Abstract
Toxicity refers to the potential of a substance such as a pesticide to cause damage to the structure or functions of an exposed organism. Pesticides can lead to harmful biological effects in exposed animals and their offspring over the medium and long term. They can affect the immunological, nervous, endocrine, and reproductive systems. DNA damage has also been linked to exposure to pesticides, and this damage can cause abortions, degenerative diseases, and cancer. The aim of this work was to establish whether women who are indirectly exposed to pesticides exhibit a compromised health status, including genotoxic effect. Women exposed indirectly to pesticides in Chimchanga and Colaisaca in the south of Ecuador underwent hematological and biochemical tests and micronucleus assay in buccal cells. The subjects were also genotyped for GSTM1, GSTT1, GSTP1, and PON1 polymorphisms, which can modify an individual’s capacity to metabolize pesticides and relation with damage of DNA. The study revealed hepatic toxicity in Colaisaca women (AST and ALT) and an increase in the rate of micronucleus (MN) in Colaisaca individuals. In addition, genetic polymorphisms in PON1 and GSTP1 showed effects of modulating the frequency of karyolytic cells, karyorrhectic cells, and condensed chromatin cells.
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References
Ahluwalia M, Kaur A (2018) Modulatory role of GSTT1 and GSTM1 in Punjabi agricultural workers exposed to pesticides. Environ Sci Pollut Res 25:1–6. https://doi.org/10.1007/s11356-018-1459-7
Alwang J, Larochelle C, Barrera V (2017) Farm decision making and gender: results from a randomized experiment in Ecuador. World Dev 92:117–129. https://doi.org/10.1016/j.worlddev.2016.11.015
Androutsopoulos VP, Hernandez AF, Liesivuori J, Tsatsakis AM (2013) A mechanistic overview of health associated effects of low levels of organochlorine and organophosphorous pesticides. Toxicology 307:89–94. https://doi.org/10.1016/j.tox.2012.09.011
Araoud M, Neffeti F, Douki W, Ben Hfaiedh H, Akrout M, Hassine M, Fadhel Najjar M, Kenani A (2012) Adverse effects of pesticides on biochemical and haematological parameters in Tunisian agricultural workers. Journal of Exposure Science and Environmental Epidemiology, 243–247. https://doi.org/10.1038/jes.2012.11
Bolognesi C (2003) Genotoxicity of pesticides: a review of human biomonitoring studies. 251–272. https://doi.org/10.1016/S1383-5742(03)00015-2
Bolognesi C, Creus A, Ostrosky- P, Marcos R (2011) Micronuclei and pesticide exposure. Mutagenesis 26(1):19–26. https://doi.org/10.1093/mutage/geq070
Cattani D, Cesconetto PA, Tavares MK, Parisotto EB, De Oliveira PA, Rieg CEH, Zamoner A (2017) Developmental exposure to glyphosate-based herbicide and depressive-like behavior in adult offspring: implication of glutamate excitotoxicity and oxidative stress. Toxicology 387:67–80. https://doi.org/10.1016/j.tox.2017.06.001
Costa C, Teixeira JP, Silva S, Roma-Torres J, Coelho P, Gaspar J, Mayan O (2006) Cytogenetic and molecular biomonitoring of a Portuguese population exposed to pesticides. Mutagenesis 21(5):343–350. https://doi.org/10.1093/mutage/gel039
de Adad LMM, De Andrade HHR, Kvitko K, Lehmann M, de Cavalcante AACM, Dihl RR (2015) Occupational exposure of workers to pesticides: toxicogenetics and susceptibility gene polymorphisms. Genet Mol Biol 38(3):308–315. https://doi.org/10.1590/S1415-475738320140336
Espitia-Pérez L, da Silva J, Brango H, Espitia-Pérez P, Pastor-Sierra K, Salcedo-Arteaga S, Henriques JAP (2018) Genetic damage in environmentally exposed populations to open-pit coal mining residues: analysis of buccal micronucleus cytome (BMN-cyt) assay and alkaline, Endo III and FPG high-throughput comet assay. Mutat Res Genet Toxicol Environ Mutagen 836(June 2017):24–35. https://doi.org/10.1016/j.mrgentox.2018.06.002
Fareed M, Pathak MK, Bihari V, Kamal R, Srivastava AK (2013) Adverse respiratory health and hematological alterations among agricultural workers occupationally exposed to organophosphate pesticides: a cross-sectional study in North India. North 8(7):1–11. https://doi.org/10.1371/journal.-pone.0069755
Gaikwad AS, Karunamoorthy P, Kondhalkar SJ, Ambikapathy M, Beerappa R (2015) Assessment of hematological, biochemical effects and genotoxicity among pesticide sprayers in grape garden. J Occup Med Toxicol 10(1):1–6. https://doi.org/10.1186/s12995-015-0049-6
García-García CR, Parrón T, Requena M, Alarcón R, Tsatsakis AM, Hernández AF (2016) Occupational pesticide exposure and adverse health effects at the clinical, hematological and biochemical level. Life Sci 145:274–283. https://doi.org/10.1016/j.lfs.2015.10.013
Ginsberg G, Neafsey P, Hattis D, Guyton KZ, Johns DO, Sonawane B (2009) Critical reviews genetic polymorphism in paraoxonase 1 ( PON1 ): population distribution of PON1 activity. J Toxicol Environ Health 12:473–507. https://doi.org/10.1080/10937400903158409
Ghosh R, Siddharth M, Kuman Kare P, Prakash Kalra O, Kumar Tripathi A (2018) Role of Organochlorine Pesticides in Chronic Kidney Diseases of Unknown Etiology. Chronic Kidney Disease - from Pathophysiology to Clinical Improvements. IntechOpen. https://doi.org/10.5772/intechopen.71196
Humbert R, Adler DA, Disteche CM, Hassett C, Omiecinski CJ, Furlong CE (1993) The molecular basis of the human serum paraoxonase activity polymorphism. Nat Genet 3(1):73–76. https://doi.org/10.1038/ng0193-73
International Agency for Cancer Research, (IARC). (2018). List of pesticides Classifications. Retrieved from https://monographs.iarc.fr/list-ofclassifications-volumes/. Accessed 3 Oct 2018
Kumar S, Kaushik G, Dar MA, Nimesh S, Villarreal-Chiu JF (2018) Microbial degradation of organophosphate pesticides: a review. Pedosphere 28(2):190–208. https://doi.org/10.1016/S1002-0160(18)60017-7
Li B, Sedlacek M, Manoharan I, Boopathy R, Duysen EG, Masson P, Lockridge O (2005) Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochem Pharmacol 70(11):1673–1684. https://doi.org/10.1016/j.bcp.2005.09.002
Liu Q, Wang Q, Xu C, Shao W, Zhang C, Liu H, Jiang Z, Gu A (2017) Organochloride pesticides impaired mitochondrial function in hepatocytes and aggravated disorders of fatty acid metabolism.Scientific Reports 7:46339. https://doi.org/10.1038/srep46339
Maqbool F, Mostafalou S, Bahadar H, Abdollahi M (2015) Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sci 145:265–273. https://doi.org/10.1016/j.lfs.2015.10.022
Martínez F, Santoli López M, Carballo M (2017) Assessment of the health status and risk of genotoxic and cytotoxic damage in Argentinian adolescents living near horticultural crops
Milatovic D, Gupta RC, Aschner M (2006) Anticholinesterase toxicity and oxidative stress. The Scientific World Journal. 6:295–310. https://doi.org/10.1100/tsw.2006.38
National heart lung and blood institute, (NHLBI) (2015) Blood tests. Retrieved from https://www.nhlbi.nih.gov/health-topics/blood-tests. Accessed 10 Oct 2018
National Institute of Statistics and Census, (INEC) (2013) Descriptive analysis of the environmental module - use of pesticides in agriculture
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health : the urgent need for a new concept in agriculture. Front. Public Health 4:1–8. https://doi.org/10.3389/fpubh.2016.00148
Payán-Rentería R, Garibay-Chávez G, Rangel-Ascencio R, Preciado-Martínez V, Muñoz-Islas L, Beltrán-Miranda C, De Celis R (2012) Effect of chronic pesticide exposure in farm workers of a Mexico community. Arch Environ Occup Health 67(1):22–30. https://doi.org/10.1080/19338244.2011.564230
Rojas-Garcia AE et al (2011) Symptoms in pesticide retailers. J Occup Environ Med 53(5):517–521. https://doi.org/10.1097/JOM.0b013e318215fbf2
Sailaja K, Surekha D, Rao DN, Rao DR, Vishnupriya S (2010) Association of the GSTP1 gene (Ile105Val) polymorphism with chronic myeloid leukemia. Asian Pac J Cancer Prev 11(2):461–464
Sandoval-Carrillo A, Aguilar-Duran M, Vázquez-Alaniz F, Castellanos-Juárez FX, Barraza-Salas M, Sierra-Campos E, La Llave-León O (2013) Genes are associated with increased risk of preeclampsia in the Mexican mestizo population. Genet Mol Res 13:2160–2165
Scheer N, Wilson I (2016) A comparison between genetically humanized and chimeric liver humanized mouse models for studies in drug metabolism and toxicity. Drug Discov Today 21:250–263. https://doi.org/10.1016/j.drudis.2015.09.002
Silva VF, Rabaioli F, Alves S, Flesch G, Picinini J, Singh V, Simon D (2018) Ecotoxicology and environmental safety modulation of DNA damage in workers occupationally exposed to pesticides. Ecotoxicol Environ Saf 159(March):164–171. https://doi.org/10.1016/j.ecoenv.2018.04.052
Singh S, Kumar V, Thakur S, Dev B (2010) DNA damage and cholinesterase activity in occupational. Environ Toxicol Pharmacol 31(2):278–285. https://doi.org/10.1016/j.etap.2010.11.005
Skinner MK, Manikkam M, Tracey R, Guerrero-bosagna C, Haque M, & Nilsson EE (2013) Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity
Taylor P, Freire C, Koifman RJ, Koifman S (2015) Journal of toxicology and environmental health , part a : current issues hematological and hepatic alterations in Brazilian population heavily exposed to organochlorine pesticides. J Toxicol Environ Health 78(April):37–41. https://doi.org/10.1080/15287394.2014.999396
Thomas P, Holland N, Bolognesi C, Kirsch-Volders M, Bonassi S, Zeiger E, Fenech M (2009) Buccal micronucleus cytome assay. Nat Protoc 4(6):825–837. https://doi.org/10.1038/nprot.2009.53
Thomas P, Holland N, Bolognesi C, Kirsch-volders M, Bonassi S, Zeiger E et al (2011) Buccal micronucleus cytome assay, (October). https://doi.org/10.1038/nprot.2009.53
World Health Organization, (WHO) (2017) Health topics: Pesticides. Retrieved from http://www.who.int/topics/pesticides/en
Xotlanihua-Gervacio M d C, Guerrero-Flores MC, Herrera-Moreno JF, Medina-Díaz IM, Bernal-Hernández YY, Barrón-Vivanco BS, Rojas-garcía AE (2018) Micronucleus frequency is correlated with antioxidant enzyme levels in workers occupationally exposed to pesticides. Environ Sci Pollut Res 25:31558–31568
Yuantari, M., Van Gestel, C., Van Straalen, N., Widianarko, B., Sunoko, H., & Shobib, M. (2015). Knowledge, attitude, and practice of Indonesian farmers regarding the use of personal protective equipment against pesticide exposure, 187. https://doi.org/10.1007/s10661-015-4371-3
Zaragoza B, A, Valladares Carranza B, Ortega Santana C, Zamora Espinosa J, Velázquez Ordoñez V, Aparicio Burgos J, Zaragoza Bastida A et al (2016) No Title 6(1):43–55
Acknowledgments
We acknowledge the technical support of Gabriela González and Patricio Espinosa. The authors express their gratitude to all of the individuals who volunteered to participate in this study. This study was only possible with the help of the “Organización Cantonal de Mujeres Emprendedoras Campesinas y Urbanas de Calvas- OCMECUC.” We also especially thank Emilio Aguilar and Julio Ajila, Emperatriz Sarango, Gabriel Chamba, José Espinosa, Blanca Cueva, Enrique Sarango, Zoila Guamán, and Marisol Jima.
Funding
This work was financially supported by UTPL (no. PROY_CCSAL_1334).
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Arévalo-Jaramillo, P., Idrobo, A., Salcedo, L. et al. Biochemical and genotoxic effects in women exposed to pesticides in Southern Ecuador. Environ Sci Pollut Res 26, 24911–24921 (2019). https://doi.org/10.1007/s11356-019-05725-7
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DOI: https://doi.org/10.1007/s11356-019-05725-7