011-9574-5.
  • Warner, T. T., and A. H. Schapira. 2003. Genetic and environmental factors in the cause of Parkinson’s disease. Ann. Neurol. 53:16–25. doi:10.1002/ana.10487.
  • Weed, D. L. 2005. Weight of evidence: A review of concept and methods. Risk Anal. 25:1545–57. doi:10.1111/j.1539-6924.2005.00699.x.
  • Wenning, G. K., I. Litvan, and E. Tolosa. 2011. Milestones in atypical and secondary Parkinsonisms. Mov. Disord. 26:1083–95. doi:10.1002/mds.23713.
  • Zhang, X. F., M. Thompson, and Y. H. Xu. 2016. Multifactorial theory applied to the neurotoxicity of paraquat and paraquat-induced mechanisms of developing Parkinson’s disease. Lab. Invest. 96:496–507. doi:10.1038/labinvest.2015.161.

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