Cellular and genetic damage as determinants of pesticide toxicity
Abstract
The use of pesticides in Colombia has allowed effective pest control, increasing agricultural, forestry and livestock productivity. However, both occupational and environmental exposure to pesticides can generate harmful effects on human health, since they can induce damage to genetic material, causing the development of diseases, including cancer. Although the harmful effects caused by exposure to pesticides are widely known, specific information about genomic damage (gene and chromosomal damage) generated by exposure to them is scarce or absent. This review aims to describe the cellular and genetic effects induced by exposure to pesticides, as well as their implications for disease development. Considering the wide use of pesticides in
the world, as well as their impacts on health, increasing our knowledge of their harmful effects will allow us to establish future possibilities for applying tests for the early detection of diseases, as well as developing programs and/or preventive actions aimed at protecting the most vulnerable individuals in occupational and environmental settings.
Keywords
Chromosomal Instability, Genotoxicity, Occupational exposure, Pesticides
References
- FinAgro, “ El momento del Agro | Finagro” , 2020. https://www.finagro.com.co/noticias/el-momento-del-agro (accedido may 08, 2020).
- C. Moncayo, “ DANE presenta las cifras reales del campo colombiano” , Instituto Nacional de Contadores Públicos de Colombia, dic. 02, 2016. https://www.incp.org.co/dane-presenta-las-cifras-reales-del-campo-colombiano/(accedido may 08, 2020).
- Dinero, “ El agro, uno de los posibles ganadores tras la crisis” , ¿Por qué el agro se podría impulsar tras la crisis?, 2020. http://www.dinero.com/pais/articulo/por-que-el-agro-se-podria-impulsar-tras-la-crisis/284301 (accedido may 08, 2020).
- E. Z. Violante, E. A. García, L. C. Ojinaga, y W. D. Heusser, “ Daño genético y exposición a plaguicidas en trabajadores agrícolas del Valle de San Quintín, Baja California, México” , p. 9.
- A. Arafa, M. Afify, y N. Samy, “ Evaluation of Adverse Health Effects of Pesticides Exposure [Biochemical & Hormonal] among Egyptian Farmers” , J. Appl. Sci. Res, vol. 9, n.o 7, pp. 4404-4409, 2013.
- S. M. Bréga et al., “ Clinical, cytogenetic and toxicological studies in rural workers exposed to pesticides in Botucatu, São Paulo, Brazil” , Cad. Saúde Pública, vol. 14, n.o suppl 3, pp. S117-S123, 1998, doi: 10.1590/S0102-311X1998000700011. DOI: https://doi.org/10.1590/S0102-311X1998000700011
- M. L. Castrejón Godínez, E. Sanchez Salinas, y L. Ortíz, “ PLAGUICIDAS: GENERALIDADES, USOS E IMPACTOS SOBRE EL AMBIENTE Y LA SALUD” , Prim. Ed., vol. 1, p. 30, 2014.
- R. Valencia Quintana et al., “ GENOTOXICIDAD DE PLAGUICIDAS EN SISTEMAS VEGETALES” , p. 26.
- K.Z. Guyton et al., “ Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate” , vol. 16. Lancet Oncol, pp. 490-491, 2015, [En línea]. Disponible en: https:// doi.org/10.1016/S1470-2045(15)70134-8. DOI: https://doi.org/10.1016/S1470-2045(15)70134-8
- A. del P. Díaz Gómez, “ Informe De Evento Intoxicaciones Por Sustancias Químicas, Colombia” , Instituto Nacional de Salud, 2017.
- J. Graziano de Silva, Cód̤igo Internacional de Conducta para la Gestin̤ de Plaguicidas., vol. 1. Roma: Food & Agriculture Org, 2015.
- Instituto Colombiano Agropecuario, “ Plaguicidas Químicos” , ICA, 2020. https://www.ica.gov.co/areas/agricola/servicios/regulacion-y-control-de-plaguicidas-quimicos.aspx (accedido may 08, 2020).
- E. Carod Benedico, “ Insecticidas organofosforados. "De la guerra química al riesgo” , Medifam, vol. 12, n.o 5, pp. 51-62, 2002. DOI: https://doi.org/10.4321/S1131-57682002000500005
- A. Ferrer, “ Intoxicación por plaguicidas” , An. Sist. Sanit. Navar., vol. 26, n.o 1, pp. 155-171, 2003, doi: 10.4321/S1137-66272003000200009. DOI: https://doi.org/10.4321/S1137-66272003000200009
- M. H. Badii y J. Landeros, “ Plaguicidas que afectan a la salud humana y la sustentabilidad” , CULCyT, vol. 19, n.o 4, pp. 21-34, 2007.
- G. Solís González, A. A. Cortés Téllez, Z. I. Téllez Pérez, y C. Bartolomé Camacho, “ Toxicidad aguda del herbicida N-(fosfonometil) glicina sobre representantes planctónicos Artemia franciscana y Microcystis aeruginosa” , Rev.Esp.Cienc.Quim.Biol, vol. 22, pp. 1-8, 2019, doi: DOI: 10.22201/fesz.23958723e.2019.0.192. DOI: https://doi.org/10.22201/fesz.23958723e.2019.0.192
- R. S. Benítez Leite, “ Plaguicidas Y Efectos Sobre La Salud Humana: Un Estado Del Arte” . 2012, [En línea]. Disponible en: http://www.serpajpy.org.py/wp-content/uploads/2014/03/Plaguicidas-y-efectos-sobre-la-salud-humana1.pdf.
- D. Benedetti et al., “ Genetic damage in soybean workers exposed to pesticides: Evaluation with the comet and buccal micronucleus cytome assays” , Mutat. Res. Toxicol. Environ. Mutagen., vol. 752, n.o 1-2, pp. 28-33, abr. 2013, doi: 10.1016/j.mrgentox.2013.01.001. DOI: https://doi.org/10.1016/j.mrgentox.2013.01.001
- H. Jacobsen-Pereira et al., “ Markers of genotoxicity and oxidative stress in farmers exposed to pesticides” , Ecotoxicol. Environ. Saf., vol. 148, pp. 177-183, feb. 2018, doi: 10.1016/j.ecoenv.2017.10.004. DOI: https://doi.org/10.1016/j.ecoenv.2017.10.004
- A. Sabarwal, R. Agarwal, y R. P. Singh, “ Fisetin inhibits cellular proliferation and induces mitochondria-dependent apoptosis in human gastric cancer cells.” , Mol. Carcinog., vol. 56, pp. 499–514., 2017. DOI: https://doi.org/10.1002/mc.22512
- A. Sabarwal, K. Kumara, y R. P. Singha, “ Hazardous effects of chemical pesticides on human health–Cancer and other associated disorders.” , Environmental Toxicology and Pharmacology, vol. 63, pp. 103-114, 2018. DOI: https://doi.org/10.1016/j.etap.2018.08.018
- I. Helali, S. Ferchichi, H. Harizi, M. Aouni, y A. Maaouia, “ Modulation of macrophage functionality induced in vitro by chlorpyrifos and carbendazim pesticides” , J. Immunotoxicol, vol. 5, pp. 745–750, 2016, doi: https://doi.org/10.1080/1547691X.2016. 1181124. DOI: https://doi.org/10.1080/1547691X.2016.1181124
- T. Ali, M. Ismail, F. Asad, A. Ashraf, U. Waheed, y Q. M. Khan, “ Pesticide genotoxicity in cotton picking women in Pakistan evaluated using comet assay” , Drug Chem. Toxicol., vol. 41, n.o 2, pp. 213-220, abr. 2018, doi: 10.1080/01480545.2017.1343342. DOI: https://doi.org/10.1080/01480545.2017.1343342
- M. Boussabbeh, I. Ben Salem, M. Hamdi, S. Ben Fradj, S. Abid-Essefi, y H. Bacha, “ Diazinon, an organophosphate pesticide, induces oxidative stress and genotoxicity in cells deriving from large intestine” , Environ. Sci. Pollut. Res., vol. 23, n.o 3, pp. 2882-2889, feb. 2016, doi: 10.1007/s11356-015-5519-y. DOI: https://doi.org/10.1007/s11356-015-5519-y
- S. Pastor, Csaba Siffel, M. Ricard, y P. Stylianos, “ Biomonitoring of four European populations occupationally exposed to pesticides: use of micronuclei as biomarkers” , Mutagenesis, vol. 18, n.o 3, pp. 249-258, 2003. DOI: https://doi.org/10.1093/mutage/18.3.249
- G. Martínez Luna, J. Castillo Cadena, J. H. Serment Guerrero, y P. R. Valencia Quintana, “ Efecto De La Exposición Laboral A Plaguicidas Sobre La Calidad Espermática, Daño Al Adn Y Su Asociación Con Los Polimorfismos De Gst” , Universidad Autonoma Del estado de México, Toluca, 2014.
- D. Alissa, F. Mañas, B. Bosch, N. Gentile, N. Bernardi, y N. Gorla, “ Biomarcadores De Daño Genético En Poblaciones Humanas Expuestas A Plaguicidas” , Acta Biol. Colomb., vol. 17, pp. 485-510, 2012.
- C. Martínez-Valenzuela, “ Riesgo Genotóxico Por Exposición A Plaguicidas En Trabajadores Agrícolas” , Rev. Int. Contam. Ambient., vol. 23, pp. 185-200, 2007.
- L. Díaz González y C. Alonso González, “ Consecuencias de la exposición materno-infantil a disruptores endocrinos: Impacto en el ámbito de los transtornos reproductivos” , Universidad de Cantabria, Santander, 2018.
- I. R. González Espinoza, C. Garza Villarreal, O. A. Juárez León, y E. Téllez Bernal, “ Cáncer de mama con receptores hormonales positivos: tratamiento adyuvante, primera línea en cáncer metastásico y nuevas estrategias (inhibición de mTOR)” , Gaceta Mexicana de Oncología, vol. 14, dic. 2015, doi: 10.1016/j.gamo.2015.11.001. DOI: https://doi.org/10.1016/j.gamo.2015.11.001
- M. Lema, “ RUTA PI3K / PTEN / AKT” . 2012, Accedido: may 18, 2020. [En línea]. Disponible en: http://mauriciolema.webhost4life.com/Moloncol2012/files/MolOncol04_PI3K_PTEN_AKT.pdf.
- M. Fernandez, D. Martín, y F. Rubiños, “ Clorofenoxiácidos.” , Plaguicidas, jun. 10, 2010. https://tplaguicidas.wordpress.com/clorofenoxiacidos/ (accedido may 11, 2020).
- K. Kvitko et al., “ Susceptibility to DNA damage in workers occupationally exposed to pesticides, to tannery chemicals and to coal dust during mining” , Genet. Mol. Biol., vol. 35, n.o 4 suppl 1, pp. 1060-1068, 2012, doi: 10.1590/S1415-47572012000600022. DOI: https://doi.org/10.1590/S1415-47572012000600022
- V. F. S. Kahl et al., “ Chronic occupational exposure endured by tobacco farmers from Brazil and association with DNA damage” , Mutagenesis, vol. 33, n.o 2, pp. 119-128, abr. 2018, doi: 10.1093/mutage/gex045. DOI: https://doi.org/10.1093/mutage/gex045
- S. Gangemi et al., “ Occupational exposure to pesticides as a possible risk factor for the de- velopment of chronic diseases in humans” , Mol. Med. Rep, vol. 14, pp. 4475–4488, 2016, doi: https://doi.org/10.3892/mmr.2016.5817. DOI: https://doi.org/10.3892/mmr.2016.5817
- A. F. Muñoz Aristizábal, “ Evaluación del daño en el ADN en dos poblaciones colombianas de agricultores y floricultores” , Rev. UDCA Actual. Divulg. Científica, vol. 12, n.o 1, pp. 7-16, feb. 2009, doi: 10.31910/rudca.v12.n1.2009.637. DOI: https://doi.org/10.31910/rudca.v12.n1.2009.637
- S. Koutros et al., “ Xenobiotic-metabolizing gene variants, pesticide use, and the risk of prostate cancer” , Pharmacogenet. Genomics, vol. 21, pp. 615–623, 2011, doi: https://doi.org/ 10.1097/FPC.0b013e3283493a57. DOI: https://doi.org/10.1097/FPC.0b013e3283493a57
- L. Hou, X. Zhang, D. Wang, y A. Baccarelli, “ Environmental chemical exposures and human epigenetics.” , Int. J. Epidemiol., vol. 41, pp. 79–105, 2012, doi: https://doi.org/10.1093/ ije/dyr154. DOI: https://doi.org/10.1093/ije/dyr154
- V. N. Rakitsky, V. A. Koblyakov, y V. S. Turusov, “ Nongenotoxic (epigenetic) carcinogens: pesticides as an example. A critical review. Teratog. Carcinog. Mutagen” , vol. 20, pp. 229-240, 2000. DOI: https://doi.org/10.1002/1520-6866(2000)20:4<229::AID-TCM5>3.0.CO;2-M
- J. George y Y. Shukla, “ Pesticides and cancer: insights into toxicoproteomic-based findings.” , J Proteomics, vol. 74, pp. 2713-2722, 2011. DOI: https://doi.org/10.1016/j.jprot.2011.09.024
- N. Sailaja et al., “ Genotoxic evaluation of workers employed in pesticide production” , Mutat. Res. Toxicol. Environ. Mutagen., vol. 609, n.o 1, pp. 74-80, oct. 2006, doi: 10.1016/j.mrgentox.2006.06.022. DOI: https://doi.org/10.1016/j.mrgentox.2006.06.022
- E. Vakonaki, D.A. Spandidos, A.M. Tsatsakis, V.P. Androutsopoulos, y J. Liesivuori, “ Pesticides and oncogenic modulation” , Toxicology, vol. 307, pp. 42–45, 2013, doi: https://doi. org/10.1016/j.tox.2013.01.008. DOI: https://doi.org/10.1016/j.tox.2013.01.008
- K. Kaur y R. Kaur, “ Occupational Pesticide Exposure, Impaired DNA Repair, and Diseases. Indian J Occup Environ .” , Indian J Occup Environ Med., vol. 22, pp. 74–81, may 2018, doi: doi: 10.4103/ijoem.IJOEM_45_18: 10.4103/ijoem.IJOEM_45_18 PMID: 30319227. DOI: https://doi.org/10.4103/ijoem.IJOEM_45_18
- J. S. Alves, F. R. da Silva, G. F. da Silva, y et al, “ Investigation of potential biomarkers for the early diagnosis of cellular stability after the exposure of agricultural workers to pesticides.” , An. Acad. Bras. Cienc., vol. 88, pp. 349-360, 2016. DOI: https://doi.org/10.1590/0001-3765201520150181
- C. M. Wilhelm, A. K. Calsing, y L. B. da Silva, “ Assessment of DNA damage in floriculturists in southern Brazil.” , Environ. Sci. Pollut. Res. Int., vol. 22, pp. 8182–8189., 2015. DOI: https://doi.org/10.1007/s11356-014-3959-4
- J. Castillo Cadena, L. E. Tenorio Vieyra, A. I. Quintana Carabia, M. M. CastiGarcía Fabila, E. Madrigal Bujaidar, y S. J. Ramirez, “ Determination of DNA damage in floriculturists exposed to mixtures of pesticides.” , J. Biomed. Biotechnol., 2006. DOI: https://doi.org/10.1155/JBB/2006/97896
- P. Grover., K. Danadevi, M. Mahboob, R. Rozati, B. Banu, y M. F. Rahman, “ Evaluation of genetic damage in workers employed in pesticide production utilizing the Comet assay.” , Mutagenesis, vol. 18, pp. 201-205, 2003. DOI: https://doi.org/10.1093/mutage/18.2.201
- M. E. Varona-Uribe et al., “ Exposure to pesticide mixtures and DNA damage among rice field workers” , Arch. Environ. Occup. Health, vol. 71, n.o 1, pp. 3-9, ene. 2016, doi: 10.1080/19338244.2014.910489. DOI: https://doi.org/10.1080/19338244.2014.910489
- C. Bolognesi, G. Carrasquilla, S. Volpi, K. R. Solomon, y E. J. P. Marshall, “ Biomonitoring of Genotoxic Risk in Agricultural Workers from Five Colombian Regions: Association to Occupational Exposure to Glyphosate” , J. Toxicol. Environ. Health A, vol. 72, n.o 15-16, pp. 986-997, ago. 2009, doi: 10.1080/15287390902929741. DOI: https://doi.org/10.1080/15287390902929741
- M. Varona, O. Cárdenas, C. Crane, S. Rocha, G. Cuervo, y J. Vargas, “ Alteraciones citogenéticas en trabajadoras con riesgo ocupacional de exposición a plaguicidas en cultivos de flores en Bogotá” , biomedica, vol. 23, pp. 41-52, 2003. DOI: https://doi.org/10.7705/biomedica.v23i2.1206
- S. M. Piperakis, K. Kontogianni, C. Siffel, y M.M. Piperakis, “ Measuring the Effects of Pesticides on Occupationally Exposed Humans with the Comet Assay” , Environmental Toxicology. pp. 355-359, 2006. DOI: https://doi.org/10.1002/tox.20191
- L. S. Hoyos, S. Carvajal, L. Solano, L. Orozco, y W. W. Au, “ Cytogenetic Monitoring of Farmers exposed to pesticides in Colombia.” , Environ. Health Perspect., vol. 104, p. 4, 1996. DOI: https://doi.org/10.2307/3432818
- H Cakir Karabas, I Ozcan, L Turker Sener, S Dolek Guler, I Albeniz, y TL Erdem}, “ Evaluation of Cell and DNA Damage Induced by Panoramic Radiography” , vol. 22, pp. 1-8, 2019.
- S. Weidner Maluf, D. Ferreira Passos, A. Bacelar, G. Speit, y B. Erdtmann, “ AssessmentofDNADamageinLymphocytesofWorkers ExposedtoX-radiationUsingtheMicronucleusTestand the CometAssay” , Environ. Mol. Mutagen., vol. 38, pp. 311-315, 2001. DOI: https://doi.org/10.1002/em.10029
- D. Benedetti et al., “ DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides.” , Mutagenesis, vol. 33, pp. 87-95, 2018. DOI: https://doi.org/10.1093/mutage/gex035
- C. Bolognesi, A. Creus., P. Ostrosky Wegman, y R. Marcos, “ Micronuclei and pesticide exposure.” , Mutagenesis, vol. 26, pp. 19–26, 2011. DOI: https://doi.org/10.1093/mutage/geq070
- N. D. Ghisi, E. C. De Oliveira, y A. J. Prioli, “ Does exposure to glyphosate lead to an in- crease in the micronuclei frequency A systematic and meta-analytic review.” , Chemosphere, vol. 145, pp. 42–54., 2016. DOI: https://doi.org/10.1016/j.chemosphere.2015.11.044
- Y. Carbajal López, S. Gómez Arroyo, R. Villalobos Pietrini, M. E. Calderón Segura, y A. Martínez Arroyo, “ Biomonitoring of agricultural workers exposed to pesticide mixtures in Guerrero state, Mexico, with comet assay and micronucleus test.” , Environ. Sci. Pollut. Res. Int., vol. 23, n.o 2513–2520., 2015. DOI: https://doi.org/10.1007/s11356-015-5474-7
- V. Garaj-Vrhovac y D. Zeljezic, “ Assessment of genome damage in a population of Croatian workers employed in pesticide production by chromosomal aberration analysis, micronucleus assay and Comet assay.” , J Appl Toxicol, vol. 22, pp. 249-255., 2002. DOI: https://doi.org/10.1002/jat.855
- S. Ergene, A. Celik, T. Cavas, y F. Kaya, “ Genotoxic biomonitoring study of population residing in pesticide contaminated regions in Goksu Delta: micronucleus, chromosomal aberrations and sister chromatid exchanges.” , Environ Int, vol. 33, pp. 877-885., 2007. DOI: https://doi.org/10.1016/j.envint.2007.04.003
- C. Costa et al., “ Micronucleus frequencies in lymphocytes and reticulocytes in a pesticide-exposed population in Portugal.” , J Toxicol Environ Health A, n.o 74, pp. 960-970, 2011. DOI: https://doi.org/10.1080/15287394.2011.582024
- L. M. de M. Adad, H. H. R. de Andrade, K. Kvitko, M. Lehmann, A. A. de C. M. Cavalcante, y R. R. Dihl, “ Occupational exposure of workers to pesticides: Toxicogenetics and susceptibility gene polymorphisms” , Genet. Mol. Biol., vol. 38, n.o 3, pp. 308-315, sep. 2015, doi: 10.1590/S1415-475738320140336. DOI: https://doi.org/10.1590/S1415-475738320140336
- A. Tayyaba, I. Muhummad, A. Farkhanda, A. Ashraf, U. Waheed, y Q. M. Khan, “ Pesticide genotoxicity in cotton picking women in Pakistan evaluated using comet assay” , Drug Chem. Toxicol., pp. 1-9, 2017.
- F. R. Da Silva, K. Kvitko, P. Rohr, M. B. Abreu, F. V. Thiesen, y J. Da Silva, “ Genotoxic assessment in tobacco farmers at different crop times.” , Sci. Total Environ., vol. 490, pp. 334–341., 2014. DOI: https://doi.org/10.1016/j.scitotenv.2014.05.018
- A. S. Gaikwad, P. Karunamoorthy, S. J. Kondhalkar, M. Ambikapathy, y R. Beerappa, “ Assessment of hematological, biochemical effects and genotoxicity among pesticide sprayers in grape garden” , J. Occup. Med. Toxicol., vol. 10, n.o 1, p. 11, dic. 2015, doi: 10.1186/s12995-015-0049-6. DOI: https://doi.org/10.1186/s12995-015-0049-6
- V. How, Z. Hashim, P. Ismail, S. Md Said, D. Omar, y S. Bahri Mohd Tamrin, “ Exploring Cancer Development in Adulthood: Cholinesterase Depression and Genotoxic Effect From Chronic Exposure to Organophosphate Pesticides Among Rural Farm Children” , J. Agromedicine, vol. 19, n.o 1, pp. 35-43, ene. 2014, doi: 10.1080/1059924X.2013.866917. DOI: https://doi.org/10.1080/1059924X.2013.866917
- T. Bernieri, M. F. Moraes, P. G. Ardenghi, y L. Basso da Silva, “ Assessment of DNA damage and cholinesterase activity in soybean farmers in southern Brazil: High versus low pesticide exposure” , J. Environ. Sci. Health Part B, vol. 55, n.o 4, pp. 355-360, 2019, doi: 10.1080/03601234.2019.1704608. DOI: https://doi.org/10.1080/03601234.2019.1704608
- H.-P. Hutter et al., “ Indicators of Genotoxicity in Farmers and Laborers of Ecological and Conventional Banana Plantations in Ecuador” , Int. J. Environ. Res. Public. Health, vol. 17, n.o 4, p. 1435, feb. 2020, doi: 10.3390/ijerph17041435. DOI: https://doi.org/10.3390/ijerph17041435
- V. Garaj Vrhovac y D. Zzeljezic, “ Evaluation of DNA damage in workers occupationally exposed to pesticides using single-cell gel electrophoresis (SCGE) assay Pesticide genotoxicity revealed by comet assay” , Mutation Research. Elsevier Science, pp. 279-285, 2000. DOI: https://doi.org/10.1016/S1383-5718(00)00092-9
- M. R. Chowdhury y S. Dubey, “ Role of Cytogenetics and Molecular Genetics in Human Health and Medicine” , en Animal Biotechnology, Elsevier, 2014, pp. 451-472. DOI: https://doi.org/10.1016/B978-0-12-416002-6.00024-9
- G. E. Bianco, E. Suarez, L. Cazon, T. B. de la Puente, M. R. B. Ahrendts, y J. C. De Luca, “ Prevalence of chromosomal aberrations in Argentinean agricultural workers” , Environ. Sci. Pollut. Res., vol. 24, n.o 26, pp. 21146-21152, sep. 2017, doi: 10.1007/s11356-017-9664-3. DOI: https://doi.org/10.1007/s11356-017-9664-3
- B.M. Qaqish, O. Al-Dalahmah, Y. Al-Motassem, A. Battah, y S.S. Ismail, “ Occupational exposure to pesticides and occurrence of the chromosomal translocation t(14;18) among farmers in Jordan” , Toxicol. Rep., vol. 3, pp. 225–229, 2015, doi: https://doi.org/10. 1016/j.toxrep.2016.01.002. DOI: https://doi.org/10.1016/j.toxrep.2016.01.002
- V. F. Garry et al., “ Chromosome rearrangements in fumigant appliers: possible relationship to non-Hodgkin’s lymphoma risk.” , Cancer Epidemiol Biomarkers Prev, vol. 1, pp. 287–291, 1992.
- Z. Figueroa y et al, “ Dialkyl Phosphate Urinary Metabolites and Chromosomal Abnormalities in Human Sperm.” , Environ Res, vol. 143, pp. 256–265., nov. 2015, doi: doi:10.1016/j.envres.2015.10.021. DOI: https://doi.org/10.1016/j.envres.2015.10.021
- L. S. Gold, M. Ward, M. Dosemeci, y A. J. De Roos, “ Systemic autoimmune disease mortality and occupational exposures.” , Arthritis Rheum., vol. 56, pp. 3189-3201., 2007. DOI: https://doi.org/10.1002/art.22880
- S. Cepeda, M. Forero-Castro, D. Cárdenas-Nieto, M. Martínez-Agüero, y M. Rondón-Lagos, “ Chromosomal Instability in Farmers Exposed to Pesticides: High Prevalence of Clonal and Non-Clonal Chromosomal Alterations” , Risk Manag. Healthc. Policy, vol. Volume 13, pp. 97-110, feb. 2020, doi: 10.2147/RMHP.S230953. DOI: https://doi.org/10.2147/RMHP.S230953
- M. Zalacain, L. Sierrasesúmaga, y A. Patiño, “ El ensayo de micronúcleos como medida de inestabilidad genética inducida por agentes genotóxicos” , An. Sist. Sanit. Navar., vol. 28, n.o 2, ago. 2005, doi: 10.4321/S1137-66272005000300007. DOI: https://doi.org/10.4321/S1137-66272005000300007
- B. Weinhold, “ Epigenetics: the science of change.” , Environ. Health. Perspect, vol. 114, pp. A160-167, 2006. DOI: https://doi.org/10.1289/ehp.114-a160
- C. J. Maslansky y G. M. Williams, “ Evidence for an epigenetic mode of action in organochlorine pesticide hepatocarcinogenicity: a lack of genotoxicity in rat, mouse, and hamster hepatocytes.” , J. Toxicol. Environ. Health, vol. 8, pp. 121-130., 1981. DOI: https://doi.org/10.1080/15287398109530056
- M. N. Skinner y M. D. Anway, “ Epigenetic transgenerational actions of vinclozolin on the development of disease and cancer.” , Crit. Rev. Oncog, vol. 13, pp. 75-82., 2007. DOI: https://doi.org/10.1615/CritRevOncog.v13.i1.30
- J. W. Lee et al., “ Cancer incidence among pesticide applicators exposed to chlorpyrifos in the Agricultural Health Study.” , J Natl Cancer Inst, vol. 96, pp. 1781-1789., 2004b. DOI: https://doi.org/10.1093/jnci/djh324
- C. Freire y S. Koifman, “ Pesticide exposure and Parkinson’s disease: Epidemiological evidence of association.” , Neurotoxicology., 2012. DOI: https://doi.org/10.1016/j.neuro.2012.05.011
- H. Doi et al., “ Motor neuron disorder simulating ALS induced by chronic inhalation of pyrethroid insecticides.” , Neurology, vol. 67, pp. 1894-1895, 2006. DOI: https://doi.org/10.1212/01.wnl.0000244489.65670.9f
- S. Xinqiang, Z. Yu, Y. Ningning, D. Erqin, W. Lei, y D. Hongtao, “ Molecular mechanism of celastrol in the treatment of systemic lupus erythematosus based on network pharmacology and molecular docking technology” , Life Sci., vol. 240, p. 117063, ene. 2020, doi: 10.1016/j.lfs.2019.117063. DOI: https://doi.org/10.1016/j.lfs.2019.117063
- H. Shojaei SaadI y M. Abdollahi, “ Is there a link between human infertilities and exposure to pesticides?” , Int J Pharmacol, vol. 8, pp. 708-710, 2012. DOI: https://doi.org/10.3923/ijp.2012.708.710
- B. A. Weldon et al., “ Urinary microRNAs as potential biomarkers of pesticide exposure.” , Toxicol. Appl. Pharmacol., pp. 19-25, 2016. DOI: https://doi.org/10.1016/j.taap.2016.01.018
- A. S. Hick, M. G. Paczkowski, A. B. Gadano, y M. A. Carballo, “ Biomarcadores de Genotoxicidad en Individuos Expuestos al Arsénico” , Lat. Am. J. Pharm., p. 9, 2007.
- G. V. Maele Fabry, V. Libotte, J. Willems, y D. Lison, “ Review and meta-analysis of risk estimates for prostate cancer in pesticide manufacturing workers.” , Cancer Causes Control, vol. 17, pp. 353-373, 2006. DOI: https://doi.org/10.1007/s10552-005-0443-y
- G. V. Maele Fabry, S. Duhayon, y D. Lison, “ A systematic review of myeloid leukemias and occupational pesticide exposure.” , Cancer Causes Control, vol. 18, pp. 457-478., 2007. DOI: https://doi.org/10.1007/s10552-007-0122-2
- G. V. Maele Fabry, S. Duhayon, C. Mertens, y D. Lison, “ Risk of leukaemia among pesticide manufacturing workers: a review and meta-analysis of cohort” , Environ Res, vol. 106, pp. 121-137., 2008. DOI: https://doi.org/10.1016/j.envres.2007.09.002
- W. J. Lee, D. P. Sandler, A. Blair, C. Samanic, A. J. Cross, y M. C. Alavanja, “ Pesticide use and colorectal cancer risk in the Agricultural Health Study.” , Int J Cancer, vol. 121, pp. 339-346., 2007. DOI: https://doi.org/10.1002/ijc.22635
- W. J. Lee et al., “ Cancer incidence among pesticide applicators exposed to alachlor in the Agricultural Health Study.” , Am J Epidemiol, vol. 159, pp. 373-380., 2004a. DOI: https://doi.org/10.1093/aje/kwh040
- M. Weselak, T. E. Arbuckle, y W. Foster, “ Pesticide exposures and developmental outcomes: the epidemiological evidence.” , J. Toxicol. Environ. Health. B. Crit. Rev, vol. 10, pp. 41-80., 2007. DOI: https://doi.org/10.1080/10937400601034571
- C. M. Rocheleau, P. A. Romitti, y L. K. Dennis, “ Pesticides and hypospadias: a meta- analysis.” J Pediatr Urol, 2009. DOI: https://doi.org/10.1016/j.jpurol.2008.08.006
- S. Kumar, “ Occupational exposure associated with reproductive dysfunction.” , J. Occup. Health., vol. 46, pp. 1-19., 2004. DOI: https://doi.org/10.1539/joh.46.1
- L. M. Frazier, “ Reproductive Disorders Associated with Pesticide Exposure.” , J. Agromedicine, vol. 12, pp. 27-37, 2007. DOI: https://doi.org/10.1300/J096v12n01_04
- L. Bonetta, “ Pesticide-Parkinson link explored.” , Nat. Med., vol. 8, p. 1050, 2002. DOI: https://doi.org/10.1038/nm1002-1050
- V. Maele Fabry, P. Hoet, F. Vilain, y D. Lison, “ Occupational exposure to pesticides and Parkinson’s disease: A systematic review and meta-analysis of cohort studies.” , Environ. Int., vol. 46, pp. 30-43, 2012. DOI: https://doi.org/10.1016/j.envint.2012.05.004
- J. R. Richardson et al., “ Elevated serum pesticide levels and risk of Parkinson disease.” , Arch. Neurol., vol. 66, pp. 870-875, 2009. DOI: https://doi.org/10.1001/archneurol.2009.89
- K. M. Hayden et al., “ Occupational exposure to pesticides increases the risk of incident AD: the Cache County study.” , 1524-1530., vol. 74, pp. 1524-1530., 2010. DOI: https://doi.org/10.1212/WNL.0b013e3181dd4423
- T. Parron, M. Requena, A. F. Hernandez, y R. Alarcon, “ Association between environmental exposure to pesticides and neurodegenerative diseases. Toxicol. Appl. Pharmacol. 256(3), 379-385” , Toxicol. Appl. Pharmacol., vol. 256, pp. 379-385, 2011. DOI: https://doi.org/10.1016/j.taap.2011.05.006
- V. McGuire et al., “ Occupational exposures and amyotrophic lateral sclerosis. A population-based case-control study.” , Am. J. Epidemiol, vol. 145, pp. 1076-1088., 1997. DOI: https://doi.org/10.1093/oxfordjournals.aje.a009070
- M. Freedman, “ Amyotrophic lateral sclerosis and occupational exposure to 2,4- dichlorophenoxyacetic acid. Occup.” , Environ. Med., vol. 58, pp. 609-610., 2001. DOI: https://doi.org/10.1136/oem.58.9.609a
- F. Bonvicini, N. Marcello, J. Mandrioli, V. Pietrini, y M. Vinceti, “ Exposure to pesticides and risk of amyotrophic lateral sclerosis: a population-based case-control study.” , Ann. Ist. Super. Sanita., vol. 46, pp. 284-287, 2010.
- K. A. Thayer, J. J. Heindel, J. R. Bucher, y M. A. Gallo, “ Role of Environmental Chemicals in Diabetes and Obesity: A National Toxicology Program Workshop Report.” , Environ. Health. Perspect., vol. 120, pp. 779-789., 2012. DOI: https://doi.org/10.1289/ehp.1104597
- A. N. Zamzila, I. Aminu, S. Niza, M. R. Razman, y M. A. Hadi, “ Chronic Organophosphate Pesticide Exposure and Coronary Artery disease: finding a bridge.” , IIUM Research, Invention and Innovation Exhibition (IRIIE)., 2011.
- A. F. Hernandez, T. Parron, y R. Alarcon, “ Pesticides and asthma. Curr. Opin. Allergy.” , Clin. Immunol., vol. 11, pp. 90-96., 2011. DOI: https://doi.org/10.1097/ACI.0b013e3283445939
- J. A. Hoppin et al., “ Pesticide use and chronic bronchitis among farmers in the Agricultural Health Study.” , Am. J. Ind. Med., vol. 50, pp. 969-979., 2007. DOI: https://doi.org/10.1002/ajim.20523
- G. S. Cooper, E. L. Treadwell, E. W. St Clair, G. S. Gilkeson, y M. A. Dooley, “ Occupational risk factors for the development of systemic lupus erythematosus.” , J. Rheumatol., vol. 31, pp. 1928-1933., 2004.
- C. G. Parks et al., “ Insecticide use and risk of rheumatoid arthritis and systemic lupus erythematosus in the Women’s Health Initiative Observational Study.” , Arthritis Care Res. (Hoboken), vol. 63, pp. 184-194, 2011. DOI: https://doi.org/10.1002/acr.20335
- C. V. Álvarez Gongalvez, F. E. Arellano, y A. L. Pérz Carrera, “ Técnicas De Estudio Para La Evaluación Del Daño Al Adn Y Su Aplicación En La Producción Animal” , SNS, vol. 7, pp. 1-17, 2015.
- F. Faust, F. Kassie, S. S. Knasmuller, R. H. Boedecker, M. Mann, y S. Mersch, “ The use of the alkaline comet assay with lymphocytes in human biomonitoring studies.” , Mutat. Res., pp. 209–229. DOI: https://doi.org/10.1016/j.mrrev.2003.09.007
- UTI, “ Genotoxicidad – UTI – Unidad de Toxicidad In Vitro” , 2016. https://sitios.ces.edu.co/uti/genotoxicidad/ (accedido may 07, 2020).
- “ Citogenética: Cariotipo de Alta Resolución” , Cibic Laboratorios, sep. 20, 2017. http://www.cibic.com.ar/laboratorios-bioquimicos/citogenetica-cariotipo-de-alta-resolucion/ (accedido feb. 07, 2020).
- Laboratorio de estudios Genéticos y Reproducción, “ Cariotipo – BioCegyr” , 2015. http://www.biocegyr.com.ar/cariotipo/ (accedido may 07, 2020).
- N. Pérez-Herrera, J. M. Ceballos-Quintal, y D. Pinto-Escalante, “ Prevalencia de intercambio de cromátides hermanas en una población libre de exposición a agentes clastogénicos.” , Rev. Bioméd., vol. 10, n.o 2, pp. 71-76, 1999.
- “ Hibridación Genómica Comparada (HGC)” , Laboratorio Médico Echavarría, dic. 14, 2017. https://www.labechavarria.com/hibridacion-genomica-comparada-hgc (accedido may 07, 2020).
- Genética Molecular de Colombia, “ Hibridación Genómica Comparativa” , 2020. https://www.geneticamolecular.com.co/2014-12-19-23-25-42/2015-01-15-03-29-42/hibridacion-genomica-comparativa.html (accedido may 07, 2020).
- C. Tejada, A. Herrera, and E. Ruiz, “Utilización de biosorbentes para la remoción de níquel y plomo en sistemas binarios,” Ciencia En Desarrollo, vol. 7, no. 1, pp. 31–36, 2016. DOI: https://doi.org/10.19053/01217488.4228
- J. M. Hernández Rivas, N. C. Gutiérrez Gutiérrez, M. B. González Sánchez, y J. L. García Hernández, “Técnicas de estudio cromosómico. Citogenética convencional, hibridación in situ fluorescente y sus variedades. Aplicaciones clínicas”, Med. - Programa Form. Médica Contin. Acreditado, vol. 8, n.o 82, pp. 4392-4397, ene. 2002, doi: 10.1016/S0304-5412(02)70820-2. DOI: https://doi.org/10.1016/S0304-5412(02)70820-2
- E. D. Green, “Hibridación fluorescente in situ (FISH) | NHGRI”, Genome.gov. https://www.genome.gov/es/genetics-glossary/Hibridacion-fluorescente-in-situ (accedido may 07, 2020).