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Assessment of occupational exposure to pesticide mixtures with endocrine-disrupting activity

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Abstract

Occupational exposure to pesticide mixtures comprising active substance(s) and/or co-formulant(s) with known/possible endocrine-disrupting activity was assessed using long-term activity records for 50 professional operators representing arable and orchard cropping systems in Greece, Lithuania, and the UK. Exposure was estimated using the harmonised Agricultural Operator Exposure Model, and risk was quantified as a point of departure index (PODI) using the lowest no observed (adverse) effect level. Use of substances with known/possible endocrine activity was common, with 43 of the 50 operators applying at least one such active substance on more than 50% of spray days; at maximum, one UK operator sprayed five such active substances and 10 such co-formulants in a single day. At 95th percentile, total exposure was largest in the UK orchard system (0.041 × 10−2 mg kg bw−1 day−1) whereas risk was largest in the Greek cropping systems (PODI 0.053 × 10−1). All five cropping systems had instances indicating potential for risk when expressed at a daily resolution (maximum PODI 1.2–10.7). Toxicological data are sparse for co-formulants, so combined risk from complex mixtures of active substances and co-formulants may be larger in reality.

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References

  • Bang DY, Kyung M, Kim MJ, Jung BY, Cho MC, Choi SM, Kim YW, Lim SK, Lim DS, Won AJ, Kwack SJ, Lee Y, Kim HS, Lee BM (2012) Human risk assessment of endocrine-disrupting chemicals derived from plastics food containers. Compr Rev Food Sci Food Saf 11:453–470

    Article  CAS  Google Scholar 

  • Bullock WH, Ignacio JS (2006) A strategy for assessing and managing occupational exposures, 3rd edn. American Industrial Hygiene Association (AIHA Press), Fairfax

  • Castro MJL, Ojeda C, Cirelli AF (2014) Advances in surfactants for agrochemicals. Environ Chem Lett 12:85–95

    Article  CAS  Google Scholar 

  • Christiansen S, Kortenkamp A, Axelstad M, Boberg J, Scholze M, Jacobsen PR, Faust M, Lichtensteiger W, Schlumpf M, Burdorf A, Hass U (2012) Mixtures of endocrine disrupting contaminants modelled on human high end exposures: an exploratory study in rats. Int J Androl 35:303–316

    Article  CAS  Google Scholar 

  • Cremonese C, Piccoli C, Pasqualotto F, Clapauch R, Koifman RJ, Koifman S, Freire C (2017) Occupational exposure to pesticides, reproductive hormone levels and sperm quality in young Brazilian men. Reprod Toxicol 67:174–185

    Article  CAS  Google Scholar 

  • Damalas CA, Abdollahzadeh G (2016) Farmers’ use of personal protective equipment during handling of plant protection products: determinants of implementation. Sci Total Environ 571:730–736

    Article  CAS  Google Scholar 

  • Defarge N, Takacs E, Lozano VL et al (2016) Co-formulants in glyphosate-based herbicides disrupt aromatase activity in human cells below toxic levels. Int J Environ Res Public Health 13:264. https://doi.org/10.3390/ijerph13030264

    Article  CAS  Google Scholar 

  • EFSA (2013a) Scientific opinion on the hazard assessment of endocrine disruptors: scientific criteria for identification of endocrine disruptors and appropriateness of existing test methods for assessing effects mediated by these substances on human health and the Environment. EFSA J 11(3):3132

    Article  CAS  Google Scholar 

  • EFSA (2013b) Scientific opinion on the identification of pesticides to be included in cumulative assessment groups on the basis of their toxicological profile. EFSA J 11(7):3293

    Google Scholar 

  • Ewence A, Rumsby P, Johnson I (2013) Extended impact assessment study of the human health and environmental criteria for endocrine disrupting substances proposed by HSE, CRD. Report number Defra9088.02. WRc plc, Swindon

    Google Scholar 

  • Ewence A, Brescia S, Johnson I, Rumsby PC (2015) An approach to the identification and regulation of endocrine disrupting pesticides. Food Chem Toxicol 78:214–220

    Article  CAS  Google Scholar 

  • Futran Fuhrman V, Tal A, Arnon S (2015) Why endocrine disrupting chemicals (EDCs) challenge traditional risk assessment and how to respond. J Hazard Mater 286:589–611

    Article  CAS  Google Scholar 

  • Garthwaite D, Sinclair CJ, Glass R et al (2015) Collection of pesticide application data in view of performing environmental risk assessments for pesticides. EFSA Supporting Publications 12(7):846E

    Article  Google Scholar 

  • Groβkopf C, Martin S, Mielke H et al (2013) Joint development of a new agricultural operator exposure model. BfR Wissenschaft, Berlin

    Google Scholar 

  • Hass U, Boberg J, Christiansen S, Jacobsen PR, Vinggaard AM, Taxvig C, Poulsen ME, Herrmann SS, Jensen BH, Petersen A, Clemmensen LH, Axelstad M (2012) Adverse effects on sexual development in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod Toxicol 34:261–274

    Article  CAS  Google Scholar 

  • Hernandez AF, Tsatsakis AM (2017) Human exposure to chemical mixtures: challenges for the integration of toxicology with epidemiology data in risk assessment. Food Chem Toxicol 103:188–193

    Article  CAS  Google Scholar 

  • Hossain F, Ali O, D’Souza UJA, Naing DKS (2010) Effects of pesticide use on semen quality among farmers in rural areas of Sabah, Malaysia. J Occup Health 52:353–360

    Article  CAS  Google Scholar 

  • Kienzler A, Bopp SK, van der Linden S, Berggren E, Worth A (2016) Regulatory assessment of chemical mixtures: requirements, current approaches and future perspectives. Regul Toxicol Pharmacol 80:321–334

    Article  CAS  Google Scholar 

  • Kortenkamp A, Faust M, Scholze M, Backhaus T (2007) Low-level exposure to multiple chemicals: reason for human health concerns? Environ Health Perspect 115:106–114

    Article  Google Scholar 

  • Lewis KA, Tzilivakis J, Warner DJ, Green A (2016) An international database for pesticide risk assessments and management. Hum Ecol Risk Assess Int J 22:1050–1064

    Article  CAS  Google Scholar 

  • Lichtenberg B, Mischke U, Scherf S, Rover M, Martin S (2015) Hazard and risk based allocation of safety instruction to operators handling pesticides. J. Consum Protect Food Saf 10:373–384

    Article  CAS  Google Scholar 

  • Liu P, Song X, Yuan W, Wen W, Wu X, Li J, Chen X (2006) Effects of cypermethrin and methyl parathion mixtures on hormone levels and immune functions in Wistar rats. Arch Toxicol 80:449–457

    Article  CAS  Google Scholar 

  • Lv X, Pan L, Wang J, Lu L, Yan W, Zhu Y, Xu Y, Guo M, Zhuang S (2017) Effects of triazole fungicides on androgenic disruption and CYP3A4 enzyme activity. Environ Pollut 222:504–512

    Article  CAS  Google Scholar 

  • Manibusan MK, Touart LW (2017) A comprehensive review of regulatory test methods for endocrine adverse health effects. Crit Rev Toxicol 47:433–481

    Article  CAS  Google Scholar 

  • Marx-Stoelting P, Niemann L, Ritz V, Ulbrich B, Gall A, Hirsch-Ernst KI, Pfeil R, Solecki R (2014) Assessment of three approaches for regulatory decision making on pesticides with endocrine disrupting properties. Regul Toxicol Pharmacol 70:590–604

    Article  CAS  Google Scholar 

  • Marx-Stoelting P, Pfeil R, Ritz V (2016) Science-based decision matrix for the identification of endocrine disruptors for regulatory purposes. J Verbr Lebensm 11:203–208

    Article  CAS  Google Scholar 

  • Mehrpour O, Karrari P, Zamani N, Tsatsakis AM, Abdollahi M (2014) Occupational exposure to pesticides and consequences on male semen and fertility: a review. Toxicol Lett 230:146–156

    Article  CAS  Google Scholar 

  • Melching-Kollmuss S, Fussell KC, Schneider S, Buesen R, Groeters S, Strauss V, van Ravenzwaay B (2017) Comparing effect levels of regulatory studies with endpoints derived in targeted anti-androgenic studies: example prochloraz. Arch Toxicol 91:143–162

    Article  CAS  Google Scholar 

  • Mesnage R, Phedonos A, Biserni M, Arno M, Balu S, Corton JC, Ugarte R, Antoniou MN (2017) Evaluation of estrogen receptor alpha activation by glyphosate-based herbicide constituents. Food Chem Toxicol 108:30–42

    Article  CAS  Google Scholar 

  • Mullin CA, Fine JD, Reynolds RD, Frazier MT (2016) Toxicological risks of agrochemical spray adjuvants: organosilicone surfactants may not be safe. Front Public Health 4:92. https://doi.org/10.3389/fpubh.2016.00092

    Article  Google Scholar 

  • OECD (2012) Guidance document on standardised test guidelines for evaluating chemicals for endocrine disruption. Joint Meeting of the Chemicals Committee and the Working Party on Chemicals, Pesticides and Biotechnology. ENV/JM/MONO(2012)22. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono%282012%2922&doclanguage=en. Accessed 15 March 2018

  • Panizzi S, Suciu NA, Trevisan M (2017) Combined ecotoxicological risk assessment in the frame of European authorisation of pesticides. Sci Total Environ 580:136–146

    Article  CAS  Google Scholar 

  • PPDB (2018) The Pesticide Properties Database (PPDB) developed by the Agriculture & Environment Research Unit (AERY), University of Hertfordshire, funded by UK national sources and the EU-funded Footprint Project (FP6-SSP-022704). http://sitem.herts.ac.uk/aeru/ppdb/en/atoz.htm. Accessed 15 March 2018

  • Rizzati V, Briand O, Guillou H, Gamet-Payrastre L (2016) Effects of pesticide mixtures in human and animal models: an update of the recent literature. Chem Biol Interact 254:231–246

    Article  CAS  Google Scholar 

  • Rocheleau CM, Romitti PA, Dennis LK (2009) Pesticides and hypospadias: a meta-analysis. J Pediatr Urol 5:17–24

    Article  Google Scholar 

  • Sarigiannis DA, Hansen U (2012) Considering the cumulative risk of mixtures of chemicals – a challenge for policy makers. Environ Health 11:S18

    Article  Google Scholar 

  • Sidorkiewicz I, Zareba K, Wolczynski S, Czerniecki J (2017) Endocrine-disrupting chemicals – mechanism of action on male reproductive system. Toxicol Ind Health 33:601–609

    Article  CAS  Google Scholar 

  • Slama R, Bourguignon J, Demeneix B et al (2016) Scientific issues relevant to setting regulatory criteria to identify endocrine-disrupting substances in the European Union. Environ Health Perspect 124:1497–1503

    Article  Google Scholar 

  • Solecki R, Kortenkamp A, Bergman A, Chahoud I, Degen GH, Dietrich D, Greim H, Håkansson H, Hass U, Husoy T, Jacobs M, Jobling S, Mantovani A, Marx-Stoelting P, Piersma A, Ritz V, Slama R, Stahlmann R, van den Berg M, Zoeller RT, Boobis AR (2017) Scientific principles for the identification of endocrine-disrupting chemicals: a consensus statement. Arch Toxicol 91:1001–1006

    Article  CAS  Google Scholar 

  • Teng M, Qi S, Zhu W, Wang Y, Wang D, Dong K, Wang C (2018) Effects of the bioconcentration and parental transfer of environmentally relevant concentrations of difenoconazole on endocrine disruption in zebrafish (Danio rerio). Environ Pollut 233:208–217

    Article  CAS  Google Scholar 

  • Testai E, Galli CL, Dekant W, Marinovich M, Piersma AH, Sharpe RM (2013) A plea for risk assessment of endocrine disrupting chemicals. Toxicology 314:51–59

    Article  CAS  Google Scholar 

  • Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33:378–455

    Article  CAS  Google Scholar 

  • WHO/IPCS (2002) Global assessment of the state-of-the-science of endocrine disruptors. http://www.who.int/ipcs/publications/new_issues/endocrine_disruptors/en/. Accessed 15 Jan 2018

  • Wong HL, Garthwaite DG, Ramwell CT, Brown CD (2018) Assessment of exposure of professional agricultural operators to pesticides. Sci Total Environ 619-620:874–882

    Article  CAS  Google Scholar 

  • Yusoff SNM, Kamari A, Aljafree NFA (2016) A review of materials used as carrier agents in pesticide formulations. Int J Enviorn Sci Technol 13:2977–2994

    Article  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge sponsorship of this research by the Ministry of Education, Malaysia, and the Universiti Malaysia Kelantan (UMK).

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Authors and Affiliations

  1. Environment Department, University of York, York, YO10 5NG, UK

    Hie Ling Wong & Colin D. Brown

  2. Faculty of Earth Science, University Malaysia Kelantan, Locked Bag 100, 17600, Jeli, Kelantan, Malaysia

    Hie Ling Wong

  3. Fera Science Ltd. (Fera), Sand Hutton, York, YO41 1LZ, UK

    David G. Garthwaite & Carmel T. Ramwell

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  1. Hie Ling Wong
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  2. David G. Garthwaite
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Correspondence to Hie Ling Wong.

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Responsible editor: Philippe Garrigues

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Wong, H.L., Garthwaite, D.G., Ramwell, C.T. et al. Assessment of occupational exposure to pesticide mixtures with endocrine-disrupting activity. Environ Sci Pollut Res 26, 1642–1653 (2019). https://doi.org/10.1007/s11356-018-3676-5

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  • DOI: https://doi.org/10.1007/s11356-018-3676-5

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