Skip to main content

Advertisement

SpringerLink
Log in

Estimating household exposure to pyrethroids and the relative contribution of inhalation pathway in a sample of Japanese children

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Several synthetic pyrethroids are suspected to have carcinogenicity or reproductive toxicity. However, there is little knowledge about indoor air pollution in residences or the extent of intake by the residents of the newly developed pyrethroids, transfluthrin, profluthrin, and metofluthrin, although they have been widely used indoors as mosquito repellents and mothproof repellents in recent years. In the present study, the household exposure to pyrethroids through all exposure pathways and the contribution of inhalation pathway in Japanese children were examined by measuring urinary pyrethroid metabolites in the children and the airborne pyrethroids in their residences. Urine excreted first after waking up was collected from subjects aged 6 to 15 years (n = 132), and airborne pyrethroids were sampled in the subjects’ bedrooms for 24 h. Nineteen pyrethroids and their nine urinary metabolites were measured. Their daily intakes estimated were as follows (median, ng/kg b.w./d): bifenthrin, 56; transfluthrin, 22; metofluthrin, 11; profluthrin, 0.86. The contribution rates of the amounts absorbed by inhalation to the amounts absorbed via all of the exposure pathways while at home tended to decrease in the following order: profluthrin (median 15%) ≈ transfluthrin (14%) > metofluthrin (1%) > bifenthrin (0.1%). Transfluthrin was considered to be the most notable pyrethroid as an indoor air pollutant. Our study demonstrated widespread exposure to transfluthrin, metofluthrin, profluthrin, and bifenthrin in a sample of Japanese children.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  • Babina K, Dollard M, Pilotto L, Edwards JW (2012) Environmental exposure to organophosphorus and pyrethroid pesticides in South Australian preschool children: a cross sectional study. Environ Int 48:109–120. https://doi.org/10.1016/j.envint.2012.07.007

    Article  CAS  Google Scholar 

  • Barr DB, Olsson AO, Wong LY, Udunka S, Baker SE, Whitehead RD Jr, Magsumbol MS, Williams BL, Needham LL (2010) Urinary concentrations of metabolites of pyrethroid insecticides in the general U.S. population: National Health and Nutrition Examination Survey 1999-2002. Environ Health Perspect 118:742–748. https://doi.org/10.1289/ehp.0901275

    Article  CAS  Google Scholar 

  • Becker K, Seiwert M, Angerer J, Kolossa-Gehring M, Hoppe HW, Ball M, Schulz C, Thumulla J, Seifert B (2006) GerES IV pilot study: assessment of the exposure of German children to organophosphorus and pyrethroid pesticides. Int J Hyg Environ Health 209:221–233. https://doi.org/10.1016/j.ijheh.2005.12.002

    Article  CAS  Google Scholar 

  • Bonsnes RW, Taussky HH (1945) On the colorimetric determination of creatinine by the Jaffe reaction. J Biol Chem 158:581–591

    Article  CAS  Google Scholar 

  • Bradman A, Whitaker D, Quirós L, Castorina R, Claus Henn B, Nishioka M, Morgan J, Barr DB, Harnly M, Brisbin JA, Sheldon LS, McKone TE, Eskenazi B (2007) Pesticides and their metabolites in the homes and urine of farmworker children living in the Salinas Valley, CA. J Expo Sci Environ Epidemiol 17:331–349. https://doi.org/10.1038/sj.jes.7500507

    Article  CAS  Google Scholar 

  • Centers for Disease Control and Prevention (CDC) (2019) Fourth national report on human exposure to environmental chemicals, updated tables, January 2019, Volume One. CDC, National Center for Environmental Health, Division of Laboratory Sciences, Atlanta, GA, USA

  • Chemical Daily (2019) 17019 no kagaku shohin. The Chemical Daily, Tokyo, Japan

    Google Scholar 

  • Communication and Information Resource Centre for Administrations, Businesses and Citizens (CIRCABC) (2014) Regulation (EU) n°528/2012 concerning the making available on the market and use of biocidal products, Evaluation of active substances, Assessment report, Transfluthrin (insecticides, acaricides and products to control other arthropods), 13 March 2014, RMS: the Netherlands. https://circabc.europa.eu/sd/a/910c7533-aba6-4a93-87c3-31c5f2b04445/Transfluthrin%20-%20PT18 (Accessed 27 July 2020)

  • Couture C, Fortin MC, Carrier G, Dumas P, Tremblay C, Bouchard M (2009) Assessment of exposure to pyrethroids and pyrethrins in a rural population of the Montérégie area, Quebec, Canada. J Occup Environ Hyg 6:341–352. https://doi.org/10.1080/15459620902850907

    Article  CAS  Google Scholar 

  • Deguchi Y, Yamada T, Hirose Y, Nagahori H, Kushida M, Sumida K, Sukata T, Tomigahara Y, Nishioka K, Uwagawa S, Kawamura S, Okuno Y (2009) Mode of action analysis for the synthetic pyrethroid metofluthrin-induced rat liver tumors: evidence for hepatic CYP2B induction and hepatocyte proliferation. Toxicol Sci 108:69–80. https://doi.org/10.1093/toxsci/kfp006

    Article  CAS  Google Scholar 

  • Ding G, Shi R, Gao Y, Zhang Y, Kamijima M, Sakai K, Wang G, Feng C, Tian Y (2012) Pyrethroid pesticide exposure and risk of childhood acute lymphocytic leukemia in Shanghai. Environ Sci Technol 46:13480–13487. https://doi.org/10.1021/es303362a

    Article  CAS  Google Scholar 

  • Elbetieha A, Da’as SI, Khamas W, Darmani H (2001) Evaluation of the toxic potentials of cypermethrin pesticide on some reproductive and fertility parameters in the male rats. Arch Environ Contam Toxicol 41:522–528. https://doi.org/10.1007/s002440010280

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2008) FAO specifications and evaluations for agricultural pesticides, Permethrin (40:60 cis:trans isomer ratio), FAO, Roma, Italy. http://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/Specs/Permetrhin08.pdf (Accessed 27 July 2020)

  • Food and Agriculture Organization of the United Nations (FAO) and the World Health Organization (WHO) (2012) Inventory of evaluations performed by the Joint Meeting on Pesticide Residues (JMPR). https://apps.who.int/pesticide-residues-jmpr-database/ (Accessed 27 July 2020)

  • Food and Agriculture Organization of the United Nations (FAO) and World Health Organization (WHO) (2009) Pesticide residues in food – 2009, Evaluations 2009, Part II – Toxicological. Joint FAO/WHO Meeting on Pesticide Residues. pp. 3–52, Geneva, Switzerland

  • Fortin MC, Bouchard M, Carrier G, Dumas P (2008a) Biological monitoring of exposure to pyrethrins and pyrethroids in a metropolitan population of the Province of Quebec, Canada. Environ Res 107:343–350. https://doi.org/10.1016/j.envres.2008.03.002

    Article  CAS  Google Scholar 

  • Fortin MC, Carrier G, Bouchard M (2008b) Concentrations versus amounts of biomarkers in urine: a comparison of approaches to assess pyrethroid exposure. Environ Health 7:55. https://doi.org/10.1186/1476-069X-7-55

    Article  CAS  Google Scholar 

  • Glorennec P, Serrano T, Fravallo M, Warembourg C, Monfort C, Cordier S, Viel JF, Le Gléau F, Le Bot B, Chevrier C (2017) Determinants of children's exposure to pyrethroid insecticides in western France. Environ Int 104:76–82. https://doi.org/10.1016/j.envint.2017.04.007

    Article  CAS  Google Scholar 

  • Hamada R, Ueda Y, Wada K, Saito I, Nomura H, Kamijima M, Nakane K, Nagata C, Kondo T, Ueyama J (2020) Ten-year temporal trends (2006-2015) and seasonal-differences in urinary metabolite concentrations of novel, hygiene-used pyrethroids in Japanese children. Int J Hyg Environ Health 225:113448. https://doi.org/10.1016/j.ijheh.2019.113448

    Article  CAS  Google Scholar 

  • Health Canada (2019) Fifth report on human biomonitoring of environmental chemicals in Canada, results of the Canadian Health Measures Survey Cycle 5 (2016–2017), the Minister of Health, Ottawa, Ontario, Canada

  • Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 5:46–51

    Article  CAS  Google Scholar 

  • Kaneko H (2010) Pyrethroid chemistry and metabolism. In Hayes’ Handbook of Pesticide Toxicology, 3rd ed, eds. Krieger R, Elsevier. pp. 1635–1663

  • Kim SS, Rhee GS, Kim SH, Sohn KH, Kwack SJ, Kim BH, Lee RD, Park KL (2002) Permethrin affects reproductive developments in rats. Teratology 65:333

    Google Scholar 

  • Kumagai S, Matsunaga I (2000) A lung model describing uptake of organic solvents and roles of mucosal blood flow and metabolism in the bronchioles. Inhal Toxicol 12:491–510. https://doi.org/10.1080/089583700402888

    Article  CAS  Google Scholar 

  • Leng G, Gries W (2005) Simultaneous determination of pyrethroid and pyrethrin metabolites in human urine by gas chromatography-high resolution mass spectrometry. J Chromatogr B 814:285–294. https://doi.org/10.1016/j.jchromb.2004.10.044

    Article  CAS  Google Scholar 

  • Leng G, Berger-Preiß E, Levsen K, Ranft U, Sugiri D, Hadnagy W, Idel H (2005) Pyrethroids used indoor - ambient monitoring of pyrethroids following a pest control operation. Int J Hyg Environ Health 208:193–199. https://doi.org/10.1016/j.ijheh.2005.01.016

    Article  CAS  Google Scholar 

  • Leng G, Gries W, Selim S (2006) Biomarker of pyrethrum exposure. Toxicol Lett 162:195–201. https://doi.org/10.1016/j.toxlet.2005.09.030

    Article  CAS  Google Scholar 

  • Li AJ, Kannan K (2018) Urinary concentrations and profiles of organophosphate and pyrethroid pesticide metabolites and phenoxyacid herbicides in populations in eight countries. Environ Int 121:1148–1154. https://doi.org/10.1016/j.envint.2018.10.033

    Article  CAS  Google Scholar 

  • Lu C, Barr DB, Pearson M, Bartell S, Bravo R (2006) A longitudinal approach to assessing urban and suburban children's exposure to pyrethroid pesticides. Environ Health Perspect 114:1419–1423. https://doi.org/10.1289/ehp.9043

    Article  CAS  Google Scholar 

  • MacBean C (2008-2010) e-Pesticide manual. 15th ed., ver. 5.1, British Crop Protection Council, Alton, UK

  • Mallick P, Moreau M, Song G, Efremenko AY, Pendse SN, Creek MR, Osimitz TG, Hines RN, Hinderliter P, Clewell HJ, Lake BG, Yoon M (2020) Development and application of a life-stage physiologically based pharmacokinetic (PBPK) model to the assessment of internal dose of pyrethroids in humans. Toxicol Sci 173:86–99. https://doi.org/10.1093/toxsci/kfz211

    Article  Google Scholar 

  • Massey Jr FJ (1951) The Kolmogorov-Smirnov test for goodness of fit. J Am Stat Assoc 46 (Issue 253): 68-78. https://doi.org/10.2307/2280095

  • Matsuo N, Ujihara K, Shono Y, Iwasaki T, Sugano M, Yoshiyama T, Uwagawa S (2005) Discovery and development of a novel pyrethroid insecticide ‘Metofluthrin (SumiOne, Eminence)’. SUMITOMO KAGAKU 2005-II, 4–16

  • Moniz AC, Cruz-Casallas PE, Oliveira CA, Lucisano A, Florio JC, Nicolau AA, Spinosa HS, Bernardi MM (1999) Perinatal fenvalerate exposure: behavioral and endocrinology changes in male rats. Neurotoxicol Teratol 21:611–618. https://doi.org/10.1016/s0892-0362(99)00004-5

    Article  CAS  Google Scholar 

  • Morgan MK, Sheldon LS, Croghan CW, Jones PA, Chuang JC, Wilson NK (2007) An observational study of 127 preschool children at their homes and daycare centers in Ohio: environmental pathways to cis- and trans-permethrin exposure. Environ Res 104:266–274. https://doi.org/10.1016/j.envres.2006.11.011

    Article  CAS  Google Scholar 

  • Moriyama M, Saito H, Kabuto M (1987) Relationship between twenty-four hour urinary creatinine excretion and weight, or weight and height of Japanese children. J Nutr Sci Vitaminol 33:185–193. https://doi.org/10.3177/jnsv.33.185

    Article  CAS  Google Scholar 

  • Osaka A, Ueyama J, Kondo T, Nomura H, Sugiura Y, Saito I, Nakane K, Takaishi A, Ogi H, Wakusawa S, Ito Y, Kamijima M (2016) Exposure characterization of three major insecticide lines in urine of young children in Japan - neonicotinoids, organophosphates, and pyrethroids. Environ Res 147:89–96. https://doi.org/10.1016/j.envres.2016.01.028

    Article  CAS  Google Scholar 

  • Panuwet P, Prapamontol T, Chantara S, Barr DB (2009) Urinary pesticide metabolites in school students from northern Thailand. Int J Hyg Environ Health 212:288–297. https://doi.org/10.1016/j.ijheh.2008.07.002

    Article  CAS  Google Scholar 

  • Roca M, Miralles-Marco A, Ferré J, Pérez R, Yusà V (2014) Biomonitoring exposure assessment to contemporary pesticides in a school children population of Spain. Environ Res 131:77–85. https://doi.org/10.1016/j.envres.2014.02.009

    Article  CAS  Google Scholar 

  • Spjøtvoll E, Stoline MR (1973) An extension of the T-method of multiple comparison to include the cases with unequal sample sizes. J Am Stat Assoc 68:976–978. https://doi.org/10.1080/01621459.1973.10481458

    Article  Google Scholar 

  • Tao L, Chen M, Collins E, Lu C (2013) Simultaneous quantitation of seven pyrethroid metabolites in human urine by capillary gas chromatography-mass spectrometry. J Sep Sci 36:773–780. https://doi.org/10.1002/jssc.201200655

    Article  CAS  Google Scholar 

  • Tisch M, Faulde MK, Maier H (2005) Genotoxic effects of pentachlorophenol, lindane, transfluthrin, cyfluthrin, and natural pyrethrum on human mucosal cells of the inferior and middle nasal conchae. Am J Rhinol 19:141–151

    Article  Google Scholar 

  • 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 48:1931–1939. https://doi.org/10.1021/es403661a

    Article  CAS  Google Scholar 

  • Tulve NS, Egeghy PP, Fortmann RC, Whitaker DA, Nishioka MG, Naeher LP, Hilliard A (2008) Multimedia measurements and activity patterns in an observational pilot study of nine young children. J Expo Sci Environ Epidemiol 18:31–44. https://doi.org/10.1038/sj.jes.7500600

    Article  CAS  Google Scholar 

  • U.S. Environmental Protection Agency (EPA) (2006) Reregistration eligibility decision for resmethrin, List A, Case no. 0421. US EPA, Washington, DC

  • U.S. Environmental Protection Agency (EPA) (2009a) Reregistration eligibility decision (RED) for permethrin, Revised May 2009, Case no. 2510. US EPA, Washington, DC

  • U.S. Environmental Protection Agency (EPA) (2009b) Reregistration eligibility decision (RED) for allethrins, Revised May 2009, List C, Case no. 0437. US EPA, Washington, DC

  • Ueda Y, Oda M, Saito I, Hamada R, Kondo T, Kamijima M, Ueyama J (2018) A sensitive and efficient procedure for the high-throughput determination of nine urinary metabolites of pyrethroids by GC-MS/MS and its application in a sample of Japanese children. Anal. Bioanal Chem 410:6207–6217. https://doi.org/10.1007/s00216-018-1229-x

    Article  CAS  Google Scholar 

  • Ujihara K, Sugano M, Nakada K, Iwakura K, Nishihara K, Katoh H (2010) Discovery and development of profluthrin (Fairytale), a new active ingredient of moth proofer. SUMITOMO KAGAKU 2010-II, 13–23

  • Wielgomas B, Piskunowicz M (2013) Biomonitoring of pyrethroid exposure among rural and urban populations in northern Poland. Chemosphere 93:2547–2553. https://doi.org/10.1016/j.chemosphere.2013.09.070

    Article  CAS  Google Scholar 

  • Ye X, Pan W, Zhao S, Zhao Y, Zhu Y, Liu J, Liu W (2017a) Relationships of pyrethroid exposure with gonadotropin levels and pubertal development in Chinese boys. Environ Sci Technol 51:6379–6386. https://doi.org/10.1021/acs.est.6b05984

    Article  CAS  Google Scholar 

  • Ye X, Pan W, Zhao Y, Zhao S, Zhu Y, Liu W, Liu J (2017b) Association of pyrethroids exposure with onset of puberty in Chinese girls. Environ Pollut 227:606–612. https://doi.org/10.1016/j.envpol.2017.04.035

    Article  CAS  Google Scholar 

  • Yokohira M, Arnold LL, Lautraite S, Sheets L, Wason S, Stahl B, Eigenberg D, Pennington KL, Kakiuchi-Kiyota S, Cohen SM (2011) The effects of oral treatment with transfluthrin on the urothelium of rats and its metabolite, tetrafluorobenzoic acid on urothelial cells in vitro. Food Chem Toxicol 49:1215–1223. https://doi.org/10.1016/j.fct.2011.02.022

    Article  CAS  Google Scholar 

  • Yoshida T (2009) Simultaneous determination of 18 pyrethroids in indoor air by gas chromatography/mass spectrometry. J Chromatogr A 1216:5069–5076. https://doi.org/10.1016/j.chroma.2009.04.087

    Article  CAS  Google Scholar 

  • Yoshida T (2014a) Biomarkers for monitoring transfluthrin exposure: urinary excretion kinetics of transfluthrin metabolites in rats. Environ Toxicol Pharmacol 37:103–109. https://doi.org/10.1016/j.etap.2013.11.011

    Article  CAS  Google Scholar 

  • Yoshida T (2014b) Biomarkers for monitoring profluthrin exposure: urinary excretion kinetics of profluthrin metabolites in rats. Environ Toxicol Pharmacol 37:1123–1128. https://doi.org/10.1016/j.etap.2014.03.019

    Article  CAS  Google Scholar 

  • Yoshida T (2015) 4-Methoxymethyl-2,3,5,6-tetrafluorobenzyl alcohol as a urinary biomarker for monitoring of metofluthrin, a fluorine-containing pyrethroid, in exposed rats. Biomarkers 20:71–76. https://doi.org/10.3109/1354750X.2014.992814

    Article  CAS  Google Scholar 

  • Yoshida T (2017) Analytical method for pyrethroid metabolites in urine of the non-occupationally exposed population by gas chromatography/mass spectrometry. J Chromatogr Sci 55:873–881. https://doi.org/10.1093/chromsci/bmx048

    Article  CAS  Google Scholar 

  • Zapletal A, Samanek M, Paul T (1987) Lung function in children and adolescents. In: Methods, reference values. Progress in respiration research, Herzog H (Ed.), vol 22. S. Karger, Basel, Switzerland

Download references

Acknowledgments

We thank the staff of the Osaka Institute of Public Health for assistance with the collection of samples. We thank Dainihon Jochugiku, Earth Chemical, and Sumitomo Chemical for the gift of the standard materials for measuring airborne pyrethroids and their urinary metabolites.

Funding

This work was supported by the Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (MEXT)/Japan Society for the Promotion of Science (JSPS) KAKENHI [grant number 26460820].

Author information

Authors and Affiliations

  1. Osaka Institute of Public Health, 1-3-69, Nakamichi, Higashinari-ku, Osaka, 537-0025, Japan

    Toshiaki Yoshida, Mayumi Mimura & Naomi Sakon

Authors
  1. Toshiaki Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mayumi Mimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naomi Sakon
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TY designed this study, and collected and analyzed the samples from the subjects, and a major contributor in writing the manuscript. MM and NS contributed to secure the subjects, and collected the samples from the subjects. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Toshiaki Yoshida.

Ethics declarations

Ethics approval and consent to participate

This study was carried out after approval by the Ethical Review Committee of the Osaka Prefectural Institute of Public Health (reference number 1310-11-2). Written informed consent was obtained from the parents of all the children before the study.

Conflict of interest

The authors declare that they have no conflict of interest.

Consent for publication

Not applicable.

Additional information

Responsible editor: Lotfi Aleya

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoshida, T., Mimura, M. & Sakon, N. Estimating household exposure to pyrethroids and the relative contribution of inhalation pathway in a sample of Japanese children. Environ Sci Pollut Res 28, 19310–19324 (2021). https://doi.org/10.1007/s11356-020-12060-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-12060-9

Keywords

Search

Navigation