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Blood Pharmacokinetic of 17 Common Pesticides in Mixture Following a Single Oral Exposure in Rats: Implications for Human Biomonitoring and Exposure Assessment

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Blood Pharmacokinetic of 17 Common Pesticides in Mixture Following a Single Oral Exposure in Rats: Implications for Human Biomonitoring and Exposure Assessment Archives of Toxicology (2019) 93:2849–2862 https://doi.org/10.1007/s00204-019-02546-y TOXICOGENOMICS Blood pharmacokinetic of 17 common pesticides in mixture following a single oral exposure in rats: implications for human biomonitoring and exposure assessment Caroline Chata1,2 · Paul Palazzi1 · Nathalie Grova1 · Serge Haan3 · Claude Emond1,4 · Michel Vaillant5 · Brice M. R. Appenzeller1 Received: 3 May 2019 / Accepted: 14 August 2019 / Published online: 19 August 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Human biomonitoring provides information about chemicals measured in biological matrices, but their interpretation remains uncertain because of pharmacokinetic (PK) interactions. This study examined the PKs in blood from Long–Evans rats after a single oral dose of 0.4 mg/kg bw of each pesticide via a mixture of the 17 pesticides most frequently measured in humans. These pesticides are β-endosulfan; β-hexachlorocyclohexane [β-HCH]; γ-hexachlorocyclohexane [γ-HCH]; carbofuran; chlorpyrifos; cyhalothrin; cypermethrin; diazinon; dieldrin; difufenican; fpronil; oxadiazon; pentachlorophenol [PCP]; permethrin; 1,1-dichloro-2,2bis(4-chlorophenyl)ethylene [p,p′-DDE]; 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane [p,p′- DDT]; and trifuralin. We collected blood at 10 min to 48-h timepoints in addition to one sample before gavage (for a control). We used GS–MS/MS to measure the pesticide (parents and major metabolites) concentrations in plasma, determined the PK parameters from 20 sampling timepoints, and analyzed the food, litter, and cardboard in the rats’ environment for pesticides. We detected many parents and metabolites pesticides in plasma control (e.g., diethyl phosphate [DEP]; PCP; 3-phenoxyben- zoic acid [3-PBA]; 3,5,6-trichloro-2-pyridinol [TCPy], suggesting pre-exposure contamination. The PK values post-exposure showed that the AUC0−∞ and Cmax were highest for TCPy and PCP; β-endosulfan, permethrin, and trifuralin presented the lowest values. Terminal T1/2 and MRT for γ-HCH and β-HCH ranged from 74.5 h to 117.1 h; carbofuran phenol presented the shortest values with 4.3 h and 4.8 h. These results present the frst PK values obtained through a realistic pattern applied to a mixture of 17 pesticides to assess exposure. This study also highlights the issues of background exposure and the need to work with a relevant mixture found in human matrices. Keywords Background exposure · Mixture · Pesticides · Pharmacokinetic · Rat Abbreviations ATSDR Agency for Toxic Substances and Disease 3-PBA 3-Phenoxybenzoic acid Registry ADME Absorption, distribution, metabolism, and AUC0−∞ Area under the curve excretion Cmax Maximum concentration in plasma Cl2CA Cis-/trans-3-(2,2-dichlorovinyl)-2,2-di- methylcyclopropane carboxylic acid Electronic supplementary material The online version of this ClCF3CA 3-(2-Chloro-3,3,3-trifuoro-1-propenyl)- article (https ://doi.org/10.1007/s0020 4-019-02546 -y) contains 2,2-dimethylcyclopropanecarboxylic acid supplementary material, which is available to authorized users. * Claude Emond 3 Life Sciences Research Unit, University of Luxembourg, 6 [email protected] Avenue du Swing, Belvaux, Luxembourg 4 PhysioKinetic Simulations to Human Inc. (PKSH Inc), 1 Human Biomonitoring Research Unit, Luxembourg Institute Mascouche, QC J7K 0M6, Canada of Health (LIH), Rue Henri Koch 29, 4354 Esch-sur-Alzette, Luxembourg 5 Competence Center for Methodology and Statistics, Luxembourg Institute of Health (LIH), Rue Thomas Edison 2 Faculty of Science, Technology and Communication, 1A-B, 1445 Luxembourg, Luxembourg University of Luxembourg, 2 Avenue de l’Université, 4365 Esch-sur-Alzette, Luxembourg Vol.:(0123456789)1 3 2850 Archives of Toxicology (2019) 93:2849–2862 DEP Diethyl phosphate in Europe from 2010 through 2014 (EFSA 2017). The DETP Diethyl thiophosphate European Food Safety Authority (EFSA) analyzed more ED30 Efective dose than 78,000 samples from 750 diferent food products and EDTA Ethylenediaminetetraacetic acid detected 800 diferent pesticides in them (EFSA 2017). EFSA European Food Safety Authority Human exposure to pesticides can occur through dif- FNR Luxembourg National Research Fund ferent pathways (e.g., ingestion of food, water, or dust; (Fonds National de la Recherche) inhalation of particles, vapors, or gases; through dermal GC Gas chromatography contact). Nevertheless, ingestion is the major route of GC–MS/MS Gas chromatography with tandem mass exposure for the general population (Curl et al. 2015; Shel- spectrometry don and Berry 1999). Researchers have discussed the pos- HCH Hexachlorocyclohexane (gamma [γ], beta sible association between exposures to pesticides and other [β]) environmental contaminants and the development of meta- LD50 Lethal dose 50% bolic disorders, diferent types of cancer, or several human MRT Mean residence time diseases, including Parkinson’s disease (Bastias-Candia PAH Polycyclic aromatic hydrocarbon et al. 2019; Hernandez et al. 2013; Jaga and Dharmani PCP Pentachlorophenol 2005; Lebov et al. 2015; Saeed et al. 2017; Storm et al. PK Pharmacokinetics 2000; van der Mark et al. 2014). For exogenous chemicals p,p′-DDD 1,1-Dichloro-2,2-bis(p-chlorophenyl) such as pesticides, the physico-chemical properties and ethane the tissue interactions drive the pharmacokinetics (PKs), p,p′-DDE 1,1-Dichloro-2,2bis(4-chlorophenyl) resulting in short or long half-lives in humans, which ethylene could subsequently cause health efects. p,p′-DDT 1,1,1-Trichloro-2,2-bis(p-chlorophenyl) Biomonitoring is the measurement of contaminants ethane (parents and metabolites) in conventional biological SPME Solid-phase microextraction matrices such as blood or urine (NRC/NAS 2006) or in T1/2 Terminal elimination half-life non-conventional matrices such as hair (Beranger et al. TCPy 3,5,6-Trichloro-2-pyridinol 2018; Palazzi et al. 2018). Biomonitoring integrates all Tmax Time to reach the Cmax exposure routes, thereby providing important and useful WHO World Health Organization information; it is frequently used during studies involving environmental epidemiology; and it provides aggregate information about multi-residues. Many published stud- Introduction ies have discussed the use of diferent human matrices (e.g., urine, blood, hair) for evaluating chemical concen- Pesticides are widely used during crop production to con- trations. For example, results from a Canadian survey, trol insects, weeds, or other organisms. According to the which evaluated urine and blood samples collected from World Health Organization (WHO), there are more than 2007 to 2011 by Health Canada, showed that parents and 1000 pesticide formulations used around the world to ensure metabolites of organochlorines, organophosphates, pyre- that pests do not damage or destroy food (WHO 2018). The throids, and carbamates were detected and ranged from widespread use of pesticides for agricultural activities rep- 56% to 99% (Haines et al. 2017). During a European bio- resents thousands of molecules with a large range of phys- monitoring study, researchers detected urinary metabolites ico-chemical properties, and each pesticide or family has of organophosphates ranging from 61 to 100% and pyre- diferent properties and toxicological efects (WHO 2018). throids ranging from 60 to 98% in 600 German children Even though the European Union developed an extensive (Schulz et al. 2009). Another European biomonitoring methodology of assessment that covers the chemical, bio- study, researchers detected urinary metabolites of organo- logical, toxicological, and environmental behaviors of the phosphates ranging from 0 to 28% and pyrethroids ranging active ingredients before a pesticide is approved for use on from 5 to 100% in 1077 French women who were preg- the market (Tsaboula et al. 2016), we are still exposed to a nant (Dereumeaux et al. 2016). A study was conducted in mixture of pesticides through our diet and our environment. Luxembourg on 14 volunteers who provided hair samples, According to the literature, 912 million of pounds of which, when analyzed, revealed exposure to 11 diferent common popular pesticides are used annually in the United pesticides (Salquebre et al. 2012). More recently, a study States (Barr 2008). During agricultural activities, manage- of 101 volunteers living in Burkina Faso, West Africa, ment and crop production are rely on the use of herbicides, detected organochlorines (64%), pyrethroids (52%), and fungicides, and insecticides, amounting to approximately organophosphate (18%) pesticides in their hair samples 3.3 × 106 t/year worldwide, or specifcally 4.2 × 105 t/year (Lehmann et al. 2018). 1 3 Archives of Toxicology (2019) 93:2849–2862 2851 As previously mentioned, human biomonitoring provides pesticides for the mixture mainly based on their prevalence information about many contaminants (multi-residues) in several human biomonitoring studies reviewed (Appen- measured in biological matrices, but their interpretation zeller and Tsatsakis 2012; Salquebre et al. 2012). remains uncertain regarding the PKs. In addition, only a Sixty healthy Long–Evans rats (females aged 12 weeks few experimental studies have described the PK parame- and weighing between 180 and 200 g each) were purchased ters for a mixture exposure scenario to low or background from Janvier Labs (Saint-Berthevin, France). Before the human exposure doses, and then calculated the PK param- study, the rats were acclimated for least 1 week to the facil- eters individually. To quantitatively measure the impacts of ity, which
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