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Prenatal exposure to pyrethroid insecticides and birth outcomes in Rural Northern China

Journal of Exposure Science & Environmental Epidemiology volume 25, pages 264–270 (2015)Cite this article

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Abstract

Although pyrethroid insecticides are widely used, little is known about potential adverse effects on fetal growth. Participating 454 mother–infant pairs were recruited from a prospective birth cohort in rural northern China between September 2010 and 2012. We measured five non-specific pyrethroid metabolites in maternal urine at delivery and examined their association with birth outcomes including birth weight, length, head circumference, and gestational duration. The creatinine-adjusted medians of pyrethroid metabolites in urine were 0.51 μg/g for cis-DCCA, 0.65 μg/g for trans-DCCA, and 0.68 μg/g for 3-PBA. The pregnant women had substantially higher levels of urinary pyrethroid metabolites compared with those reported in developed countries. A increase in total (the sum of cis-DCCA, trans-DCCA, and 3-PBA) but not individual urinary metabolite levels was associated with a decrease in birth weight (adjusted β=–96.76 g per log10 unit increase, 95% confidence interval=–173.15 to –20.37). No associations were found between individual or total metabolite levels and birth length, head circumference, or gestational duration. We report an adverse association of prenatal exposure to pyrethroids as measured by urinary metabolites with birth weight. More studies are warranted in China given the relatively high levels of urinary metabolites in our study population.

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References

  1. Lu C, Barr DB, Pearson M, Bartell S, Bravo R . A longitudinal approach to assessing urban and suburban children’s exposure to pyrethroid pesticides. Environ Health Perspect 2006; 114: 1419–1423.

    Article  CAS  Google Scholar 

  2. Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D et al. Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 2002; 171: 3–59.

    Article  CAS  Google Scholar 

  3. Agency for Toxic Substances and Disease Registry (Atlanta, GA). Toxicological Profile for Pyrethrins and Pyrethroids, September, 2003. <http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=787&tid=153>. (accessed 3 March 2011).

  4. Shafer TJ, Meyer DA, Crofton KM . Developmental neurotoxicity of pyrethroid insecticides: critical review and future research needs. Environ Health Perspect 2005; 113: 123–136.

    Article  CAS  Google Scholar 

  5. Weselak M, Arbuckle TE, Foster W . Pesticide exposures and developmental outcomes: the epidemiological evidence. J Toxicol Environ Health B Crit Rev 2007; 10: 41–80.

    Article  CAS  Google Scholar 

  6. Leng G, Leng A, Kühn KH, Lewalter J, Pauluhn J . Human dose-excretion studies with the pyrethroid insecticide cyfluthrin: urinary metabolite profile following inhalation. Xenobiotica 1997; 27: 1273–1283.

    Article  CAS  Google Scholar 

  7. Barr DB, Olsson AO, Wong LY, Udunka S, Baker SE, Whitehead RD et al. Urinary concentrations of metabolites of pyrethroid insecticides in the general U.S. population: National Health and Nutrition Examination Survey 1999-2002. Environ Health Perspect 2010; 118: 742–748.

    Article  CAS  Google Scholar 

  8. Du G, Shen O, Sun H, Fei J, Lu C, Song L et al. Assessing hormone receptor activities of pyrethroid insecticides and their metabolites in reporter gene assays. Toxicol Sci 2010; 116: 58–66.

    Article  CAS  Google Scholar 

  9. Akhtar N, Kayani SA, Ahmad MM, Shahab M . Insecticide-induced changes in secretory activity of the thyroid gland in rats. J Appl Toxicol 1996; 16: 397–400.

    Article  CAS  Google Scholar 

  10. Maiti PK, Kar A . Is triiodothyronine capable of ameliorating pyrethroid-induced thyroid dysfunction and lipid peroxidation? J Appl Toxicol 1998; 18: 125–128.

    Article  CAS  Google Scholar 

  11. Bian Q, Xu LC, Wang SL, Xia YK, Tan LF, Chen JF et al. Study on the relation between occupational fenvalerate exposure and spermatozoa DNA damage of pesticide factory workers. Occup Environ Med 2004; 61: 999–1005.

    Article  CAS  Google Scholar 

  12. Pine MD, Hiney JK, Lee B, Dees WL . The pyrethroid pesticide esfenvalerate suppresses the afternoon rise of luteinizing hormone and delays puberty in female rats. Environ Health Perspect 2008; 116: 1243–1247.

    Article  CAS  Google Scholar 

  13. Ding G, Shi R, Gao Y, Zhang Y, Kamijima M, Sakai K et al. Pyrethroid pesticide exposure and risk of childhood acute lymphocytic leukemia in Shanghai. Environ Sci Technol 2012; 46: 13480–13487.

    Article  CAS  Google Scholar 

  14. Landrigan PJ, Kimmel CA, Correa A, Eskenazi B . Children’s health and the environment: public health issues and challenges for risk assessment. Environ Health Perspect 2004; 112: 257–265.

    Article  CAS  Google Scholar 

  15. Wu C, Feng C, Qi X, Wang G, Zheng M, Chang X et al. Urinary metabolite levels of pyrethroid insecticides in infants living in an agricultural area of the Province of Jiangsu in China. Chemosphere 2013; 90: 2705–2713.

    Article  CAS  Google Scholar 

  16. Qi X, Zheng M, Wu C, Wang G, Feng C, Zhou Z et al. Urinary pyrethroid metabolites among pregnant women in an agricultural area of the Province of Jiangsu, China. Int J Hyg Environ Health 2012; 215: 487–495.

    Article  CAS  Google Scholar 

  17. Heudorf U, Angerer J . Metabolites of pyrethroid insecticides in urine specimens: current exposure in an urban population in Germany. Environ Health Perspect 2001; 109: 213–217.

    Article  CAS  Google Scholar 

  18. Oulhote Y, Bouchard MF . Urinary metabolites of organophosphate and pyrethroid pesticides and behavioral problems in canadian children. Environ Health Perspect 2013; 121: 1378–1384.

    Article  Google Scholar 

  19. Hanke W, Romitti P, Fuortes L, Sobala W, Mikulski M . The use of pesticides in a Polish rural population and its effect on birth weight. Int Arch Occup Environ Health 2003; 76: 614–620.

    Article  Google Scholar 

  20. Dabrowski S, Hanke W, Polańska K, Makowiec-Dabrowska T, Sobala W . Pesticide exposure and birthweight: an epidemiological study in Central Poland. Int J Occup Med Environ Health 2003; 16: 31–39.

    PubMed  Google Scholar 

  21. US Environmental Protection Agency. Organophosphate Pesticides: Revised Cumulative Risk Assessment, June 2002. <http://www.epa.gov/oppsrrd1/cumulative/rra-op/>. (accessed 9 May 2012).

  22. Barr DB, Needham LL . Analytical methods for biological monitoring of exposure to pesticides: a review. J Chromatogr B Analyt Technol Biomed Life Sci 2002; 778: 5–29.

    Article  CAS  Google Scholar 

  23. Eadsforth CV, Bragt PC, van Sittert NJ . Human dose-excretion studies with pyrethroid insecticides cypermethrin and alphacypermethrin: relevance for biological monitoring. Xenobiotica 1988; 18: 603–614.

    Article  CAS  Google Scholar 

  24. Leng G, Kühn KH, Idel H . Biological monitoring of pyrethroid metabolites in urine of pest control operators. Toxicol Lett 1996; 88: 215–220.

    Article  CAS  Google Scholar 

  25. Ding G, Cui C, Chen L, Gao Y, Zhou Y, Shi R et al. Prenatal low-level mercury exposure and neonatal anthropometry in rural northern China. Chemosphere 2013; 92: 1085–1089.

    Article  CAS  Google Scholar 

  26. Kühn K, Leng G, Bucholski K, Dunemann L, Idel H . Determination of pyrethroid metabolites in human urine by capillary gas chromatography−mass spectrometry. Chromatographia 1996; 43: 285–292.

    Article  Google Scholar 

  27. Hornung RW, Reed DL . Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 1990; 5: 46–51.

    Article  CAS  Google Scholar 

  28. US Centers for Disease Control and Prevention. National Report on Human Exposure to Environmental Chemicals, August 2014. <http://www.cdc.gov/exposurereport/pdf/FourthReport_UpdatedTables_Aug2014.pdf>. (accessed 3 June 2014).

  29. Castorina R, Bradman A, Fenster L, Barr DB, Bravo R, Vedar MG et al. Comparison of current-use pesticide and other toxicant urinary metabolite levels among pregnant women in the CHAMACOS cohort and NHANES. Environ Health Perspect 2010; 118: 856–863.

    Article  CAS  Google Scholar 

  30. Wielgomas B, Nahorski W, Czarnowski W . Urinary concentrations of pyrethroid metabolites in the convenience sample of an urban population of Northern Poland. Int J Hyg Environ Health 2013; 216: 295–300.

    Article  CAS  Google Scholar 

  31. Dewailly E, Forde M, Robertson L, Kaddar N, Laouan Sidi EA, Côté S et al. Evaluation of pyrethroid exposures in pregnant women from 10 Caribbean countries. Environ Int 2014; 63: 201–206.

    Article  CAS  Google Scholar 

  32. Qin L, Yang M, Wang J, Jiang D, Cao Q . Surveillance on pesticides residues in vegetables and fruits [in Chinese]. Shi Yong Yu Fang Yi Xue 2011; 8: 2315–2316.

    Google Scholar 

  33. GB2763−2005 National Standard of Maximum Residue Limits for Pesticides in Food [in Chinese]. Nation Programme on Food Safety: Beijing, China. 2005.

  34. Zhang W, Jiang F, Ou J . Global pesticide consumption and pollution: with China as a focus. Proc Int Ecol Environ Sci 2011; 1: 125–144.

    CAS  Google Scholar 

  35. Li P, Feng X, Yuan X, Chan HM, Qiu G, Sun GX et al. Rice consumption contributes to low level methylmercury exposure in southern China. Environ Int 2012; 49: 18–23.

    Article  CAS  Google Scholar 

  36. Ministry of Environmental Protection of China. Organophosphate Pesticide Wastewater Discharge Standards, November, 2008 [in Chinese] <http://www.zhb.gov.cn/>. (accessed 24 November 2008).

  37. Rupa DS, Reddy PP, Reddi OS . Reproductive performance in population exposed to pesticides in cotton fields in India. Environ Res 1991; 55: 123–128.

    Article  CAS  Google Scholar 

  38. Bell EM, Hertz-Picciotto I, Beaumont JJ . A case-control study of pesticides and fetal death due to congenital anomalies. Epidemiology 2001; 12: 148–156.

    Article  CAS  Google Scholar 

  39. Koureas M, Tsakalof A, Tsatsakis A, Hadjichristodoulou C . Systematic review of biomonitoring studies to determine the association between exposure to organophosphorus and pyrethroid insecticides and human health outcomes. Toxicol Lett 2012; 210: 155–168.

    Article  CAS  Google Scholar 

  40. Berkowitz GS, Wetmur JG, Birman-Deych E, Obel J, Lapinski RH, Godbold JH et al. In utero pesticide exposure, maternal paraoxonase activity, and head circumference. Environ Health Perspect 2004; 112: 388–391.

    Article  Google Scholar 

  41. Ross MK, Borazjani A, Edwards CC, Potter PM . Hydrolytic metabolism of pyrethroids by human and other mammalian carboxylesterases. Biochem Pharmacol 2006; 71: 657–669.

    Article  CAS  Google Scholar 

  42. Cantalamessa F . Acute toxicity of two pyrethroids, permethrin, and cypermethrin in neonatal and adult rats. Arch Toxicol 1993; 67: 510–513.

    Article  CAS  Google Scholar 

  43. Burns CJ, McIntosh LJ, Mink PJ, Jurek AM, Li AA . Pesticide exposure and neurodevelopmental outcomes: review of the epidemiologic and animal studies. J Toxicol Environ Health B Crit Rev 2013; 16: 127–283.

    Article  CAS  Google Scholar 

  44. Hildebrand ME, McRory JE, Snutch TP, Stea A . Mammalian voltage-gated calcium channels are potently blocked by the pyrethroid insecticide allethrin. J Pharmacol Exp Ther 2004; 308: 805–813.

    Article  CAS  Google Scholar 

  45. Crofton KM, Reiter LW . Pyrethroid insecticides and the gamma-aminobutyric acidA receptor complex: motor activity and the acoustic startle response in the rat. J Pharmacol Exp Ther 1987; 243: 946–954.

    CAS  PubMed  Google Scholar 

  46. Breckenridge CB, Holden L, Sturgess N, Weiner M, Sheets L, Sargent D et al. Evidence for a separate mechanism of toxicity for the Type I and the Type II pyrethroid insecticides. Neurotoxicology 2009; 30: S17–S31.

    Article  CAS  Google Scholar 

  47. Ding G, Wang P, Tian Y, Zhang J, Gao Y, Wang X et al. Organophosphate pesticide exposure and neurodevelopment in young Shanghai children. Environ Sci Technol 2012; 46: 2911–2917.

    Article  CAS  Google Scholar 

  48. Whyatt RM, Rauh V, Barr DB, Camann DE, Andrews HF, Garfinkel R et al. Prenatal insecticide exposures and birth weight and length among an urban minority cohort. Environ Health Perspect 2004; 112: 1125–1132.

    Article  CAS  Google Scholar 

  49. Kemmeren JM, van Poppel G, Verhoef P, Jarvis MJ . Plasma cotinine: stability in smokers and validation of self-reported smoke exposure in nonsmokers. Environ Res 1994; 66: 235–243.

    Article  CAS  Google Scholar 

  50. Woodward M, Tunstall-Pedoe H, Smith WC, Tavendale R . Smoking characteristics and inhalation biochemistry in the Scottish population. J Clin Epidemiol 1991; 44: 1405–1410.

    Article  CAS  Google Scholar 

  51. Eskenazi B, Harley K, Bradman A, Weltzien E, Jewell NP, Barr DB et al. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 2004; 112: 1116–1124.

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledge the Department of Environmental Health staff, students, hospital partners, participants, and families without whom this study would have not been possible. We specifically thank Guoquan Wang and Chao Feng (CDC, Shanghai) for their work on specimen management and pyrethroid insecticide measurement. This research was partially supported by the Natural Science Foundation of China (Grant No. 81172625 and 81402645) and the Key Discipline Construction Project of Shanghai Municipal Public Health (Grant No. 12GWZX0401).

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  1. MOE and Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Guodong Ding & Ying Tian

  2. Department of Environmental Health, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Chang Cui, Limei Chen, Yu Gao, Yijun Zhou, Rong Shi & Ying Tian

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  1. Guodong Ding
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Correspondence to Ying Tian.

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Ding, G., Cui, C., Chen, L. et al. Prenatal exposure to pyrethroid insecticides and birth outcomes in Rural Northern China. J Expo Sci Environ Epidemiol 25, 264–270 (2015). https://doi.org/10.1038/jes.2014.86

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