Abstract
Urinary metabolites of organophosphate (OP) and pyrethroid (PYR) pesticides and biomarkers of effects were studied in a population (n=40) residing in an important agricultural area of the province of Córdoba (Argentina). Detection frequencies (DF) higher than 85% were observed for the metabolites of pirimiphos (2-diethylamino-6-methylpyrimidin-4-ol –DEAMPY-, median 7.5 μg/g creatinine, DF: 100%), parathion (p-nitrophenol, 0.99 μg/g creatinine, 100%), and chlorpyrifos (3,5,6-trichloro-2-pyridinol, 0.25 μg/g creatinine, 85%). The DEAMPY concentrations doubled the levels found in other studies and were negatively associated with Er-AChE activity, suggesting the appearance of health effects already in environmental exposure levels below established acceptable daily intakes (ADIs). 3-Phenoxybenzoic acid, the metabolite of several PYR pesticides, was also found in all samples. This metabolite was also significantly negatively correlated with Er-AChE, indicating effects of pyrethroid pesticides on the acetylcholine system even at concentrations below the ADI.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abu-Qare AW, Abou-Donia MB (2000) Urinary excretion of metabolites following a single dermal dose of [14C]methyl parathion in pregnant rats. Toxicology 150(1-3):119–127. https://doi.org/10.1016/S0300-483X(00)00250-X
Arcury TA, Grzywacz JG, Isom S, Whalley LE, Vallejos QM, Chen H, Galván L, Barr DB, Quandt SA (2009) Seasonal variation in the measurement of urinary pesticide. Int J Occup Environ Health 15(4):339–350. https://doi.org/10.1179/oeh.2009.15.4.339
Barr DB (2008) Biomonitoring of exposure to pesticides. J Chem Health Saf 15(6):20–19. https://doi.org/10.1016/j.jchas.2008.07.001
Barr DB, Barr JR, Maggio VL, Whitehead RD, Sadowski MA, Whyatt M, Needham LL (2002) A multi-analyte method for the quantification of contemporary pesticides in human serum and plasma using high-resolution mass spectrometry. J Chromatogr B778:99–111. https://doi.org/10.1016/s0378-4347(01)00444-3
Becaria Coquet J, Caballero VR, Camisasso MC, González MF, Niclis C, Román MD, Muñoz SE, Leone CM, Procino F, Osella AR, Aballay LR (2020) Diet quality, obesity and breast cancer risk: an epidemiologic study in Córdoba, Argentina. Nutr Cancer 72:1026–1035. https://doi.org/10.1080/01635581.2019.1664601
Bjørling-Poulsen M, Andersen HR, Grandjean P (2008) Potential developmental neurotoxicity of pesticides used in Europe. Environ Health 22:7–50. https://doi.org/10.1186/1476-069X-7-50
Bolognesi C (2003) Genotoxicity of pesticides: a review of human biomonitoring studies. Mutat Res 543:251–272. https://doi.org/10.1016/s1383-5742(03)00015-2
Bolognesi C, Parrini M, Bonassi S, Ianello G, Salanitto A (1993) Cytogenetic analysis of a human population occupationally exposed to pesticides. Mutat Res 285:239–249. https://doi.org/10.1016/0027-5107(93)90112-S
Braeckman RA, Audenaert F, Willems JL, Belpaire FM, Bogaert MG (1983) Toxicokinetics of methyl parathion and parathion in the dog after intravenous and oral administration. Arch Toxicol 54:71–82. https://doi.org/10.1007/BF00277817
Bravo N, Grimalt JO, Bocca B, Pino A, Bin M, Brumatti LV, Rosolen V, Barbone F, Ronfani L, Alimonti A, Calamandrei G (2019) Urinary metabolites of organophosphate and pyrethroid pesticides in children from an Italian cohort (PHIME, Trieste). Environ Res 176:108508. https://doi.org/10.1016/j.envres.2019.05.039
Bravo N, Grimalt JO, Mazej D, Tratnik JS, Sarigiannis DA, Horvat M (2020a) Mother/child organophosphate and pyrethroid distributions. Environ Int 134:105264. https://doi.org/10.1016/j.envint.2019.105264
Bravo N, Peralta S, Grimalt JO, Martínez MA, Rovira J, Schuhmacher M (2020b) Organophosphate metabolite concentrations in maternal urine during pregnancy. Environ Res 176:1–6. https://doi.org/10.1016/j.envres.2019.109003
Butinof M, Fernández RA, Lerda D, Lantieri MJ, Filippi I, Díaz MP (2019) Biomonitoreo en exposición a plaguicidas y su aporte en vigilancia epidemiológica en agroaplicadores en Córdoba, Argentina. Gac Sanit 33(3):216–221. https://doi.org/10.1016/j.gaceta.2017.12.002
CASAFE (Cámara de Sanidad Agropecuaria y Fertilizantes) (2016) Datos del Mercado Argentino de Fitosanitario.https://www.casafe.org/pdf/2018/ESTADISTICAS/Informe-Mercado-Fitosanitarios-2016.pdf. Accessed 10 February 2020 .
Davis MD, Wade EL, Restrepo PR, Roman-Esteva W, Bravo R, Kuklenyik P, Calafat AM (2013) Semi-automated solid phase extraction method for the mass spectrometric quantification of 12 specific metabolites of organophosphorus pesticides, synthetic pyrethroids, and select herbicides in human urine. J Chromatogr B929:18–26. https://doi.org/10.1016/j.jchromb.2013.04.005
Dewailly E, Forde M, Robertson L, Kaddar N, Laouan Sidi EA, Côté S, Gaudreau E, Drescher O, Ayotte P (2014) Evaluation of pyrethroid exposures in pregnant women from 10 Caribbean countries. Environ Int 63:201–206. https://doi.org/10.1016/j.envint.2013.11.014
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Fukuto TR (1990) Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254. https://doi.org/10.1289/ehp.9087245
Garí M, González-Quinteiro Y, Bravo N, Grimalt JO (2018) Analysis of metabolites of organophosphate and pyrethroid pesticides in human urine from urban and agricultural populations (Catalonia and Galicia). Sci Total Environ 622–623:526–533. https://doi.org/10.1016/j.scitotenv.2017.11.355
Gentile N, Mañas F, Bosch B, Peralta L, Gorla N, Aiassa D (2012) Micronucleus assay as a biomarker of genotoxicity in the occupational exposure to agrochemicals in rural workers. Bull Environ Contam Toxicol 88:816–822. https://doi.org/10.1007/s00128-012-0589-8
Hancock DB, Martin ER, Mayhew GM, Stajich JM, Jewett R, Stacy MA, Scott BL, Vance JM, Scott WK (2008) Pesticide exposure and risk of Parkinson's disease: a family-based case-control study. BMC Neurol 8:1–12. https://doi.org/10.1186/1471-2377-8-6
Heffernan AL, English K, Toms LML, Calafat AM, Valentin-Blasini L, Hobson P, Broomhall S, Ware RS, Jagals P, Sly PD, Mueller JF (2016) Cross-sectional biomonitoring study of pesticide exposures in Queensland, Australia, using pooled urine samples. Environ Sci Pollut Res 23:23436–23448. https://doi.org/10.1007/s11356-016-7571-7
Hernández AF, Parrón T, Tsatsakis AM, Requena M, Alarcón R, López-Guarnido O (2013) Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicol. 307:136–145. https://doi.org/10.1016/j.tox.2012.06.009
Heudorf U, Angerer J (2001) Metabolites of Pyrethroid Insecticides in urine specimens: current exposure in an urban population in Germany. Environ Health Perspect 109(3):213–217. https://doi.org/10.1289/ehp.01109213
INTA (Instituto de Tecnología Agropecuaria/Secreataría de Agricultura, Ganadería y Pesca (2009) Estudios socio-economicos de la sustentabilidad de los sistemas de producción y recursos naturales. Zonas Agroeconómicas Homogéneas Córdoba. https://inta.gob.ar/sites/default/files/script-tmp-inta-zonas_agroeconmicas_09cba.pdf. Accessed 24 March 2020.
Joint Meeting on Pesticide Residues (JMPR) FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) (2006) http://www.fao.org/agriculture/crops/thematic-sitemap/theme/pests/lpe/en/. Accessed 20 February 2020
Joint Meeting on Pesticide Residues (JMPR) FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) (2020) http://www.fao.org/agriculture/crops/thematic-sitemap/theme/pests/lpe/en/. Accessed 15 February 2020
Jokanović M (2018) Neurotoxic effects of organophosphorus pesticides and possible association with neurodegenerative diseases in man: a review. Toxicology. 1(410):125–131. https://doi.org/10.1016/j.tox.2018.09.009
Katsikantami I, Colosio C, Alegakis A, Tzatzarakis MN, Vakonaki E, Rizos AK, Sarigiannis DA, Tsatsakis AM (2019) Estimation of daily intake and risk assessment of organophosphorus pesticides based on biomonitoring data – the internal exposure approach. Food Chem Toxicol 123:57–71. https://doi.org/10.1016/j.fct.2018.10.047
Koch HM, Hardt J, Angerer J (2001) Biological monitoring of exposure of the general population to the organophosphorus pesticides chlorpyrifos and chlorpyrifos-methyl by determination of their specific metabolite 3,5,6-trichloro-2-pyridinol. Int J Hyg Environ Health 204:175–180. https://doi.org/10.1078/1438-4639-00082
Koureas M, Tsakalof A, Tsatsakis A, Hadjichristodoulou C (2012) Systematic review of biomonitoring studies to determine the association between exposure to organophosphorus and pyrethroid insecticides and human health outcomes. Toxicol Lett 210:155–168. https://doi.org/10.1016/j.toxlet.2011.10.007
Lantieri MJ, Butinof M, Fernández RA, Stimolo MI, Blanco M, Díaz MP (2011) Work practices, exposure assessment and geographical analysis of pesticide applicators in Argentina. In: Stoytcheva M (ed) Pesticides in the modern world - effects of pesticides exposure. Croatia, pp 115–138. https://www.intechopen.com/books/pesticides-in-the-modern-world-effects-of-pesticides-exposure/work-practices-exposure-assessment-and-geographical-analysis-of-pesticide-applicators-in-argentina
Le Grand R, Dulaurent S, Gaulier JM, Saint-Marcoux F, Moesch C, Lachâtre G (2011) Simultaneous determination of five synthetic pyrethroid metabolites in urine by liquid chromatography–tandem mass spectrometry: application to 39 persons without known exposure to pyrethroids. Toxicol Lett 210(2):248–253. https://doi.org/10.1016/j.toxlet.2011.08.016
Leng G, Leng A, Kuhn K-H, Lewalter J (1997) Human dose-excretion studies with the pyrethroid insecticide cyfluthrin : urinary metabolite profile following inhalation. Xenobiotica 27:1273–1283
Lewis RC, Cantonwine DE, Del Toro LV, Calafat AM, Valentin-Blasini L, Davis MD, Montesano MA, Alshawabkeh AN, Cordero JF, Meeker JD (2015) Distribution and determinants of urinary biomarkers of exposure to organophosphate insecticides in Puerto Rican pregnant women. Sci Total Environ 512-513:337–344. https://doi.org/10.1016/j.scitotenv.2015.01.059
MAGyP (Ministerio de Agricultura, Ganadería y Pesca) (2018) Estimaciones Agrícolas. Argentina: http://datosestimaciones.magyp.gob.ar/reportes.php?reporte=Estimaciones. Accessed 24 January 2020
Manthripragada AD, Costello S, Cockburn MG, Bronstein JM, Ritz B (2010) Paraoxonase 1 (PON1), agricultural organophosphate exposure, and Parkinson disease. Epidemiology 21(1):87–94. https://doi.org/10.1097/EDE.0b013e3181c15ec6
McKinlay R, Plant JA, BellJNB VN (2008) Endocrine disrupting pesticides: Implications for risk assessment. Environ Int 34:168–183. https://doi.org/10.1016/j.envint.2007.07.013
Moltoni L (2012) Evolución del mercado de herbicidas en Argentina. http://inta.gob.ar/documentos/economia-y-desarrollo-agroindustrial-boletin-1-2-evolucion-del-mercado-en-argentina. Accessed 13 January 2020
Morgan MK (2015) Predictors of urinary levels of 2,4-dichlorophenoxyacetic acid, 3,5,6-trichloro-2-pyridinol, 3-phenoxybenzoic acid, and pentachlorophenol in 121 adults in Ohio. Int J Hyg Environ Health 218:479–488. https://doi.org/10.1016/j.ijheh.2015.03.015
Morgan DP, Hetzler HL, Slach EF, Lin LI (1977) Urinary excretion of paranitrophenol and alkyl phosphates following ingestion of methyl or ethyl parathion by human subjects. Arch Environ Contam Toxicol 6:159–173
Olsson AO, Nguyen JV, Sadowski MA, Barr DB (2003) A liquid chromatography/electrospray ionization–tandem mass spectrometry method for quantification of specific organophosphorus pesticide biomarkers in human urine. Anal Bioanal Chem 376:808–815. https://doi.org/10.1007/s00216-003-1978-y
Panuwet P, Prapamontol T, Chantara S, Thavornyuthikarn P, Montesano MA, Whitehead RD, Barr DB (2008) Concentrations of urinary pesticide metabolites in small-scale farmers in Chiang Mai Province, Thailand. Sci Total Environ 407:655–668. https://doi.org/10.1016/j.scitotenv.2008.08.044
Payne-Sturges D, Cohen J, Castorina R, Axelrad DA, Woodruff TJ (2009) Evaluating Cumulative Organophosphorus Pesticide Body Burden of Children: A National Case Study. Environ Sci Technol 43:7924–7930
Perry MJ, Venners SA, Barr DB, Xub X (2007) Environmental pyrethroid and organophosphorus insecticide exposures and sperm concentration. Reprod Toxicol 23:113–118. https://doi.org/10.1016/j.reprotox.2006.08.005
Phung DT, Connell D, Miller G, Hodge M, Patel R, Cheng R, Abeyewardene M, Chu C (2012) Biological monitoring of chlorpyrifos exposure to rice farmers in Vietnam. Chemosphere 87:294–300. https://doi.org/10.1016/j.chemosphere.2011.11.075
Ratelle M, Coté J, Bouchard M (2015) Time profiles and toxicokinetic parameters of key biomarkers of exposure to cypermethrin in orally exposed volunteers compared with previously available kinetic data following permethrin exposure. J Appl Toxicol 35:1586–1593
Raymer JH, Studabaker WB, Gardner M, Talton J, Quandt SA (2014) Pesticide exposures to migrant farmworkers in Eastern NC: detection of metabolites in farmworker urine associated with housing violations and camp characteristics. Am J Ind Med 57:323–337. https://doi.org/10.1002/ajim.22284
Rohlman DS, Anger WK, Lein PJ (2011) Correlating neurobehavioral performance with biomarkers of organophosphorus pesticides exposure. Neurotoxicol. 32(2):268–276. https://doi.org/10.1016/j.neuro.2010.12.008
Sams C, Jones K (2012) Biological monitoring for exposure to deltametrhin: A human oral dosing study and background levels in the UK general population. Toxicol Lett 213:35–38. https://doi.org/10.1016/j.toxlet.2011.04.014
Saoudi A, Fréry N, Zeghnoun A, Bidondo ML, Deschamps V, Göen T, Garnier R, Guldner L (2014) Serum levels of organochlorine pesticides in the French adult population: the French National Nutrition and Health Study (ENNS), 2006–2007. Sci Total Environ 472:1089–1099. https://doi.org/10.1016/j.scitotenv.2013.11.044
Schettgen T, Alt A, Esser A, Kraus T (2015) Current data on the background burden to the persistent organochlorine pollutants HCB, p,p'-DDE as well as PCB 138, PCB 153 and PCB 180 in plasma of the general population in Germany. Int J Hyg Environ Health 218(4):380–385. https://doi.org/10.1016/j.ijheh.2015.02.006
Trunnelle KJ, Bennett DH, Tulve NS, Clifton MS, Davis MD, Calafat AM, Moran R, Tancredi DJ, Hertz-Picciotto I (2014) Urinary pyrethroid and chlorpyrifos metabolite concentrations in Northern California families and their relationship to indoor residential insecticide levels, part of the study of use of products and exposure related behavior (SUPERB). Environ Sci Technol 48(3):1931–1939. https://doi.org/10.1021/es403661a
Wang L, Liu Z, Zhang J, Wu Y, Sun H (2016) Chlorpyrifos exposure in farmers and urban adults: Metabolic characteristic, exposure estimation, and potential effect of oxidative damage. Environ Res 149:164–170. https://doi.org/10.1016/j.envres.2016.05.011
Woollen BH, Marsh JR, Laird WJD, Lesser JE (1992) The metabolism of cypermethrin in man: differences in urinary metabolite profiles following oral and dermal administration. Xenobiotica 22:983–991
Yusa V, Millet M, Coscolla C, Pardo O, Roca M (2015a) Occurrence of biomarkers of pesticide exposure in non-invasive human specimens. Chemosphere 139:91–108. https://doi.org/10.1016/j.chemosphere.2015.05.082
Yusa V, Millet M, Coscolla C, Roca M (2015b) Analytical methods for human biomonitoring of pesticides. A review. Anal Chim Acta 891:15–31. https://doi.org/10.1016/j.aca.2015.05.032
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Funding
This work was supported by grants from the Agencia Nacional de Promoción Científica y Técnica (FONCyT-PICT2015-1784), Secretaría de Ciencia y Técnica (SECyT, UNC, Res. 411/2018), and Project EDCMET (H2020-HEALTH/0490-825762) funded by the European Union. The present work is part of the PhD thesis of I. Filippi, who gratefully acknowledges a fellowship from CONICET.
Agencia Nacional de Promoción Científica y Tecnológica (Grant ref: FONCyT-PICT2015-1784). Principal investigator recipient: Dr. Maria V Amé
Agencia Nacional de Promoción Científica y Tecnológica (Grant ref: UNC, Rs. 411/2018). Principal investigator recipient: Dr. Maria V Amé
Horizon 2020 Framework Programme (Grant ref: H2020-HEALTH/0490-825762). Principal investigator recipient: Prof. Joan O. Grimalt
Author information
Authors and Affiliations
Contributions
Iohanna Filippi: Methodology, investigation, writing - original draft
Natalia Bravo: Methodology, data analysis, writing - original draft
Joan Grimalt: Methodology, data analysis, resources, writing - review and editing, funding acquisition
Mariana Butinof: Conceptualization and funding acquisition
Daniel Lerda: Conceptualization and methodology
Ricardo A. Fernández: Conceptualization and Methodology
Sonia E. Muñoz: Conceptualization, resources, and Supervision
María V. Amé: Conceptualization, resources, supervision, funding acquisition, writing - review and editing
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Written informed consent was obtained from the subjects who agreed to participate in the study. The proposal was approved by the Ethics Review Committee of Hospital Nacional de Clínicas and is enrolled in the Ethics Committee of Health Investigations of the Córdoba Province (RePIS N°1582 and 044/10).
Consent for publication
Not applicable
Competing Interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 63 kb)
Rights and permissions
About this article
Cite this article
Filippi, I., Bravo, N., Grimalt, J.O. et al. Pilot study of exposure of the male population to organophosphate and pyrethroid pesticides in a region of high agricultural activity (Córdoba, Argentina). Environ Sci Pollut Res 28, 53908–53916 (2021). https://doi.org/10.1007/s11356-021-14397-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14397-1