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Pyrethroid pesticide exposure and hematological cancer: epidemiological, biological and molecular evidence

  • María del Pilar Navarrete-Meneses and Patricia Pérez-Vera EMAIL logo
Published/Copyright: March 23, 2019

Abstract

Pyrethroid insecticides are commonly used worldwide. The chronic effects of these compounds are of concern given that epidemiological studies have suggested an association with hematological cancer, particularly in children. However, the biological evidence at molecular and cellular levels is limited. A review on the molecular and cellular effects of pyrethroids is helpful to guide the study of the biological plausibility of the association of pyrethroids with hematological cancer. We reviewed studies suggesting that pyrethroids are genotoxic, induce genetic rearrangements, alter gene expression and modify DNA. All of these biological modifications could potentially contribute to the carcinogenic process in hematopoietic cells.


Corresponding author: Patricia Pérez-Vera, PhD, Cancer Genetics Laboratory, Human Genetics Department, National Pediatrics Institute, Insurgentes Sur 3700-C, C.P. 04530 Mexico City, Mexico, Phone: +52 55 1084090 ext. 1471

Acknowledgments

Financial support was provided by CONACyT CB-2012-01-183467 (P.P.-V.) and by National Pediatrics Institute. This article constitutes a partial fulfillment of the Graduate Program in Biological Sciences of the National Autonomous University of México (UNAM). María del Pilar Navarrete-Meneses acknowledges the scholarship and financial support provided by the National Council of Science and Technology (CONACyT) CVU 385279, and UNAM.

  1. Declaration of Interests: The authors report no declarations of interest.

References

1. 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(24):13480–7.10.1021/es303362aSearch in Google Scholar PubMed

2. Matthews G. Pesticides: health, safety and the environment. UK: John Wiley & Sons; 2008:249.Search in Google Scholar

3. Rossbach B, Appel KE, Mross KG, Letzel S. Uptake of permethrin from impregnated clothing. Toxicol Lett 2010;192(1):50–5.10.1016/j.toxlet.2009.06.863Search in Google Scholar PubMed

4. US EPA O of PP. About Pesticides | Pesticides | US EPA [Internet]. Available from: http://www.epa.gov/pesticides/about/.Search in Google Scholar

5. Pages from vector059to118-2.pdf – vector088to118.pdf [Internet]. Available from: http://www.who.int/water_sanitation_health/resources/vector088to118.pdf.Search in Google Scholar

6. Menegaux F, Baruchel A, Bertrand Y, Lescoeur B, Leverger G, Nelken B, et al. Household exposure to pesticides and risk of childhood acute leukaemia. Occup Environ Med 2006;63(2):131–4.10.1136/oem.2005.023036Search in Google Scholar PubMed PubMed Central

7. Palmquist K, Salatas J, Fairbrother A. Pyrethroid Insecticides: Use, Environmental Fate, and Ecotoxicology. In: Perveen F, editor. Insecticides – Advances in Integrated Pest Management [Internet]. InTech; 2012. Available from: http://www.intechopen.com/books/insecticides-advances-in-integrated-pest-management/pyrethroid-insecticides-use-environmental-fate-and-ecotoxicology.10.5772/29495Search in Google Scholar

8. Morgan MK. Children’s exposures to pyrethroid insecticides at home: a review of data collected in published exposure measurement studies conducted in the United States. Int J Environ Res Public Health 2012;9(8):2964–85.10.3390/ijerph9082964Search in Google Scholar PubMed PubMed Central

9. IARC Monographs Volume 53. IARC monograph [Internet]. 1990. Available from: http://monographs.iarc.fr/ENG/Monographs/vol53/mono53-13.pdf.Search in Google Scholar

10. Rusiecki JA, Patel R, Koutros S, Beane-Freeman L, Landgren O, Bonner MR, et al. Cancer incidence among pesticide applicators exposed to permethrin in the Agricultural Health Study. Environ Health Perspect 2009;117(4):581–6.10.1289/ehp.11318Search in Google Scholar PubMed PubMed Central

11. Turner MC, Wigle DT, Krewski D. Residential pesticides and childhood leukemia: a systematic review and meta-analysis. Ciênc Saúde Coletiva 2011;16(3):1915–31.10.1590/S1413-81232011000300026Search in Google Scholar

12. Merhi M, Raynal H, Cahuzac E, Vinson F, Cravedi JP, Gamet-Payrastre L. Occupational exposure to pesticides and risk of hematopoietic cancers: meta-analysis of case-control studies. Cancer Causes Control 2008;18(10):1209–26.10.1007/s10552-007-9061-1Search in Google Scholar PubMed

13. Boffetta P, Desai V. Exposure to permethrin and cancer risk: a systematic review. Crit Rev Toxicol 2018;48(6):433–42.10.1080/10408444.2018.1439449Search in Google Scholar PubMed

14. Herrera A, Barrueco C, Caballo C, de la Peña E. Effect of permethrin on the induction of sister chromatid exchanges and micronuclei in cultured human lymphocytes. Environ Mol Mutagen 1992;20(3):218–22.10.1002/em.2850200311Search in Google Scholar PubMed

15. Barrueco C, Herrera A, Caballo C, de la Peña E. Induction of structural chromosome aberrations in human lymphocyte cultures and CHO cells by permethrin. Teratog Carcinog Mutagen 1994;14(1):31–8.10.1002/tcm.1770140105Search in Google Scholar

16. Undeğer U, Başaran N. Effects of pesticides on human peripheral lymphocytes in vitro: induction of DNA damage. Arch Toxicol 2005;79(3):169–76.10.1007/s00204-004-0616-6Search in Google Scholar

17. Institóris L, Undeger U, Siroki O, Nehéz M, Dési I. Comparison of detection sensitivity of immuno- and genotoxicological effects of subacute cypermethrin and permethrin exposure in rats. Toxicology 1999;137(1):47–55.10.1016/S0300-483X(99)00081-5Search in Google Scholar

18. Turkez H, Aydin E. The effects of taurine on permethrininduced cytogenetic and oxidative damage in cultured human lymphocytes. Arh Hig Rada Toksikol 2012;63(1):27–34.10.2478/10004-1254-63-2012-2114Search in Google Scholar

19. Ramos-Chavez LA, Sordo M, Calderon-Aranda E, Castañeda-Saucedo E, Ostrosky-Wegman P, Moreno-Godinez ME. A permethrin/allethrin mixture induces genotoxicity and cytotoxicity in human peripheral blood lymphocytes. J Toxicol Environ Health A 2015;78(1):7–14.10.1080/15287394.2015.956025Search in Google Scholar

20. Xia D, Parvizi N, Zhou Y, Xu K, Jiang H, Li R, et al. Paternal fenvalerate exposure influences reproductive functions in the offspring. Reprod Sci 2013;20(11):1308–15.10.1177/1933719113483015Search in Google Scholar

21. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. Pesticside and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod Toxicol 2012;34(4):708–19.10.1016/j.reprotox.2012.08.010Search in Google Scholar

22. Mandarapu R, Prakhya BM. In vitro myelotoxic effects of cypermethrin and mancozeb on human hematopoietic progenitor cells. J Immunotoxicol 2015;12(1):48–55.10.3109/1547691X.2014.880535Search in Google Scholar

23. Chatterjee S, Basak P, Chaklader M, Das P, Pereira JA, Chaudhuri S, et al. Pesticide induced alterations in marrow physiology and depletion of stem and stromal progenitor population: an experimental model to study the toxic effects of pesticide. Environ Toxicol 2014;29(1):84–97.10.1002/tox.20775Search in Google Scholar

24. Kasat K, Go V, Pogo BGT. Effects of pyrethroid insecticides and estrogen on WNT10B proto-oncogene expression. Environ Int 2002;28(5):429–32.10.1016/S0160-4120(02)00072-7Search in Google Scholar

25. Zhou J-L, Ding Z, Ge X, Shi Q-M, Wang H-X, Chen G, et al. Cypermethrin inhibits interleukin-6-induced androgen receptor transactivation through signal transducer and activator of transcription 3. Toxicol Mech Methods 2017;27(9):717–22.10.1080/15376516.2017.1351505Search in Google Scholar

26. El Okda E-S, Abdel-Hamid MA-A, Hamdy AM. Immunological and genotoxic effects of occupational exposure to α-cypermethrin pesticide. Int J Occup Med Environ Health 2017;30(4):603–15.10.13075/ijomeh.1896.00810Search in Google Scholar

27. Ahmadi F, Ghanbari K. Proposed model for binding of permethrin and deltamethrin insecticides with ct-DNA, a structural comparative study. Ecotoxicol Environ Saf 2014;106:136–45.10.1016/j.ecoenv.2014.02.018Search in Google Scholar

28. Saxena PN, Chauhan LKS, Gupta SK. Cytogenetic effects of commercial formulation of cypermethrin in root meristem cells of Allium sativum: spectroscopic basis of chromosome damage. Toxicology 2005;216(2–3):244–52.10.1016/j.tox.2005.08.008Search in Google Scholar

29. Chen H, Xiao J, Hu G, Zhou J, Xiao H, Wang X. Estrogenicity of organophosphorus and pyrethroid pesticides. J Toxicol Environ Health A 2002;65(19):1419–35.10.1080/00984100290071243Search in Google Scholar

30. 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 Off J Soc Toxicol 2010;116(1):58–66.10.1093/toxsci/kfq120Search in Google Scholar

31. Yang O, Kim HL, Weon J-I, Seo YR. Endocrine-disrupting chemicals: review of toxicological mechanisms using molecular pathway analysis. J Cancer Prev 2015;20(1):12–24.10.15430/JCP.2015.20.1.12Search in Google Scholar

32. Kale M, Rathore N, John S, Bhatnagar D. Lipid peroxidative damage on pyrethroid exposure and alterations in antioxidant status in rat erythrocytes: a possible involvement of reactive oxygen species. Toxicol Lett 1999;105(3):197–205.10.1016/S0378-4274(98)00399-3Search in Google Scholar

33. Mignini F, Nasuti C, Fedeli D, Mattioli L, Cosenza M, Artico M, et al. Protective effect of alpha-lipoic acid on cypermethrin-induced oxidative stress in Wistar rats. Int J Immunopathol Pharmacol 2013;26(4):871–81.10.1177/039463201302600405Search in Google Scholar

34. Gabbianelli R, Falcioni G, Nasuti C, Cantalamessa F. Cypermethrin-induced plasma membrane perturbation on erythrocytes from rats: reduction of fluidity in the hydrophobic core and in glutathione peroxidase activity. Toxicology 2002;175(1–3):91–101.10.1016/S0300-483X(02)00058-6Search in Google Scholar

35. Punareewattana K, Smith BJ, Blaylock BL, Longstreth J, Snodgrass HL, Gogal RM, et al. Topical permethrin exposure inhibits antibody production and macrophage function in C57Bl/6N mice. Food Chem Toxicol 2001;39(2):133–9.10.1016/S0278-6915(00)00116-2Search in Google Scholar

36. Wang X, Gao X, He B, Zhu J, Lou H, Hu Q, et al. Cis-bifenthrin induces immunotoxicity in adolescent male C57BL/6 mice. Environ Toxicol 2017;32(7):1849–56.10.1002/tox.22407Search in Google Scholar

37. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144(5):646–74.10.1016/j.cell.2011.02.013Search in Google Scholar

38. Krieger RI. Hayes’ Handbook of Pesticide Toxicology. Elsevier, 2010. 1238 p.Search in Google Scholar

39. Nasuti C, Cantalamessa F, Falcioni G, Gabbianelli R. Different effects of Type I and Type II pyrethroids on erythrocyte plasma membrane properties and enzymatic activity in rats. Toxicology 2003;191(2):233–44.10.1016/S0300-483X(03)00207-5Search in Google Scholar

40. Davies TGE, Field LM, Usherwood PNR, Williamson MS. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 2007;59(3):151–62.10.1080/15216540701352042Search in Google Scholar PubMed

41. Facts and Statistics | Leukemia and Lymphoma Society [Internet]. Available from: http://www.lls.org/http%3A/llsorg.prod.acquia-sites.com/facts-and-statistics/facts-and-statistics-overview/facts-and-statistics.Search in Google Scholar

42. Roberts JR, Karr CJ, Paulson JA, Brock-Utne AC, Brumberg HL, Campbell CC, et al. Pesticide exposure in children. Pediatrics 2012;130(6):e1757–63.10.1542/peds.2012-2758Search in Google Scholar PubMed PubMed Central

43. Barr DB, Olsson AO, Wong L-Y, 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(6):742–8.10.1289/ehp.0901275Search in Google Scholar PubMed PubMed Central

44. Leng G, Gries W, Selim S. Biomarker of pyrethrum exposure. Toxicol Lett 2006;162(2–3):195–201.10.1016/j.toxlet.2005.09.030Search in Google Scholar PubMed

45. ATSDR – Toxicological Profile: Pyrethrins and Pyrethroids [Internet]. Available from: http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=787&tid=153.Search in Google Scholar

46. Lu C, Barr DB, Pearson MA, Walker LA, Bravo R. The attribution of urban and suburban children’s exposure to synthetic pyrethroid insecticides: a longitudinal assessment. J Expo Sci Environ Epidemiol 2009;19(1):69–78.10.1038/jes.2008.49Search in Google Scholar PubMed

47. Glorennec P, Serrano T, Fravallo M, Warembourg C, Monfort C, Cordier S, et al. Determinants of children’s exposure to pyrethroid insecticides in western France. Environ Int 2017;104:76–82.10.1016/j.envint.2017.04.007Search in Google Scholar PubMed

48. Neta G, Goldman LR, Barr D, Apelberg BJ, Witter FR, Halden RU. Fetal exposure to chlordane and permethrin mixtures in relation to inflammatory cytokines and birth outcomes. Environ Sci Technol 2011;45(4):1680–7.10.1021/es103417jSearch in Google Scholar PubMed PubMed Central

49. Limon-Miro AT, Aldana-Madrid ML, Alvarez-Hernandez G, Antunez-Roman LE, Rodriguez-Olibarria G, Valencia Juillerat ME. Breast milk intake and mother to infant pesticide transfer measured by deuterium oxide dilution in agricultural and urban areas of Mexico. Chemosphere 2017;181:682–9.10.1016/j.chemosphere.2017.04.110Search in Google Scholar PubMed

50. Mylène Ratelle JC. Toxicokinetics of permethrin biomarkers of exposure in orally exposed volunteers. Toxicol Lett 2014;232(2):369–75.10.1016/j.toxlet.2014.12.003Search in Google Scholar PubMed

51. Cancer Facts and Statistics 2015 | Research | American Cancer Society [Internet]. [cited 2015 Apr 21]. Available from: http://www.cancer.org/research/cancerfactsstatistics/cancerfactsfigures2015/index.Search in Google Scholar

52. Peto J. Cancer epidemiology in the last century and the next decade. Nature 2001;411(6835):390–5.10.1038/35077256Search in Google Scholar PubMed

53. Sankpal UT, Pius H, Khan M, Shukoor MI, Maliakal P, Lee CM, et al. Environmental factors in causing human cancers: emphasis on tumorigenesis. Tumour Biol 2012;33(5):1265–74.10.1007/s13277-012-0413-4Search in Google Scholar PubMed

54. Saillenfait A-M, Ndiaye D, Sabaté J-P. Pyrethroids: exposure and health effects – an update. Int J Hyg Environ Health 2015;218(3):281–92.10.1016/j.ijheh.2015.01.002Search in Google Scholar PubMed

55. Hernández AF, Menéndez P. Linking pesticide exposure with pediatric leukemia: potential underlying mechanisms. Int J Mol Sci 2016;17(4):461.10.3390/ijms17040461Search in Google Scholar PubMed PubMed Central

56. Alavanja MCR, Bonner MR. Occupational pesticide exposures and cancer risk: a review. J Toxicol Environ Health B Crit Rev 2012;15(4):238–63.10.1080/10937404.2012.632358Search in Google Scholar PubMed PubMed Central

57. Roulland S, Lebailly P, Lecluse Y, Briand M, Pottier D, Gauduchon P. Characterization of the t(14;18) BCL2-IGH translocation in farmers occupationally exposed to pesticides. Cancer Res 2004;64(6):2264–9.10.1158/0008-5472.CAN-03-3604Search in Google Scholar

58. Greaves MF, Wiemels J. Origins of chromosome translocations in childhood leukaemia. Nat Rev Cancer 2003;3(9):639–49.10.1038/nrc1164Search in Google Scholar PubMed

59. Weichenthal S, Moase C, Chan P. A Review of pesticide exposure and cancer incidence in the agricultural health study cohort. Environ Health Perspect 2010;118(8):1117–25.10.1289/ehp.0901731Search in Google Scholar PubMed PubMed Central

60. Berkowitz GS, Obel J, Deych E, Lapinski R, Godbold J, Liu Z, et al. Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ Health Perspect 2003;111(1):79–84.10.1289/ehp.5619Search in Google Scholar PubMed PubMed Central

61. Alavanja MCR, Hofmann JN, Lynch CF, Hines CJ, Barry KH, Barker J, et al. Non-hodgkin lymphoma risk and insecticide, fungicide and fumigant use in the agricultural health study. PLoS One 2014;9(10):e109332.10.1371/journal.pone.0109332Search in Google Scholar PubMed PubMed Central

62. Garry VF. Pesticides and children. Toxicol Appl Pharmacol 2004;198(2):152–63.10.1016/j.taap.2003.11.027Search in Google Scholar PubMed

63. Malagoli C, Costanzini S, Heck JE, Malavolti M, De Girolamo G, Oleari P, et al. Passive exposure to agricultural pesticides and risk of childhood leukemia in an Italian community. Int J Hyg Environ Health 2016;219(8):742–8.10.1016/j.ijheh.2016.09.015Search in Google Scholar PubMed PubMed Central

64. Ferreira JD, Couto AC, Pombo-de-Oliveira MS, Koifman S, Brazilian Collaborative Study Group of Infant Acute Leukemia. In utero pesticide exposure and leukemia in Brazilian children<2 years of age. Environ Health Perspect 2013;121(2):269–75.10.1289/ehp.1103942Search in Google Scholar PubMed PubMed Central

65. Pui C-H, Evans WE. Treatment of acute lymphoblastic leukemia. N Engl J Med 2006;354(2):166–78.10.1056/NEJMra052603Search in Google Scholar PubMed

66. Rivera-Luna R, Correa-González C, Altamirano-Alvarez E, Sánchez-Zubieta F, Cárdenas-Cardós R, Escamilla-Asian G, et al. Incidence of childhood cancer among Mexican children registered under a public medical insurance program. Int J Cancer 2013;132(7):1646–50.10.1002/ijc.27771Search in Google Scholar PubMed

67. Borkhardt A, Wilda M, Fuchs U, Gortner L, Reiss I. Congenital leukaemia after heavy abuse of permethrin during pregnancy. Arch Dis Child Fetal Neonatal Ed 2003;88(5):F436–7.10.1136/fn.88.5.F436Search in Google Scholar PubMed PubMed Central

68. Lafiura KM, Bielawski DM, Posecion NC, Ostrea EM, Matherly LH, Taub JW, et al. Association between prenatal pesticide exposures and the generation of leukemia-associated T(8;21). Pediatr Blood Cancer 2007;49(5):624–8.10.1002/pbc.21283Search in Google Scholar PubMed

69. Gabbianelli R, Nasuti C, Falcioni G, Cantalamessa F. Lymphocyte DNA damage in rats exposed to pyrethroids: effect of supplementation with Vitamins E and C. Toxicology 2004;203(1–3):17–26.10.1016/j.tox.2004.05.012Search in Google Scholar

70. Caballo C, Herrera A, Barrueco C, Santa-María A, Sanz F, de la Peña E. Analysis of cytogenetic damage induced in CHO cells by the pyrethroid insecticide fenvalerate. Teratog Carcinog Mutagen 1992;12:243–9.10.1002/tcm.1770120602Search in Google Scholar

71. Surrallés J, Xamena N, Creus A, Catalán J, Norppa H, Marcos R. Induction of micronuclei by five pyrethroid insecticides in whole-blood and isolated human lymphocyte cultures. Mutat Res 1995;341(3):169–84.10.1016/0165-1218(95)90007-1Search in Google Scholar

72. Tisch M, Schmezer P, Faulde M, Groh A, Maier H. Genotoxicity studies on permethrin, DEET and diazinon in primary human nasal mucosal cells. Eur Arch Otorhinolaryngol 2002;259(3):150–3.10.1007/s004050100406Search in Google Scholar PubMed

73. Sundaramoorthy R, Velusamy Y, Balaji APB, Mukherjee A, Chandrasekaran N. Comparative cytotoxic and genotoxic effects of permethrin and its nanometric form on human erythrocytes and lymphocytes in vitro. Chem Biol Interact 2016;257:119–24.10.1016/j.cbi.2016.08.001Search in Google Scholar PubMed

74. Navarrete-Meneses MP, Salas-Labadía C, Sanabrais-Jiménez M, Santana-Hernández J, Serrano-Cuevas A, Juárez-Velázquez R, et al. Exposure to the insecticides permethrin and malathion induces leukemia and lymphoma-associated gene aberrations in vitro. Toxicol In Vitro 2017;44:17–26.10.1016/j.tiv.2017.06.013Search in Google Scholar PubMed

75. Suárez-Larios K, Salazar-Martínez A-M, Montero-Montoya R. Screening of pesticides with the potential of inducing DSB and successive recombinational repair. J Toxicol 2017;2017:9.10.1155/2017/3574840Search in Google Scholar PubMed PubMed Central

76. Patel S, Bajpayee M, Pandey AK, Parmar D, Dhawan A. In vitro induction of cytotoxicity and DNA strand breaks in CHO cells exposed to cypermethrin, pendimethalin and dichlorvos. Toxicol In Vitro 2007;21(8):1409–18.10.1016/j.tiv.2007.05.009Search in Google Scholar PubMed

77. Meyer C, Hofmann J, Burmeister T, Gröger D, Park TS, Emerenciano M, et al. The MLL recombinome of acute leukemias in 2013. Leukemia 2013;27(11):2165–76.10.1038/leu.2013.135Search in Google Scholar PubMed PubMed Central

78. Navarrete-Meneses MP, Pedraza-Meléndez AI, Salas-Labadía C, Moreno-Lorenzana D, Pérez-Vera P. Low concentrations of permethrin and malathion induce numerical and structural abnormalities in KMT2A and IGH genes in vitro. J Appl Toxicol 2018;38:1262–70.10.1002/jat.3638Search in Google Scholar PubMed

79. Villarini M, Moretti M, Pasquini R, Scassellati-Sforzolini G, Fatigoni C, Marcarelli M, et al. In vitro genotoxic effects of the insecticide deltamethrin in human peripheral blood leukocytes: DNA damage (‘comet’ assay) in relation to the induction of sister-chromatid exchanges and micronuclei. Toxicology 1998;130(2–3):129–39.10.1016/S0300-483X(98)00097-3Search in Google Scholar

80. Matsuoka A, Hayashi M, Ishidate M. Chromosomal aberration tests on 29 chemicals combined with S9 mix in vitro. Mutat Res 1979;66(3):277–90.10.1016/0165-1218(79)90089-2Search in Google Scholar

81. Zeljezic D, Vinkovic B, Kasuba V, Kopjar N, Milic M, Mladinic M. The effect of insecticides chlorpyrifos, α-cypermethrin and imidacloprid on primary DNA damage, TP 53 and c-Myc structural integrity by comet-FISH assay. Chemosphere 2017;182:332–8.10.1016/j.chemosphere.2017.05.010Search in Google Scholar PubMed

82. Zhang R, Niu Y, Du H, Cao X, Shi D, Hao Q, et al. A stable and sensitive testing system for potential carcinogens based on DNA damage-induced gene expression in human HepG2 cell. Toxicol In Vitro 2009;23(1):158–65.10.1016/j.tiv.2008.10.006Search in Google Scholar PubMed

83. Kocaman AY, Topaktaş M. The in vitro genotoxic effects of a commercial formulation of alpha-cypermethrin in human peripheral blood lymphocytes. Environ Mol Mutagen 2009;50(1):27–36.10.1002/em.20434Search in Google Scholar PubMed

84. Sandal S, Yilmaz B. Genotoxic effects of chlorpyrifos, cypermethrin, endosulfan and 2,4-D on human peripheral lymphocytes cultured from smokers and nonsmokers. Environ Toxicol 2011;26(5):433–42.10.1002/tox.20569Search in Google Scholar PubMed

85. Želježić D, Mladinić M, Žunec S, Lucić Vrdoljak A, Kašuba V, Tariba B, et al. Cytotoxic, genotoxic and biochemical markers of insecticide toxicity evaluated in human peripheral blood lymphocytes and an HepG2 cell line. Food Chem Toxicol 2016;96:90–106.10.1016/j.fct.2016.07.036Search in Google Scholar PubMed

86. Turkez H, Togar B, Polat E. Olive leaf extract modulates permethrin induced genetic and oxidative damage in rats. Cytotechnology 2012;64(4):459–64.10.1007/s10616-011-9424-zSearch in Google Scholar PubMed PubMed Central

87. Roma GC, de Oliveira PR, Araujo AM, Bechara GH, Mathias MIC. Genotoxic and mutagenic effects of permethrin in mice: micronuclei analysis in peripheral blood erythrocytes. Microsc Res Tech 2012;75(12):1732–6.10.1002/jemt.22124Search in Google Scholar PubMed

88. Wiemels J. Chromosomal translocations in childhood leukemia: natural history, mechanisms, and epidemiology. J Natl Cancer Inst Monogr 2008;(39):87–90.10.1093/jncimonographs/lgn006Search in Google Scholar PubMed

89. Diel F, Horr B, Borck H, Savtchenko H, Mitsche T, Diel E. Pyrethroids and piperonyl-butoxide affect human T-lymphocytes in vitro. Toxicol Lett 1999;107(1–3):65–74.10.1016/S0378-4274(99)00032-6Search in Google Scholar

90. Aouey B, Derbali M, Chtourou Y, Bouchard M, Khabir A, Fetoui H. Pyrethroid insecticide lambda-cyhalothrin and its metabolites induce liver injury through the activation of oxidative stress and proinflammatory gene expression in rats following acute and subchronic exposure. Environ Sci Pollut Res Int 2017;24(6):5841–56.10.1007/s11356-016-8323-4Search in Google Scholar PubMed

91. Schnyder S, Du NT, Le HB, Singh S, Loredo GA, Vaughan AT. Estrogen treatment induces MLL aberrations in human lymphoblastoid cells. Leuk Res 2009;33(10):1400–4.10.1016/j.leukres.2009.01.023Search in Google Scholar PubMed PubMed Central

92. Le H, Singh S, Shih S-J, Du N, Schnyder S, Loredo GA, et al. Rearrangements of the MLL gene are influenced by DNA secondary structure, potentially mediated by topoisomerase II binding. Genes Chromosomes Cancer 2009;48(9):806–15.10.1182/blood.V112.11.3105.3105Search in Google Scholar

93. Merlo DF, Agramunt S, Anna L, Besselink H, Botsivali M, Brady NJ, et al. Micronuclei in cord blood lymphocytes and associations with biomarkers of exposure to carcinogens and hormonally active factors, gene polymorphisms, and gene expression: The NewGeneris cohort. Environ Health Perspect 2014;122(2):193–200.10.1289/ehp.1206324Search in Google Scholar PubMed PubMed Central

94. Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010;48(6):749–62.10.1016/j.freeradbiomed.2009.12.022Search in Google Scholar PubMed PubMed Central

95. Fiaschi T, Chiarugi P. Oxidative stress, tumor microenvironment, and metabolic reprogramming: a diabolic liaison. Int J Cell Biol [Internet] 2012. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3361160/.10.1155/2012/762825Search in Google Scholar PubMed PubMed Central

96. Wang X, Martínez M-A, Dai M, Chen D, Ares I, Romero A, et al. Permethrin-induced oxidative stress and toxicity and metabolism. A review. Environ Res 2016;149:86–104.10.1016/j.envres.2016.05.003Search in Google Scholar PubMed

97. Li H-Y, Zhong Y-F, Shi N. [Effect of deltamethrin on production of reactive oxygen species in PC12 cells]. Chin J Ind Hyg Occup Dis 2008;26(11):654–8.Search in Google Scholar

98. Maurya SK, Mishra J, Tripathi VK, Sharma R, Siddiqui MH. Cypermethrin induces astrocyte damage: role of aberrant Ca(2+), ROS, JNK, P38, matrix metalloproteinase 2 and migration related reelin protein. Pestic Biochem Physiol 2014;111:51–9.10.1016/j.pestbp.2014.03.005Search in Google Scholar PubMed

Received: 2018-11-08
Accepted: 2019-01-23
Published Online: 2019-03-23
Published in Print: 2019-06-26

©2019 Walter de Gruyter GmbH, Berlin/Boston

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