Advertisement

Environmental Chemistry Letters

, Volume 16, Issue 4, pp 1377–1391 | Cite as

Toxicity of the pyrethroid bifenthrin insecticide

  • Ye Yang
  • Nanxiang Wu
  • Chunlei Wang
Review
  • 106 Downloads

Abstract

Bifenthrin is a chiral synthetic pyrethroid insecticide that has been commonly used for agricultural and domestic pest control over the past decades. Due to its widespread application, residues of bifenthrin has been frequently detected in environmental media, residential areas and biota, thus posing potential risks to the health of wildlife and humans. In particular, bifenthrin exhibits high acute lethal toxicity to aquatic species, and it is the primary contributor to the toxicity of insecticides in waters. Additionally, bifenthrin can also cause sublethal toxic effects on various non-target organisms, including developmental toxicity, neurobehavioral toxicity, oxidative damage, immune toxicity and endocrine disrupting effects. Here we review recent studies about the fate of bifenthrin in the environment and biological systems, the toxicity of the chiral parent compound bifenthrin and the toxic effects of main metabolites. The adverse effects of bifenthrin, identified from both in vitro and in vivo studies, and the potential underlying mechanisms are presented. We discuss the enantiomeric difference in the toxicological effects of bifenthrin, since enantiomers of chiral compounds show different interactions with biological systems. Pyrethroid insecticides metabolites are not acutely toxic, but they have sublethal toxicity, such as endocrine disrupting effects and immunotoxicity. We provide emerging evidence for toxic effects of several main metabolites.

Keywords

Chiral synthetic pyrethroids Bifenthrin Environmental fate Biotransformation Toxicological effects Enantioselectivity 

Notes

Acknowledgements

This work was supported by Zhejiang Provincial Natural Science Foundation of China (LY17B070009) and Zhejiang Provincial Science and Technology Program (2017F30003) and Zhejiang Medical and Health Science and Technology Project (2017KY036).

References

  1. Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaiee A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10(6):RA141–RA147.  https://doi.org/10.20455/ros.2017.823 Google Scholar
  2. Abdou R, Sasaki K, Khalil W, Shah S, Murasawa Y, Shimoda M (2010) Effects of several pyrethroids on hepatic cytochrome p450 activities in rats. J Vet Med Sci 72(4):425–433.  https://doi.org/10.1292/jvms.09-0347 Google Scholar
  3. Allinson G, Zhang P, Bui AD, Allinson M, Rose G, Marshall S, Pettigrove V (2015) Pesticide and trace metal occurrence and aquatic benchmark exceedances in surface waters and sediments of urban wetlands and retention ponds in Melbourne. Aust Environ Sci Pollut Res Int 22(13):10214–10226.  https://doi.org/10.1007/s11356-015-4206-3 Google Scholar
  4. Beggel S, Werner I, Connon RE, Geist JP (2010) Sublethal toxicity of commercial insecticide formulations and their active ingredients to larval fathead minnow (Pimephales promelas). Sci Total Environ 408(16):3169–3175.  https://doi.org/10.1016/j.scitotenv.2010.04.004 Google Scholar
  5. Beggel S, Connon R, Werner I, Geist J (2011) Changes in gene transcription and whole organism responses in larval fathead minnow (Pimephales promelas) following short-term exposure to the synthetic pyrethroid bifenthrin. Aquat Toxicol 105(1–2):180–188.  https://doi.org/10.1016/j.aquatox.2011.06.004 Google Scholar
  6. Berkowitz GS, Obel J, Deych E, Lapinski R, Godbold J, Liu ZS, Landrigan PJ, Wolff MS (2003) Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ Health Perspect 111(1):79–84.  https://doi.org/10.1289/ehp.5619 Google Scholar
  7. Bertotto LB, Richards J, Gan J, Volz DC, Schlenk D (2017) Effects of bifenthrin exposure on the estrogenic and dopaminergic pathways in zebrafish embryos and juveniles. Environ Toxicol Chem 37(1):236–246.  https://doi.org/10.1002/etc.3951 Google Scholar
  8. Bradbury SP, Coats JR (1989) Comparative toxicology of the pyrethroid insecticides. Rev Environ Contam Toxicol 108:133–177.  https://doi.org/10.1007/978-1-4613-8850-0_4 Google Scholar
  9. Brander SM, He G, Smalling KL, Denison MS, Cherr GN (2012) The in vivo estrogenic and in vitro anti-estrogenic activity of permethrin and bifenthrin. Environ Toxicol Chem 31(12):2848–2855.  https://doi.org/10.1002/etc.2019 Google Scholar
  10. Brander SM, Jeffries KM, Cole BJ, DeCourten BM, WilsonWhite J, Hasenbein S, Fangue NA, Connon RE (2016) Transcriptomic changes underlie altered egg protein production and reduced fecundity in an estuarine model fish exposed to bifenthrin. Aquat Toxicol 174:247–260.  https://doi.org/10.1016/j.aquatox.2016.02.014 Google Scholar
  11. Burr SA, Ray DE (2004) Structure-activity and interaction effects of 14 different pyrethroids on voltage-gated chloride ion channels. Toxicol Sci 77(2):341–346.  https://doi.org/10.1093/toxsci/kfh027 Google Scholar
  12. Cao Z, Shafer TJ, Murray TF (2011) Mechanisms of pyrethroid insecticide-induced stimulation of calcium influx in neocortical neurons. J Pharmacol Exp Ther 336(1):197–205.  https://doi.org/10.1124/jpet.110.171850 Google Scholar
  13. Chang J, Wang Y, Wang H, Li J, Xu P (2016) Bioaccumulation and enantioselectivity of type I and type II pyrethroid pesticides in earthworm. Chemosphere 144:1351–1357.  https://doi.org/10.1016/j.chemosphere.2015.10.011 Google Scholar
  14. Colborn T, vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101(5):378–384.  https://doi.org/10.1289/ehp.93101378 Google Scholar
  15. Crago J, Schlenk D (2015) The effect of bifenthrin on the dopaminergic pathway in juvenile rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 162:66–72.  https://doi.org/10.1016/j.aquatox.2015.03.005 Google Scholar
  16. Dai PL, Wang Q, Sun JH, Liu F, Wang X, Wu YY, Zhou T (2010) Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environ Toxicol Chem 29(3):644–649.  https://doi.org/10.1002/etc.67 Google Scholar
  17. Dar MA, Khan AM, Raina R, Verma PK, Sultana M (2013) Effect of repeated oral administration of bifenthrin on lipid peroxidation and anti-oxidant parameters in Wistar rats. Bull Environ Contam Toxicol 91(1):125–128.  https://doi.org/10.1007/s00128-013-1022-7 Google Scholar
  18. Dasgupta N, Ramalingam C (2016) Silver nanoparticle antimicrobial activity explained by membrane rupture and reactive oxygen generation. Environ Chem Lett 14:477–485.  https://doi.org/10.1007/s10311-016-0583-1 Google Scholar
  19. de la Torre FR, Ferrari L, Salibián A (2002) Freshwater pollution biomarker: response of brain acetylcholinesterase activity in two fish species. Comp Biochem Physiol C Toxicol Pharmacol 131(3):271–280.  https://doi.org/10.1016/s1532-0456(02)00014-5 Google Scholar
  20. DeGroot BC, Brander SM (2014) The role of P450 metabolism in the estrogenic activity of bifenthrin in fish. Aquat Toxicol 156:17–20.  https://doi.org/10.1016/j.aquatox.2014.07.007 Google Scholar
  21. DeMicco A, Cooper KR, Richardson JR, White LA (2010) Developmental neurotoxicity of pyrethroid insecticides in zebrafish embryos. Toxicol Sci 113(1):177–186.  https://doi.org/10.1093/toxsci/kfp258 Google Scholar
  22. Dobsíková R, Velísek J, Wlasow T, Gomulka P, Svobodová Z, Novotný L (2006) Effects of cypermethrin on some haematological, biochemical and histopathological parameters of common carp (Cyprinus carpio L.). Neuro Endocrinol Lett 27(Suppl 2):91–95.  https://doi.org/10.1007/s10695-008-9258-6 Google Scholar
  23. Dong MH (1995) Human pesticide exposure assessment (for section 3 new product/use registration) bifenthrin. EPA, California. http://www.cdpr.ca.gov/docs/whs/pdf/hs1722.pdf
  24. Đorđević TM, Šiler-Marinković SS, Đurović RD, Dimitrijević-Branković SI, Gajić Umiljendić JS (2013) Stability of the pyrethroid pesticide bifenthrin in milled wheat during thermal processing, yeast and lactic acid fermentation, and storage. J Sci Food Agric 93(13):3377–3383.  https://doi.org/10.1002/jsfa.6188 Google Scholar
  25. Du G, Shen O, Sun H, Fei J, Lu C, Song L, Xia Y, Wang S, Wang X (2010) Assessing hormone receptor activities of pyrethroid insecticides and their metabolites in reporter gene assays. Toxicol Sci 116(1):58–66.  https://doi.org/10.1093/toxsci/kfq120 Google Scholar
  26. Forsgren KL, Riar N, Schlenk D (2013) The effects of the pyrethroid insecticide, bifenthrin, on steroid hormone levels and gonadal development of steelhead (Oncorhynchus mykiss) under hypersaline conditions. Gen Comp Endocrinol 186:101–107.  https://doi.org/10.1016/j.ygcen.2013.02.047 Google Scholar
  27. Forshaw PJ, Lister T, Ray DE (1993) Inhibition of a neuronal voltage-dependent chloride channel by the type II pyrethroid, deltamethrin. Neuropharmacology 32(2):105–111.  https://doi.org/10.1016/0028-3908(93)90089-l Google Scholar
  28. Forshaw PJ, Lister T, Ray DE (2000) The role of voltage-gated chloride channels in type II pyrethroid insecticide poisoning. Toxicol Appl Pharmacol 163(1):1–8.  https://doi.org/10.1006/taap.1999.8848 Google Scholar
  29. Gammon DW, Chandrasekaran A, ElNaggar SF (2012) Comparative metabolism and toxicology of pyrethroids in mammals. In: Marrs T (ed) Mammalian toxicology of insecticides. Royal Society of Chemistry Press, Cambridge, pp 137–183.  https://doi.org/10.1039/9781849733007-00137 Google Scholar
  30. Gammon D, Liu Z, Chandrasekaran A, ElNaggar S (2015) The pharmacokinetic properties of bifenthrin in the rat following multiple routes of exposure. Pest Manag Sci 71(6):835–841.  https://doi.org/10.1002/ps.3883 Google Scholar
  31. Gan J, Lee SJ, Liu WP, Haver DL, Kabashima JN (2005) Distribution and persistence of pyrethroids in runoff sediments. J Environ Qual 34(3):836–841.  https://doi.org/10.2134/jeq2004.0240 Google Scholar
  32. Gilbreath AN, McKee LJ (2015) Concentrations and loads of PCBs, dioxins, PAHs, PBDEs, OC pesticides and pyrethroids during storm and low flow conditions in a small urban semi-arid watershed. Sci Total Environ 526:251–261.  https://doi.org/10.1016/j.scitotenv.2015.04.052 Google Scholar
  33. Glickman AH, Lech JJ (1981) Hydrolysis of permethrin, a pyrethroid insecticide, by rainbow trout and mouse tissues in vitro: a comparative study. Toxicol Appl Pharmacol 60(2):186–192.  https://doi.org/10.1016/0041-008x(91)90222-z Google Scholar
  34. Godin SJ, Crow JA, Scollon EJ, Hughes MF, DeVito MJ, Ross MK (2007) Identification of rat and human cytochrome p450 isoforms and a rat serum esterase that metabolize the pyrethroid insecticides deltamethrin and esfenvalerate. Drug Metab Dispos 35(9):1664–1671.  https://doi.org/10.1124/dmd.107.015388 Google Scholar
  35. Hadnagy W, Leng G, Sugiri D, Ranft U, Idel H (2003) Pyrethroids used indoors–immune status of humans exposed to pyrethroids following a pest control operation—a one year follow-up study. Int J Hyg Environ Health 206(2):93–102.  https://doi.org/10.1078/1438-4639-00201 Google Scholar
  36. Hall LW, Anderson RD (2014) Spatial analysis of bifenthrin sediment concentrations in California waterbodies from 2001 to 2010: identification of toxic and non-toxic areas. Hum Ecol Risk Assess Int J 20(2):497–509.  https://doi.org/10.1080/10807039.2012.743434 Google Scholar
  37. Han Y, Xia Y, Han J, Zhou J, Wang S, Zhu P, Zhao R, Jin N, Song L, Wang X (2008) The relationship of 3-PBA pyrethroids metabolite and male reproductive hormones among non-occupational exposure males. Chemosphere 72(5):785–790.  https://doi.org/10.1016/j.chemosphere.2008.03.058 Google Scholar
  38. Harper HE, Pennington PL, Hoguet J, Fulton MH (2008) Lethal and sublethal effects of the pyrethroid, bifenthrin, on grass shrimp (Palaemonetes pugio) and sheepshead minnow (Cyprinodon variegatus). J Environ Sci Health B 43(6):476–483.  https://doi.org/10.1080/03601230802174599 Google Scholar
  39. Hladik ML, Kuivila KM (2012) Pyrethroid insecticides in bed sediments from urban and agricultural streams across the United States. J Environ Monit 14(7):1838–1845.  https://doi.org/10.1039/c2em10946h Google Scholar
  40. Jeppe KJ, Kellar CR, Marshall S, Colombo V, Sinclair GM, Pettigrove V (2017) Bifenthrin causes toxicity in urban stormwater wetlands: field and laboratory assessment using Austrochiltonia (Amphipoda). Environ Sci Technol 51(12):7254–7262.  https://doi.org/10.1021/acs.est.7b01472 Google Scholar
  41. Jin M, Zhang X, Wang L, Huang C, Zhang Y, Zhao M (2009) Developmental toxicity of bifenthrin in embryo-larval stages of zebrafish. Aquat Toxicol 95(4):347–354.  https://doi.org/10.1016/j.aquatox.2009.10.003 Google Scholar
  42. Jin M, Zhang Y, Ye J, Huang C, Zhao M, Liu W (2010a) Dual enantioselective effect of the insecticide bifenthrin on locomotor behavior and development in embryonic-larval zebrafish. Environ Toxicol Chem 29(7):1561–1567.  https://doi.org/10.1002/etc.190 Google Scholar
  43. Jin MQ, Li L, Xu C, Wen Y, Zhao M (2010b) Estrogenic activities of two synthetic pyrethroids and their metabolites. J Environ Sci 22(2):290–296.  https://doi.org/10.1016/s1001-0742(09)60107-8 Google Scholar
  44. Jin Y, Pan X, Cao L, Ma B, Fu Z (2013a) Embryonic exposure to cis-bifenthrin enantioselectively induces the transcription of genes related to oxidative stress, apoptosis and immunotoxicity in zebrafish (Danio rerio). Fish Shellfish Immun 34(2):717–723.  https://doi.org/10.1016/j.fsi.2012.11.046 Google Scholar
  45. Jin Y, Wang J, Sun X, Ye Y, Xu M, Wang J, Chen S, Fu Z (2013b) Exposure of maternal mice to cis-bifenthrin enantioselectively disrupts the transcription of genes related to testosterone synthesis in male offspring. Reprod Toxicol 42:156–163.  https://doi.org/10.1016/j.reprotox.2013.08.006 Google Scholar
  46. Jin Y, Pan X, Fu Z (2014) Exposure to bifenthrin causes immunotoxicity and oxidative stress in male mice. Environ Toxicol 29(9):991–999.  https://doi.org/10.1002/tox.21829 Google Scholar
  47. Jin Y, Wang J, Pan X, MiaoW Lin X, Wang L, Fu Z (2015) Enantioselective disruption of the endocrine system by Cis-Bifenthrin in the male mice. Environ Toxicol 30(7):746–754.  https://doi.org/10.1002/tox.21954 Google Scholar
  48. Khan AM, Sultana M, Raina R, Dubey N, Verma PK (2013a) Effect of sub-acute oral exposure of bifenthrin on biochemical parameters in crossbred goats. Proc Natl Acad Sci India Sect B Biol Sci 83(3):323–328.  https://doi.org/10.1007/s40011-012-0150-x Google Scholar
  49. Khan AM, Sultana M, Raina R, Dubey N, Dar SA (2013b) Effect of sub-acute toxicity of bifenthrin on antioxidant status and hematology after its oral exposure in goats. Proc Natl Acad Sci, India, Sect B Biol Sci 83(4):545–549.  https://doi.org/10.1007/s40011-013-0157-y Google Scholar
  50. Kumari B, Kumar V, Sinha AK, Ahsan J, Ghosh AK, Wang H, DeBoeck G (2017) Toxicology of arsenic in fish and aquatic systems. Environ Chem Lett 15:43–64.  https://doi.org/10.1007/s10311-016-0588-9 Google Scholar
  51. Laskowski DA (2002) Physical and chemical properties of pyrethroids. In: Ware GW (ed) Reviews of environmental contamination and toxicology. Springer, New York, pp 47–170.  https://doi.org/10.1007/978-1-4757-4260-2_3 Google Scholar
  52. Lee S, Gan J, Kim JS, Kabashima JN, Crowley DE (2004) Microbial transformation of pyrethroid insecticides in aqueous and sediment phases. Environ Toxicol Chem 23(1):1–6.  https://doi.org/10.1897/03-114 Google Scholar
  53. Li L, Yang D, Song Y, Shi Y, Huang B, Yan J, Dong X (2017a) Effects of bifenthrin exposure in soil on whole-organism endpoints and biomarkers of earthworm Eisenia fetida. Chemosphere 168:41–48.  https://doi.org/10.1016/j.chemosphere.2016.10.060 Google Scholar
  54. Li JS, Luo F, Liu L, Ruan J, Wang N (2017b) Exposure to bifenthrin disrupts the development of testis in male Sebastiscus marmoratus. Acta Oceanol Sin 36(2):57–61.  https://doi.org/10.1007/s13131-017-1001-7 Google Scholar
  55. Li C, Cao M, Ma L, Ye X, Song Y, Pan W, Xu Z, Ma X, Lan Y, Chen P, Liu W, Liu J, Zhou J (2018a) Pyrethroid pesticide exposure and risk of primary ovarian insufficiency in Chinese women. Environ Sci Technol 52(5):3240–3248.  https://doi.org/10.1021/acs.est.7b06689 Google Scholar
  56. Li F, Ma H, Liu J (2018b) Pyrethroid insecticide cypermethrin modulates gonadotropin synthesis via calcium homeostasis and erk1/2 signaling in lbetat2 mouse pituitary cells. Toxicol Sci 162(1):43–52.  https://doi.org/10.1093/toxsci/kfx248 Google Scholar
  57. Liu W, Gan J, Schlenk D, Jury WA (2005a) Enantioselectivity in environmental safety of current chiral insecticides. Proc Natl Acad Sci USA 102(3):701–706.  https://doi.org/10.1073/pnas.0408847102 Google Scholar
  58. Liu W, Gan J, Lee S, Werner I (2005b) Isomer selectivity in aquatic toxicity and biodegradation of bifenthrin and permethrin. Environ Toxicol Chem 24(8):1861–1866.  https://doi.org/10.1897/04-457r.1 Google Scholar
  59. Liu W, Gan J, Qin S (2005c) Separation and aquatic toxicity of enantiomers of synthetic pyrethroid insecticides. Chirality 17(Suppl):127–133.  https://doi.org/10.1002/chir.20122 Google Scholar
  60. Liu J, Yang Y, Zhuang S, Yang Y, Li F, Liu W (2011) Enantioselective endocrine-disrupting effects of bifenthrin on hormone synthesis in rat ovarian cells. Toxicology 290(1):42–49.  https://doi.org/10.1016/j.tox.2011.08.016 Google Scholar
  61. Lu X (2013) Enantioselective effect of bifenthrin on antioxidant enzyme gene expression and stress protein response in PC12 cells. J Appl Toxicol 33(7):586–592.  https://doi.org/10.1002/jat.1774 Google Scholar
  62. Lu C, Barr DB, Pearson MA, Walker LA, Bravo R (2009) The attribution of urban and suburban children’s exposure to synthetic pyrethroid insecticides: a longitudinal assessment. J Expo Sci Environ Epidemiol 19(1):69–78.  https://doi.org/10.1038/jes.2008.49 Google Scholar
  63. Lund AE, Narahashi T (1982) Dose-dependent interaction of the pyrethroid isomers with sodium channels of squid axon membranes. Neurotoxicology 3(1):11–24Google Scholar
  64. McCarthy AR, Thomson BM, Shaw IC, Abell AD (2006) Estrogenicity of pyrethroid insecticide metabolites. J Environ Monit 8(1):197–202.  https://doi.org/10.1039/b511209e Google Scholar
  65. Meeker JD, Barr DB, Hauser R (2008) Human semen quality and sperm DNA damage in relation to urinary metabolites of pyrethroid insecticides. Hum Reprod 23(8):1932–1940.  https://doi.org/10.1093/humrep/den242 Google Scholar
  66. Mohapatra S, Ahuja AK (2009) Effect of moisture and soil type on the degradation of bifenthrin in soil. Pestic Res J 21(2):191–194Google Scholar
  67. Moyle PB (1976) Inland fisheries of California. University of California, Berkeley.  https://doi.org/10.2307/1443539 Google Scholar
  68. Muller-Mohnssen H (1999) Chronic sequelae and irreversible injuries following acute pyrethroid intoxication. Toxicol Lett 107(1–3):161–176.  https://doi.org/10.1016/s0378-4274(99)00043-0 Google Scholar
  69. Nallani GC, Chandrasekaran A, Kassahun K, Shen L, ElNaggar SF, Liu Z (2018) Age dependent in vitro metabolism of bifenthrin in rat and human hepatic microsomes. Toxicol Appl Pharmacol 338:65–72.  https://doi.org/10.1016/j.taap.2017.11.010 Google Scholar
  70. Nandi A, Chandil D, Lechesa R, Pryor SC, McLaughlin A, Bonventre JA, Flynn K, Weeks BS (2006) Bifenthrin causes neurite retraction in the absence of cell death: a model for pesticide associated neurodegeneration. Med Sci Monit 12(5):BR169–BR173Google Scholar
  71. Oros DR, Werner I (2005) Pyrethroid insecticides: an analysis of use patterns, distributions, potential toxicity and fate in the Sacramento–San Joaquin Delta and Central Valley. In: White paper for the interagency ecological program. SFEI Contribution 415. San Francisco Estuary Institute, OaklandGoogle Scholar
  72. Pennington PL, Harper-Laux H, Sapozhnikova Y, Fulton MH (2014) Environmental effects and fate of the insecticide bifenthrin in a salt-marsh mesocosm. Chemosphere 112:18–25.  https://doi.org/10.1016/j.chemosphere.2014.03.047 Google Scholar
  73. Phillips BM, Anderson BS, Hunt JW, Siegler K, Voorhees JP, Tjeerdema RS, McNeill K (2012) Pyrethroid and organophosphate pesticide-associated toxicity in two coastal watersheds (California, USA). Environ Toxicol Chem 31(7):1595–1603.  https://doi.org/10.1002/etc.1860 Google Scholar
  74. Qin S, Budd R, Bondarenko S, Liu W, Gan J (2006) Enantioselective degradation and chiral stability of pyrethroids in soil and sediment. J Agric Food Chem 54(14):5040–5045.  https://doi.org/10.1021/jf060329p Google Scholar
  75. Quirós-Alcalá L, Bradman A, Nishioka M, Harnly ME, Hubbard A, McKone TE, Ferber J, Eskenazi B (2011) Pesticides in house dust from urban and farmworker households in California: an observational measurement study. Environ Health 10:19–33.  https://doi.org/10.1186/1476-069x-10-19 Google Scholar
  76. Ranjan S, Ramalingam C (2016) Titanium dioxide nanoparticles induce bacterial membrane rupture by reactive oxygen species generation. Environ Chem Lett 14:487–494.  https://doi.org/10.1007/s10311-016-0586-y Google Scholar
  77. Ray DE, Fry JR (2006) A reassessment of the neurotoxicity of pyrethroid insecticide. Pharmacol Ther 111(1):174–193.  https://doi.org/10.1016/j.pharmthera.2005.10.003 Google Scholar
  78. Ren Q, Zhang T, Li S, Ren Z, Yang M, Pan H, Xu S, Qi L, Chon TS (2016) Integrative characterization of toxic response of zebrafish (Danio rerio) to deltamethrin based on AChE activity and behavior strength. Biomed Res Int 2016:1–10.  https://doi.org/10.1155/2016/7309184 Google Scholar
  79. Riah W, Laval K, Laroche-Ajzenberg E, Mougin C, Latour X, Trinsoutrot-Gattin I (2014) Effects of pesticides on soil enzymes: a review. Environ Chem Lett 12:257–273.  https://doi.org/10.1007/s10311-014-0458-2 Google Scholar
  80. Ricking M, Schwarzbauer J (2012) DDT isomers and metabolites in the environment: an overview. Environ Chem Lett 10:317–323.  https://doi.org/10.1007/s10311-012-0358-2 Google Scholar
  81. Saglio P, Trijasse S (1998) Behavioral responses to atrazine and diuron in goldfish. Arch Environ Contam Toxicol 35:484–491.  https://doi.org/10.1007/s002449900406 Google Scholar
  82. Saka WA, Akhigbe RE, Azeez OM, Babatunde TR (2011) Effects of pyrethroid insecticide exposure on haematological and haemostatic profiles in rats. Pak J Biol Sci 14(22):1024–1027.  https://doi.org/10.3923/pjbs.2011.1024.1027 Google Scholar
  83. Scollon EJ, Starr JM, Godin SJ, DeVito MJ, Hughes MF (2009) In vitro metabolism of pyrethroid pesticides by rat and human hepatic microsomes and cytochrome p450 isoforms. Drug Metab Dispos 37(1):221–228.  https://doi.org/10.1124/dmd.108.022343 Google Scholar
  84. Scollon EJ, Starr JM, Crofton KM, Wolansky MJ, DeVito MJ, Hughes MF (2011) Correlation of tissue concentrations of the pyrethroid bifenthrin with neurotoxicity in the rat. Toxicology 290(1):1–6.  https://doi.org/10.1016/j.tox.2011.08.002 Google Scholar
  85. Sheets LP (2000) A consideration of age-dependent differences in susceptibility to organophosphorus and pyrethroid insecticides. Neurotoxicology 21(1–2):57–63Google Scholar
  86. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254.  https://doi.org/10.1007/s10311-013-0407-5 Google Scholar
  87. Singh S, Singh N, Kumar V, Datta S, Wani AB, Singh D, Singh K, Singh J (2016) Toxicity, monitoring and biodegradation of the fungicide carbendazim. Environ Chem Lett. 14(3):317–329.  https://doi.org/10.1007/s10311-016-0566-2 Google Scholar
  88. Singh S, Kumar V, Chauhan A, Datta S, Wani AB, Singh N, Singh J (2018) Toxicity, degradation and analysis of the herbicide atrazine. Environ Chem Lett 16(1):211–237.  https://doi.org/10.1007/s10311-017-0665-8 Google Scholar
  89. Skandrani D, Gaubin Y, Vincent C, Beau B, Claude Murat J, Soleilhavoup JP, Croute F (2006) Relationship between toxicity of selected insecticides and expression of stress proteins (HSP, GRP) in cultured human cells: effects of commercial formulations versus pure active molecules. Biochim Biophys Acta 1760(1):95–103.  https://doi.org/10.1016/j.bbagen.2005.09.015 Google Scholar
  90. Slaninova A, Smutna M, Modra H, Svobodova Z (2009) A review: oxidative stress in fish induced by pesticides. Neuro Endocrinol Lett 30(Suppl 1):2–12Google Scholar
  91. Soderlund DM (1985) Pyrethroid-receptor interactions: stereospecific binding and effects on sodium channels in mouse brain preparations. Neurotoxicology 6(2):35–46Google Scholar
  92. Soderlund DM (2012) Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch Toxicol 86(2):165–181.  https://doi.org/10.1007/s00204-011-0726-x Google Scholar
  93. Soderlund DM, Casida JE (1977) Effects of pyrethroid structure on rates of hydrolysis and oxidation by mouse liver microsomal enzymes. Pestic Biochem Physiol 7:391–401.  https://doi.org/10.1016/0048-3575(77)90043-8 Google Scholar
  94. Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, Stevens JT, Weiner ML (2002) Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 171(1):3–59.  https://doi.org/10.1016/s0300-483x(01)00574-1 Google Scholar
  95. Stehle S, Schulz R (2015) Agricultural insecticides threaten surface waters at the global scale. Proc Natl Acad Sci USA 112(18):5750–5755.  https://doi.org/10.1073/pnas.1500232112 Google Scholar
  96. Sun H, Xu X, Xu L, Song L, Hong X, Chen J, Cui L, Wang X (2007) Antiandrogenic activity of pyrethroid pesticides and their metabolite in reporter gene assay. Chemosphere 66(3):474–479.  https://doi.org/10.1016/j.chemosphere.2006.05.059 Google Scholar
  97. Sun H, Chen W, Xu X, Ding Z, Chen X, Wang X (2014) Pyrethroid and their metabolite, 3-phenoxybenzoic acid showed similar (anti)estrogenic activity in human and rat estrogen receptor alpha-mediated reporter gene assays. Environ Toxicol Pharmacol 37(1):371–377.  https://doi.org/10.1016/j.etap.2013.11.031 Google Scholar
  98. Syed F, John PJ, Soni I (2016) Neurodevelopmental consequences of gestational and lactational exposure to pyrethroids in rats. Environ Toxicol 31(12):1761–1770.  https://doi.org/10.1002/tox.22178 Google Scholar
  99. Tran V, Hoffman N, Mofunanaya A, Pryor S, Ojugbele O, McLaughlin A, Gibson L, Bonventre JA, Flynn K, Weeks B (2006) Bifenthrin inhibits neurite outgrowth in differentiating PC12 cells. Med Sci Monit 12(2):BR57–BR62Google Scholar
  100. 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 Google Scholar
  101. Tu W, Lu B, Niu L, Xu C, Lin C, Liu W (2014) Dynamics of uptake and elimination of pyrethroid insecticides in zebrafish (Danio rerio) eleutheroembryos. Ecotoxicol Environ Saf 107:186–191.  https://doi.org/10.1016/j.ecoenv.2014.05.013 Google Scholar
  102. USEPA, United States Environmental Protection Agency (1997) Special report on environmental endocrine disruption: an effect assessment and analysis. EPA/630/R-96/012. USEPA, Washington, DCGoogle Scholar
  103. Velisek J, Svobodova Z, Machova J (2009a) Effects of bifenthrin on some haematological, biochemical and histopathological parameters of common carp (Cyprinus carpio L.). Fish Physiol Biochem 35(4):583–590.  https://doi.org/10.1007/s10695-008-9258-6 Google Scholar
  104. Velisek J, Svobodova Z, Piackova V (2009b) Effects of acute exposure to bifenthrin on some haematological, biochemical and histopathological parameters of rainbow trout (Oncorhynchus mykiss). Vet Med 54(3):131–137.  https://doi.org/10.17221/15/2009-vetmed Google Scholar
  105. Velíšek J, Jurčíková J, Dobšíková R, Svobodováa Z, Piačková V, Máchová J, Novotný L (2007) Effects of deltamethrin on rainbow trout (Oncorhynchus mykiss). Environ Toxicol Pharmacol 23(3):297–301.  https://doi.org/10.1016/j.etap.2006.11.006 Google Scholar
  106. Wang L, Liu W, Yang C, Pan Z, Gan J, Xu C, Zhao M, Schlenk D (2007) Enantioselectivity in estrogenic potential and uptake of bifenthrin. Environ Sci Technol 41(17):6124–6128.  https://doi.org/10.1021/es070220d Google Scholar
  107. Wang X, Gao X, He B, Jin Y, Fu Z (2017) Cis-bifenthrin causes immunotoxicity in murine macrophages. Chemosphere 168:1375–1382.  https://doi.org/10.1016/j.chemosphere.2016.11.121 Google Scholar
  108. Wani AB, Chadar H, Wani AH, Singh S, Upadhyay N (2017) Salicylic acid to decrease plant stress. Environ Chem Lett 15:101–123.  https://doi.org/10.1007/s10311-016-0584-0 Google Scholar
  109. Weiner ML, Nemec M, Sheets L, Sargent D, Breckenridge C (2009) Comparative functional observational battery study of twelve commercial pyrethroid insecticides in male rats following acute oral exposure. Neurotoxicology 30(Suppl 1):S1–16.  https://doi.org/10.1016/j.neuro.2009.08.014 Google Scholar
  110. Werner I, Moran K (2008) Effects of pyrethroid insecticides on aquatic organisms. In: Gan J, Spurlock F, Hendley P, Weston DP (eds) Synthetic pyrethroids: occurrence and behavior in aquatic environments. ACS Symposium Series, vol 991. American Chemical Society, Washington, DC, pp 310–335.  https://doi.org/10.1021/bk-2008-0991.ch014
  111. Weston DP, Holmes RW, Lydy MJ (2009) Residential runoff as a source of pyrethroid pesticides to urban creeks. Environ Pollut 157(1):287–294.  https://doi.org/10.1016/j.envpol.2008.06.037 Google Scholar
  112. Weston DP, Asbell AM, Hecht SA, Scholz NL, Lydy MJ (2011) Pyrethroid insecticides in urban salmon streams of the Pacific Northwest. Environ Pollut 159(10):3051–3056.  https://doi.org/10.1016/j.envpol.2011.04.008 Google Scholar
  113. Weston DP, Ramil HL, Lydy MJ (2013) Pyrethroid insecticides in municipal wastewater. Environ Toxicol Chem 32(11):2460–2468.  https://doi.org/10.1002/etc.2338 Google Scholar
  114. Weston DP, Asbell AM, Lesmeister SA, The SJ, Lydy MJ (2014) Urban and agricultural pesticide inputs to a critical habitat for the threatened delta smelt (Hypomesus transpacificus). Environ Toxicol Chem 33(4):920–929.  https://doi.org/10.1002/etc.2512 Google Scholar
  115. WHO (2009) The WHO recommended classification of pesticides by hazard and guidelines to classification 2009. WHO, GenevaGoogle Scholar
  116. WHO, FAO (2010) Specifications and evaluations for agricultural pesticides: bifenthrin, food and agriculture organization of the United Nations and World Health Organization. Rome, pp 1–33Google Scholar
  117. Whyatt RM, Camann DE, Kinney PL, Reyes A, Ramirez J, Dietrich J, Diaz D, Holmes D, Perera FP (2002) Residential pesticide use during pregnancy among a cohort of urban minority women. Environ Health Perspect 110(5):507–514.  https://doi.org/10.1289/ehp.02110507 Google Scholar
  118. Wolansky MJ, Gennings C, Crofton KM (2006) Relative potencies for acute effects of pyrethroids on motor function in rats. Toxicol Sci 89(1):271–277.  https://doi.org/10.1093/toxsci/kfj020 Google Scholar
  119. Wolansky MJ, McDaniel KL, Moser VC, Crofton KM (2007) Influence of dosing volume on the neurotoxicity of bifenthrin. Neurotoxicol Teratol 29(3):377–384.  https://doi.org/10.1016/j.ntt.2007.01.007 Google Scholar
  120. Yadav RS, Srivastava HC, Adak T, Nanda N, Thapar BR, Pant CS, Zaim M, Subbarao SK (2003) House-scale evaluation of bifenthrin indoor residual spraying for malaria vector control in India. J Med Entomol 40(1):58–63.  https://doi.org/10.1603/0022-2585-40.1.58 Google Scholar
  121. Yang Y, Ma H, Zhou J, Liu J, Liu W (2014) Joint toxicity of permethrin and cypermethrin at sublethal concentrations to the embryo-larval zebrafish. Chemosphere 96:146–154.  https://doi.org/10.1016/j.chemosphere.2013.10.014 Google Scholar
  122. Yang Y, Ye X, He B, Liu J (2016) Cadmium potentiates toxicity of cypermethrin in zebrafish. Environ Toxicol Chem 35(2):435–445.  https://doi.org/10.1002/etc.3200 Google Scholar
  123. Yang Y, Ji D, Huang X, Zhang J, Liu J (2017a) Effects of metals on enantioselective toxicity and biotransformation of cis-bifenthrin in zebrafish. Environ Toxicol Chem 36(8):2139–2146.  https://doi.org/10.1002/etc.3747 Google Scholar
  124. Yang Y, Zhang J, Yao Y (2017b) Enantioselective effects of chiral pesticides on their primary targets and secondary targets. Curr Protein Pept Sci 18(1):22–32.  https://doi.org/10.2174/1389203717666160413124239 Google Scholar
  125. Ye X, Xiong K, Liu J (2016) Comparative toxicity and bioaccumulation of fenvalerate and esfenvalerate to earthworm Eisenia fetida. J Hazard Mater 310:82–88.  https://doi.org/10.1016/j.jhazmat.2016.02.010 Google Scholar
  126. Ye X, Li F, Zhang J, Ma H, Ji D, Huang X, Curry TE Jr, Liu W, Liu J (2017a) Pyrethroid insecticide cypermethrin accelerates pubertal onset in male mice via disrupting hypothalamic-pituitary-gonadal axis. Environ Sci Technol 51(17):10212–10221.  https://doi.org/10.1021/acs.est.7b02739 Google Scholar
  127. Ye X, Pan W, Zhao S, Zhao Y, Zhu Y, Liu J, Liu W (2017b) Relationships of pyrethroid exposure with gonadotropin levels and pubertal development in Chinese boys. Environ Sci Technol 51(11):6379–6386.  https://doi.org/10.1021/acs.est.6b05984 Google Scholar
  128. Ye X, Pan W, Zhao Y, Zhao S, Zhu Y, Liu W, Liu J (2017c) 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 Google Scholar
  129. Yousef MI, El-Demerdash FM, Kamel KI, AI-Salhen KS (2003) Changes in some hematological and biochemical indices of rabbits induced by isoflavones and cypermethrin. Toxicology 189(3):223–234.  https://doi.org/10.1016/s0300-483x(03)00145-8 Google Scholar
  130. Zhang J, Zhu W, Zheng Y, Yang J, Zhu X (2008) The antiandrogenic activity of pyrethroid pesticides cyfluthrin and beta-cyfluthrin. Reprod Toxicol 25(4):491–496.  https://doi.org/10.1016/j.reprotox.2008.05.054 Google Scholar
  131. Zhang Y, Zhao M, Jin M, Xu C, Wang C, Liu W (2010) Immunotoxicity of pyrethroid metabolites in an in vitro model. Environ Toxicol Chem 29(11):2505–2510.  https://doi.org/10.1002/etc.298 Google Scholar
  132. Zhang Y, Lu M, Zhou P, Wang C, Zhang Q, Zhao M (2015) Multilevel evaluations of potential liver injury of bifenthrin. Pestic Biochem Physiol 122:29–37.  https://doi.org/10.1016/j.pestbp.2014.12.028 Google Scholar
  133. Zhang J, Zhang J, Liu R, Gan J, Liu J, Liu W (2016) Endocrine-disrupting effects of pesticides through interference with human glucocorticoid receptor. Environ Sci Technol 50(1):435–443.  https://doi.org/10.1021/acs.est.5b03731 Google Scholar
  134. Zhang J, Huang X, Liu H, Liu W, Liu J (2018) Novel pathways of endocrine disruption through pesticides interference with human mineralocorticoid receptors. Toxicol Sci 162(1):53–63.  https://doi.org/10.1093/toxsci/kfx244 Google Scholar
  135. Zhao M, Wang C, Liu KK, Sun L, Li L, Liu W (2009) Enantioselectivity in chronic toxicology and accumulation of the synthetic pyrethroid insecticide bifenthrin in Daphnia magna. Environ Toxicol Chem 28(7):1475–1479.  https://doi.org/10.1897/08-527.1 Google Scholar
  136. Zhao M, Chen F, Wang C, Zhang Q, Gan J, Liu W (2010) Integrative assessment of enantioselectivity in endocrine disruption and immunotoxicity of synthetic pyrethroids. Environ Pollut 158(5):1968–1973.  https://doi.org/10.1016/j.envpol.2009.10.027 Google Scholar
  137. Zhou T, Zhou W, Wang Q, Dai P, Liu F, Zhang Y, Sun J (2011) Effects of pyrethroids on neuronal excitability of adult honeybees Apis mellifera. Pestic Biochem Phys 100(1):35–40.  https://doi.org/10.1016/j.pestbp.2011.02.001 Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of HygieneZhejiang Academy of Medical SciencesHangzhouChina

Personalised recommendations