Environmental Science and Pollution Research

, Volume 24, Issue 2, pp 1532–1543 | Cite as

Individual and combined effect of chlorpyrifos and cypermethrin on reproductive system of adult male albino rats

  • Eman Ahmad Alaa-Eldin
  • Dalia Abdallah El-Shafei
  • Nehal S. Abouhashem
Research Article

Abstract

Commercial mixtures of chlorpyrifos and cypermethrin pesticides are widely used to enhance the toxic effects of cypermethrin on target insects. So, the purpose of the current study was to evaluate the individual and combined toxic effects of chlorpyrifos (CPF) and cypermethrin (CYP) on reproductive system of adult male albino rats. Forty adult male albino rats were randomized into main four groups: group I (control group) included 16 rats, subdivided into negative and positive control; group II (eight rats) received chlorpyrifos 6.75 mg/kg b.w./orally∕daily); group III (eight rats) (received cypermethrin 12.5 mg/kg b.w./orally∕daily); and group IV (eight rats) (received chlorpyrifos and cypermethrin at the same previously mentioned doses). All treatments were given by oral gavage for 12 weeks. We found that single CPF and CYP exposures significantly have adverse effects on reproductive function of adult male albino rats manifested by reduced testicular weight, decreased sperm count, motility and viability, significantly increased percent of morphologically abnormal spermatozoa, and significant increments in sperm DNA fragmentation index (DFI) with respect to control group. Furthermore, serum follicle stimulating hormone, luteinizing hormone, and testosterone levels were decreased significantly compared to control group. This was accompanied with histopathological changes in the testis of rats such as necrosis, degeneration, decreasing number of spermatogenic cells in some seminiferous tubules, edema, congested blood vessels, and exudate in interstitial tissue of the testis. Notably, all these changes were exaggerated in rats treated concomitantly with chlorpyrifos and cypermethrin rendering the mixture more toxic than the additive effects of each compound and causing greater damage on the reproductive system of male albino rats than the individual pesticides.

Keywords

Pesticides Organophosphorus Pyrethroids Chlorpyrifos Cypermethrin Reproductive toxicity 

References

  1. Ahmad L, Khan A, Khan MZ (2012) Pyrethroid-induced reproductive toxicopathology in non-target species. Pak Vet J 32(1):1–9Google Scholar
  2. Akhtar N, Srivastava MK, Raizada RB (2009) Assessment of chlorpyrifos toxicity on certain organs in rat, Rattus norvegicus. J Environ Biol 30(6):1047–1053Google Scholar
  3. Al-Hamdani N, Yajurvedi H (2010) Cypermethrin reversibly alters sperm count without altering fertility in mice. Ecotoxicol and Environ Saf 73:1092–1097CrossRefGoogle Scholar
  4. Ambali SF, Idris SB, Onukak C, Shittu M, Ayo JO (2010) Ameliorative effect of vitamin C on short term sensorimotor and cognitive changes induced by acute chlorpyrifos exposure in Wistar rats. Toxicol Ind Health 26:547–558CrossRefGoogle Scholar
  5. Assayed M, Salem H, Khalaf A et al (2008) Protective effects of garlic extract and vitamin C against cypermethrin reproductive toxicity in male rats. J Vet Sci 1(1):1–15Google Scholar
  6. Bancroft JD, Gamble M (2007) Connective tissue stains. In: Bancroft JD, Gamble M (eds) Theory and practice of histological techniques. 6th ed. Churchill Livingstone, London New York Philadelphia, p. 150Google Scholar
  7. Bian Q, Xu L, Wang S et al (2004) Study on the relation between occupational fenvalerate exposure and spermatozoa DNA damage of pesticide factory workers. Occup Environ Med 61:999–1005CrossRefGoogle Scholar
  8. Brown J, Schoenemann H, Chakraborty P (1994) Follicular fluid administration delayed, but didn’t prevent, the hemicastration, induced increase in follicular stimulating hormone secretion and compensatory testicular hypertrophy in ram lambs. Biol Repro 50(1):44–48CrossRefGoogle Scholar
  9. Chen L, Wang R, Wang W, Lu W, Xiao Y, Wang D, Dong Z (2015) Hormone inhibition during mini-puberty and testicular function in male rats. International journal of endocrinology and metabolism 13(4)Google Scholar
  10. Choudhary N, Goyal R, Joshi SC (2008) Effect of malathion on reproductive system of male rats. J Environ Biol 29:259–262Google Scholar
  11. Clark JD, Baldwin RL, Bayne KA, Brown M, Gebhart GF, Gonder JC, Gwathmey JK, Keeling ME, Kohn DF, Robb JW, Smith OA (1996) Guide for the care and use of laboratory animals. Institute of Laboratory Animal Resources, National Research Council. Washington, DC, p 125Google Scholar
  12. Eaton DL, Daroff RB, Autrup J et al (2008) Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol 38(12):1–125CrossRefGoogle Scholar
  13. Ekaluo UB, Ibiang YB, Ikpeme EV, Ekanem BE, Erem FA (2013) Effect of deltamethrin and ridomil on sperm parameters and reproductive hormones of male albino rats. J Toxicol Environ Health Sci 5(1):9–14CrossRefGoogle Scholar
  14. 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(4):522–528CrossRefGoogle Scholar
  15. ElMazoudy RH, Attia AA, El-Shenawy NS (2011) Protective role of propolis against reproductive toxicity of chlorpyrifos in male rats. Pestic Biochem Physiol 101(3):175–181CrossRefGoogle Scholar
  16. Evenson D, Jost L (1994) Sperm chromatin structure assay: DNA denaturability. Methods Cell Biol 42:159–176CrossRefGoogle Scholar
  17. Evenson DP, Larson KL, Jost LK (2002) Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23(1):25–43CrossRefGoogle Scholar
  18. Farag AT, Radwan AH, Sorour F, El Okazy A, El-Agamy ES, El-Sebae AE (2010) Chlorpyrifos induced reproductive toxicity in male mice. Reprod Toxicol 29(1):80–85CrossRefGoogle Scholar
  19. Goel A, Dani V, Dhawan D K (2007) Zinc mediates normalization of hepatic drug metabolizing enzymes in chlorpyrifos-induced toxicity. Toxicol Letters 169:26–33Google Scholar
  20. Greene S, Pohanish R (2005) Sittig’s handbook of pesticides and agricultural chemicals. William Andrew, Norwich, NY, pp. 174–177Google Scholar
  21. Grewal KK, Sandhu GS, Kaur R, Brar RS, Sandhu HS (2010) Toxic impacts of cypermethrin on behavior and histology of certain tissues of albino rats. Toxicol Int 17(2):94CrossRefGoogle Scholar
  22. Groten JP, Feron VJ, Sühnel J (2001) Toxicology of simple and complex mixtures. Trends Pharmacol Sci 22(6):316–322CrossRefGoogle Scholar
  23. Heikal TM, Mossa AT, Ibrahim AW, Abdel-Hamid HF (2014) Oxidative damage and reproductive toxicity associated with cyromazine and chlorpyrifos in male rats: the protective effects of green tea extract. Res J Environ Toxicol 8:53–67CrossRefGoogle Scholar
  24. Hussien H, Abdoub H, Yousef M et al (2011) Cypermethrin induced damage in genomic DNA and histopathological changes in brain and haematotoxicity in rats: the protective effect of sesame oil. Brain Res Bull 87(5):402–419Google Scholar
  25. Idris SB, Ambali SF, Ayo JO (2012) Cytotoxicity of chlopyrifos and cypermethrin: the ameliorative effects of antioxidants. Afr J Biotechnol 11(99):16461–16467Google Scholar
  26. Ikpeme EV, Okonko LE, Udensi OU (2016) Detrimental effects of chlorpyrifos and cypermethrin on reproductive physiology of male albino rats. Research Journal of Environmental Toxicology 10(1):68–74CrossRefGoogle Scholar
  27. Ikpeme EV, Udensi O, Ekaluo UB, Uyoh EA, Asuquo BO, Udoh FV, Udoh PB (2007) Effect of crude extract of Caricapapaja seeds on the reproductive efficiency of male albino rats. Global J Pure Applied Sci 13:365–368Google Scholar
  28. Ji G, Xia Y, Gu A, Shi X, Long Y, Song L, Wang S, Wang X (2011) Effects of non-occupational environmental exposure to pyrethroids on semen quality and sperm DNA integrity in Chinese men. Reproductive Toxicology 31(2):171–117CrossRefGoogle Scholar
  29. Joshi SC, Bansal B, Jasuja ND (2011) Evaluation of reproductive and developmental toxicity of cypermethrin in male albino rats. Toxicological & Environ Chemistry 93(3):593–602CrossRefGoogle Scholar
  30. Joshi SC, Mathur R, Gulati N (2007) Testicular toxicity of chlorpyrifos (an organophosphate pesticide) in albino rat. Toxicol Ind Health 23(7):439–444CrossRefGoogle Scholar
  31. Kalender Y, Kaya S, Durak D (2012) Protective effects of catechin and quercetin on antioxidant status, lipid peroxidation and testis-histoarchitecture induced by chlorpyrifos in male rats. Environ Toxicol Pharmacol 33(2):141–148CrossRefGoogle Scholar
  32. Kamijima M, Hibi H, Gotoh M, Taki KI, Saito I, Wang H, Itohara S, Yamada T, Ichihara G, Shibata E, Nakajima T (2004) A survey of semen indices in insecticide sprayers. J Occup Health 46(2):109–118CrossRefGoogle Scholar
  33. Kang HG, Jeong SH, Cho JH, Kim DG, Park JM, Cho MH (2004) Chlropyrifos-methyl shows anti-androgenic activity without estrogenic activity in rats. Toxicology 199(2):219–230CrossRefGoogle Scholar
  34. Kim S, Kwon H, Park JH, Cho B, Kim D, Oh SW, Lee CM, Choi HC (2012) A low level of serum totaltestosterone is independently associated with nonalcoholic fatty liver disease. BMC Gastroenterol 12(1):1CrossRefGoogle Scholar
  35. Kitamura S, Suzuki T, Ohta S, Fujimoto N (2003) Antiandrogenic activity and metabolism of the organophosphorus pesticide fenthion and related compounds. Environ Health Perspect 111(4):503CrossRefGoogle Scholar
  36. LI YF, Chen PA, HU JX, Jing LI, XU LC (2013) Effects of cypermethrin on male reproductive system in adult rats. Biomed Environ Sci 26(3):201–208Google Scholar
  37. Manna S, Bhattacharyya D, Mandal T et al (2004) Repeated dose toxicity of alfa cypermethrin in rats. J Vet Sci 5:241–245Google Scholar
  38. Meeker JD, Singh NP, Ryan L (2004) Urinary levels of insecticide metabolites and DNA damage in human sperm. Hum Reprod 19(11):2573–2580CrossRefGoogle Scholar
  39. Mori K, Kaido M, Fujishiro K et al (1991) Dose dependent effects of inhaled ethylene oxide on spermatogenesis in rats. Br J Ind Med 48(4):270–274Google Scholar
  40. Mosbah R, Yousef MI, Maranghi F, Mantovani A (2014) Protective role of Nigella sativa oil against reproductive toxicity, hormonal alterations, and oxidative damage induced by chlorpyrifos in male rats. Toxicol Ind Health. doi:10.1177/0748233714554675 Google Scholar
  41. Nemzek J, Boloqos G, Williams B, Remick D (2001) Differences in normal values for murine white blood cells counts and other hematological parameters based on sampling site. Inflamm Res 50:523–527CrossRefGoogle Scholar
  42. Noaishi MA, Allah AA, Afify MM (2013) Oral and dermal exposure of chlorpyrifos and cypermethrin mixture induced cytogenetic, histopathological damage and oxidative stress in rats. J Am Sci 9:56–65Google Scholar
  43. Piña-Guzman B, Solís-Heredia MJ, Quintanilla-Vega B (2005) Diazinon alters sperm chromatin structure in mice by phosphorylating nuclear protamines. Toxicol Appl Pharmacol 202(2):189–198CrossRefGoogle Scholar
  44. Qiao D, Seidler FJ, Slotkin TA (2001) Developmental neurotoxicity of chlorpyrifos modeled in vitro: comparative effects of metabolites and other cholinesterase inhibitors on DNA synthesis in PC12 and C6 cells. Environ Health Perspect 109:909–913CrossRefGoogle Scholar
  45. Recio R, Robbins WA, Ocampo-Gómez G (2001) Organophosphorous pesticide exposure increases the frequency of sperm sex null aneuploidy. Env Health Perspect 109(12):1237–1240CrossRefGoogle Scholar
  46. Sankar P, Telang AG, Manimaran A, Malik JK (2010) Immunoprotective effect of curcumin on cypermethrin-induced toxicity in rats. Toxicological and Environ Chemistry 92(10):1909–1917CrossRefGoogle Scholar
  47. Sankar P, Telang AG, Manimaran A (2012) Protective effect of curcumin on cypermethrin-induced oxidative stress in Wistar rats. Exp Toxicol Pathol 64(5):487–493CrossRefGoogle Scholar
  48. Sergerie M, Laforest G, Bujan L, Bissonnette F, Bleau G (2005) Sperm DNA fragmentation: threshold value in male fertility. Human Reprod 20(12):3446–3451CrossRefGoogle Scholar
  49. Sharma P, Huq AU, Singh R (2014) Cypermethrin-induced reproductive toxicity in the rat is prevented by resveratrol. J Hum Reprod Sci 7(2):99–106CrossRefGoogle Scholar
  50. Shittu M, Ambali SF, Ayo JO et al (2013) Evaluation of chronic chlorpyrifos-induced reproductive toxicity in male wistar rat: protective effects of vitamin C. J Exp Integr Med 3(1):23–30CrossRefGoogle Scholar
  51. Soliman MM, Attia HF, El-Ella GAA (2015) Genetic and histopathological alterations induced by cypermethrin in rat kidney and liver: protection by sesame oil. Int J Immunopathol Pharmacol 28(4):508–520CrossRefGoogle Scholar
  52. SPSS Inc. (2007) SPSS for Windows, Version 16.0. Chicago, SPSS Inc. available from: http://www.unimuenster.de/imperia/md/content/ziv/service/software/spss/handbuecher/englisch/spss_brief_guide_16.0.pdf.
  53. Timchalk C, Poet TS, Hinman MN, Busby AL, Kousba AA (2005) Pharmacokinetic and pharmacodynamic interaction for a binary mixture of chlorpyrifos and diazinon in the rat. Toxicol Appl Pharm 205:31–35CrossRefGoogle Scholar
  54. Uzun FG, Kalender S, Durak D, Demir F, Kalender Y (2009) Malathion-induced testicular toxicity in male rats and the protective effect of vitamins C and E. Food Chem Toxicol 47(8):1903–1908CrossRefGoogle Scholar
  55. Uzunhisarcikli M, Kalender Y, Dirican K, Kalender S, Ogutcu A, Buyukkomurcu F (2007) Acute, subacute and subchronic administration of methyl parathion-induced testicular damage in male rats and protective role of vitamins C and E. Pestic Biochem Physiol 87:115–122CrossRefGoogle Scholar
  56. Wang XZ, Liu SS, Sun Y, Wu JY, Zhou YL, Zhang JH (2009) Beta-cypermethrin impairs reproductive function in male mice by inducing oxidative stress. Theriogenology 72:599–611CrossRefGoogle Scholar
  57. World Health Organization (WHO) (1996) The world health report: fighting disease, fostering development. WHO, GenevaGoogle Scholar
  58. Wielgomas B, Krechniak J (2007) Toxicokinetic interactions of alpha-cypermethrin and chlorpyrifos in rats. Pol J Environ Stud 16(2):267Google Scholar
  59. Yousef M, El-Demerdash F, Al-Salhen K et al (2003) Protective role of isoflavones against the toxic effect of cypermethrin on semen quality and testosterone levels of rabbits. J Environ Sci Health 38B:463–478CrossRefGoogle Scholar
  60. Zhou S, Duan C, Michelle WH, Yang F, Wang X (2011) Individual and combined toxic effects of cypermethrin and chlorpyrifos on earthworm. J Environ Sci 23(4):676–680CrossRefGoogle Scholar
  61. Zidan NEHA (2009) Evaluation of the reproductive toxicity of chlorpyrifos methyl, diazinon and profenofos pesticides in male rats. Int J Pharmacol 5(1):51–57CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Eman Ahmad Alaa-Eldin
    • 1
  • Dalia Abdallah El-Shafei
    • 2
  • Nehal S. Abouhashem
    • 3
  1. 1.Faculty of Medicine, Department of Forensic Medicine and Clinical ToxicologyZagazig UniversityZagazigEgypt
  2. 2.Faculty of Medicine, Department of Community, Environmental and Occupational MedicineZagazig UniversityZagazigEgypt
  3. 3.Faculty of Medicine, Department of PathologyZagazig UniversityZagazigEgypt

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