Korean Journal of Agricultural Science (농업과학연구)

Institute of Agricultural Science, CNU (충남대학교 농업과학연구소)
권호 표지
DOI QR코드

DOI QR Code

Fipronil impairs the fertilization competence of boar spermatozoa

  • Adikari Arachchige Dilki Indrachapa, Adikari (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Malavige Romesha, Chandanee (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Byeong-Yeon, Kim (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Young-Joo, Yi (Department of Agricultural Education, College of Education, Sunchon National University)
  • Received : 2022.01.27
  • Accepted : 2022.02.23
  • Published : 2022.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Fipronil is a popular insecticide used in both agricultural and domestic fields. Factors that affect sperm and eggs have a direct influence on reproductive outcomes. This study was undertaken to assess the effect of varying concentrations (10 - 200 μM) of fipronil and incubation times (30 min and 2 hrs) on boar spermatozoa. Spermatozoa were evaluated for motility, motion kinematics, viability, chromatin stability, and for the generation of intracellular reactive oxygen species (ROS) and the results were compared to those from corresponding controls. The findings revealed a significant, dose-dependent reduction in sperm motility in all fipronil treatment groups at 30 min of incubation (p < 0.05). A similar dose-dependent reduction in sperm motility was observed subsequent to fipronil exposure for 2 hrs of incubation (p < 0.05). Groups treated with fipronil showed a gradual reduction in motion kinematics (p < 0.05). Moreover, a significantly higher percentage of dead sperm was observed at 200 μM fipronil, as compared to the highest live percentage obtained in controls (p < 0.05). Evaluating the sperm chromatin integrity revealed a significantly higher percentage of damaged chromatin in spermatozoa incubated with 200 μM of fipronil. Moreover, ROS production was significantly higher in fipronil-exposed sperm (p < 0.05). In conclusion, boar spermatozoa incubated with fipronil showed decreased levels of sperm motility and viability, weaker chromatin integrity, and increased levels of intracellular ROS generation, all of which indicate that exposure to fipronil potentially impairs the fertilization competence of boar spermatozoa.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (NRF-2020R1A2C1014007).

References

  1. Amaral A, Lourenco B, Marques M, Ramalho-Santos J. 2013. Mitochondria functionality and sperm quality. Reproduction 146:163-174.
  2. Arcondeguy T, Lacazette E, Millevoi S, Prats H, Touriol C. 2013. VEGF-A mRNA processing, stability and translation: A paradigm for intricate regulation of gene expression at the post-transcriptional level. Nucleic Acids Research 41:7997-8010. https://doi.org/10.1093/nar/gkt539
  3. Bisht S, Faiq M, Tolahunase M, Dada R. 2017. Oxidative stress and male infertility. Nature Reviews Urology 14:470-485. https://doi.org/10.1038/nrurol.2017.69
  4. Boothe DM. 2011. Small animal clinical pharmacology and therapeutics-E-Book. Elsevier Health Sciences, Amsterdam, Netherlands.
  5. Bromfield EG, Aitken RJ, Anderson AL, McLaughlin EA, Nixon B. 2015. The impact of oxidative stress on chaperone-mediated human sperm-egg interaction. Human Reproduction 30:2597-2613. https://doi.org/10.1093/humrep/dev214
  6. Chen R, Cui Y, Zhang X, Zhang Y, Chen M, Zhou T, Lan X, Dong W, Pan C. 2018. Chlorpyrifos induction of testicular-cell apoptosis through generation of reactive oxygen species and phosphorylation of AMPK. Journal of Agricultural and Food Chemistry 66:12455-12470. https://doi.org/10.1021/acs.jafc.8b03407
  7. Cravedi JP, Delous G, Zalko D, Viguie C, Debrauwer L. 2013. Disposition fipronil in rats. Chemosphere 93:2276-2283. https://doi.org/10.1016/j.chemosphere.2013.07.083
  8. Edwards CA, Adams RS. 1970. Persistent pesticides in the environment. Critical Reviews in Environmental Science and Technology 1:7-67.
  9. Fent GM. 2014. Fipronil. Encyclopedia of Toxicology 3rd edition 2:596-597.
  10. Gant DB, Chalmers AE, Wolff MA, Hoffman HB, Bushey DF. 1998. Fipronil: Action at the GABA receptor. Pesticides and the future: Minimizing chronic exposure of humans and the environment. pp. 147-156. Ios Press, Amsterdam, Netherlands.
  11. Garces A, Pires I, Rodrigues P. 2020. Teratological effects of pesticides in vertebrates: A review. Journal of Environmental Science and Health Part B 55:75-89. https://doi.org/10.1080/03601234.2019.1660562
  12. Gervasi MG, Visconti PE. 2017. Molecular changes and signaling events occurring in spermatozoa during epididymal maturation. Andrology 5:204-218. https://doi.org/10.1111/andr.12320
  13. Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK. 2018. Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiological Research 206:131-140. https://doi.org/10.1016/j.micres.2017.08.016
  14. Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS. 2007. Environmental fate and toxicology of fipronil. Journal of Pesticide Science 32:189-199. https://doi.org/10.1584/jpestics.R07-02
  15. Hodgson E. 2012. Biotransformation of individual pesticides: Some examples. Pesticide biotransformation and disposition. Elsevier 1:195-208.
  16. Jenardhanan P, Panneerselvam M, Mathur PP. 2016. Effect of environmental contaminants on spermatogenesis. In Seminars in cell & developmental biology. Vol. 59. pp. 126-140. Academic Press, Cambridge, MA, USA.
  17. Kanat ON, Selmanoglu G. 2020. Neurotoxic effect of fipronil in neuroblastoma SH-SY5Y cell line. Neurotoxicity Research 37:30-40.
  18. Krzyzosiak J, Molan P, Vishwanath R. 1999. Measurements of bovine sperm velocities under true anaerobic and aerobic conditions. Animal Reproduction Science 55:163-173. https://doi.org/10.1016/S0378-4320(99)00016-0
  19. Li H, Zhang P, Zhao Y, Zhang H. 2020. Low doses of carbendazim and chlorothalonil synergized to impair mouse spermatogenesis through epigenetic pathways. Ecotoxicology and Environmental Safety 188:109908. https://doi.org/10.1016/j.ecoenv.2019.109908
  20. Mahmood I, Imadi SR, Shazadi K, Gul A, Hakeem KR. 2016. Effects of pesticides on environment. In Plant, Soil and Microbes. pp. 253-269. Springer, Berlin, Germany.
  21. Martins CF, Dode MN, Bao SN, Rumpf R. 2007. The use of the acridine orange test and the TUNEL assay to assess the integrity of freeze-dried bovine spermatozoa DNA.Genetics and Molecular Research 6:94-104.
  22. Mostafalou S, Abdollahi M. 2013. Pesticides and human chronic diseases: Evidences, mechanisms, and perspectives. Toxicology and Applied Pharmacology 268:157-177. https://doi.org/10.1016/j.taap.2013.01.025
  23. Narahashi T. 2010. Neurophysiological effects of insecticides. In Hayes' Handbook of Pesticide Toxicology. pp. 799-817. Academic Press, Cambridge, MA, USA.
  24. Nichi M, Goovaerts IGF, Cortada CNM, Barnabe VH, De Clercq JBP, Bols PEJ. 2007. Roles of lipid peroxidation and cytoplasmic droplets on in vitro fertilization capacity of sperm collected from bovine epididymides stored at 4℃ and 34℃. Theriogenology 67:334-340. https://doi.org/10.1016/j.theriogenology.2006.08.002
  25. Pandya IY. 2018. Pesticides and their applications in agriculture. Asian Journal of Applied Science and Technology 2:894-900.
  26. Patel S, Sangeeta S. 2019. Pesticides as the drivers of neuropsychotic diseases, cancers, and teratogenicity among agro-workers as well as general public. Environmental Science and Pollution Research 26:91-100. https://doi.org/10.1007/s11356-018-3642-2
  27. Poppenga RH, Oehme FW. 2010. Pesticide use and associated morbidity and mortality in veterinary medicine. In Hayes' Handbook of Pesticide Toxicology. pp. 285-301. Academic Press, Cambridge, MA, USA.
  28. Pursel V, Johnson LA. 1976. Frozoen boar spermatozoa: Methods of thawing pellets. Journal of Animal Science 42:927-931. https://doi.org/10.2527/jas1976.424927x
  29. Rajmohan KS, Chandrasekaran R, Varjani S. 2020. A review on occurrence of pesticides in environment and current technologies for their remediation and management. Indian Journal of Microbiology 60:125-138. https://doi.org/10.1007/s12088-019-00841-x
  30. Shakya M, Kumar S, Fular A, Upadhaya D, Sharma AK, Bisht N, Nandi A, Ghosh S. 2020. Emergence of fipronil resistant Rhipicephalus microplus populations in Indian states. Experimental and Applied Acarology 80:1-12. https://doi.org/10.1007/s10493-019-00448-3
  31. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, et al. 2015. Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22:5-34. https://doi.org/10.1007/s11356-014-3470-y
  32. Singh NS, Sharma R, Singh SK, Singh DK. 2021. A comprehensive review of environmental fate and degradation of fipronil and its toxic metabolites. Environmental Research 199:111-316.
  33. Souza AD, Medeiros ADR, Souza ACD, Wink M, Siqueira IR, Ferreira MBC, Fernandes L, Loayza Hidalgo MP, Torres ILDS. 2011. Evaluation of the impact of exposure to pesticides on the health of the rural population: Vale do Taquari, State of Rio Grande do Sul (Brazil). Ciencia and Saude Coletiva 16:3519-3528. https://doi.org/10.1590/S1413-81232011000900020
  34. Sun L, Jin R, Peng Z, Zhou Q, Qian H, Fu Z. 2014. Effects of trilostane and fipronil on the reproductive axis in an early life stage of the Japanese medaka (Oryzias latipes). Ecotoxicology 23:1044-1054. https://doi.org/10.1007/s10646-014-1248-0
  35. Tan H, Cao Y, Tang T, Qian K, Chen WL, Li J. 2008. Biodegradation and chiral stability of fipronil in aerobic and flooded paddy soils. Science of Total Environment 407:428-437. https://doi.org/10.1016/j.scitotenv.2008.08.007
  36. Tingle CC, Rother JA, Dewhurst CF, Lauer S, King WJ. 2003. Fipronil: Environmental fate, ecotoxicology, and human health concerns. Reviews of Environmental Contamination and Toxicology 176:1-66.
  37. Walters JL, De Iuliis GN, Nixon B, Bromfield EG. 2018. Oxidative stress in the male germline: A review of novel strategies to reduce 4-hydroxynonenal production. Antioxidants 7:132. https://doi.org/10.3390/antiox7100132
  38. Wang X, Martinez MA, Wu Q, Ares I, Martinez-Larranaga MR, Anadon A, Yuan Z. 2016. Fipronil insecticide toxicology: Oxidative stress and metabolism. Critical Reviews in Toxicology 46:876-899. https://doi.org/10.1080/10408444.2016.1223014
  39. Watanabe KH, Li Z, Kroll KJ, Villeneuve DL, Garcia-Reyero N, Orlando EF, Sepulveda MS, Collette TW, Ekman DR, Ankley GT, et al. 2009. A computational model of the hypothalamic-pituitary-gonadal axis in male fathead minnows exposed to 17α-ethinylestradiol and 17β-estradiol. Toxicological Sciences 109:180-192. https://doi.org/10.1093/toxsci/kfp069
  40. Wolfe MF, Seiber JN. 1993. Environmental activation of pesticides. Occupational Medicine 8:561-573.
  41. Yang X, Zhang X, Zhang J, Ji Q, Huang W, Zhang X, Li Y. 2019. Spermatogenesis disorder caused by T-2 toxin is associated with germ cell apoptosis mediated by oxidative stress. Environmental Pollution 251:372-379. https://doi.org/10.1016/j.envpol.2019.05.023
  42. Yi YJ, Adikari AAD, Moon ST, Lee SM, Heo JM. 2021. Effects of lipopolysaccharides on the maturation of pig oocytes. Korean Journal of Agricultural Science 48:163-170. https://doi.org/10.7744/KJOAS.20210010