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Effects of oral administration of titanium dioxide particles on sperm ‎parameters and in vitro fertilization potential in mice: A comparison ‎between nano- and fine-sized particles

Document Type : Original Article

Authors

1 Department of Anatomy and Histology, Faculty of Medicine, Urmia University of Medical Sciences, Urmia, Iran

2 Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract

Titanium dioxide particles (TiO2) as the second most widely used materials in consumer products are composed of nano-sized (100 nm) particles (FPs). Toxicological studies on animals have shown that TiO2 NPs exposure can cross the blood-testis barrier and accumulate in the testis resulting in testicular tissue damage and reduction of sperm count and motility. However, there is no information on the toxic effects of TiO2 FPs on male reproductive fertility. Twenty-four adult male mice were randomly divided into three groups including control, TiO2 NPs, and TiO2 FPs (150 mg kg-1 per day). After intragastric administration for 35 days, testicular tissue alterations (seminiferous tubule diameter and germinal epithelial height), sperm parameters (count, motility, viability, morphology, and DNA quality), in vitro fertilization potential, oxidative stress assays such as malondialdehyde (MDA) content, level of glutathione (GSH) and activities of superoxide dismutase (SOD) and glutathione peroxidase (GPx) in testicular tissue were investigated. The results showed that both sizes of TiO2 caused pathologic changes in the testis and significantly increased MDA level and decreased GSH levels and activities of SOD and GPx in testicular tissue. Moreover, the administration of both sizes of TiO2 significantly decreased all of the sperm parameters and in vitro fertility (fertilization rate and pre-implantation embryos development) compared to control. Administration of TiO2 FPs similar to TiO2 NPs through inducing damages to testis led to a marked reduction in sperm quality, in vitro fertilization, and embryos development in male mice.

Keywords

References
  1. Zhao X, Ze Y, Gao G, et al. Nanosized TiO2-induced reproductive system dysfunction and its mechanism in female mice. PLoS One 2013; 8: e59378. doi: 10.1371/ journal.pone.0059378.
  2. Gu N, Hu H, Guo Q, et al. Effects of oral administration of titanium dioxide fine-sized particles on plasma glucose in mice. Food Chem Toxicol 2015; 86: 124-131.
  3. Dorier M, Brun E, Veronesi G, et al. Impact of anatase and rutile titanium dioxide nanoparticles on uptake carriers and efflux pumps in Caco-2 gut epithelial cells. Nanoscale 2015; 7(16):7352-7360.
  4. Bakare AA, Udoakang AJ, Anifowoshe AT, et al. Genotoxicity of titanium dioxide nanoparticles using the mouse bone marrow micronucleus and sperm morphology assays. J Pollut Eff Cont 2016; 4: 2. doi: 10.4172/2375-4397.1000156.
  5. Jia X, Wang S, Zhou L, et al. The potential liver, brain, and embryo toxicity of titanium dioxide nanoparticles on mice. Nanoscale Res Lett 2017; 12: 478. doi: 10. 1186/s11671-017-2242-2.
  6. Hong F, Zhao X, Si W, et al. Decreased spermatogenesis led to alterations of testis-specific gene expression in male mice following nano-TiO2 exposure. J Hazard Mater 2015; 300: 718-728.
  7. Reeves JF, Davies SJ, Dodd NJF, et al. Hydroxyl radicals (*OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat Res 2008; 640(1-2): 113-122.
  8. Nichols CE, Shepherd DL, Hathaway QA, et al. Reactive oxygen species damage drives cardiac and mitochondrial dysfunction following acute nano-titanium dioxide inhalation exposure. Nanotoxicology 2018; 12(1): 32-48.
  9. Chen E, Ruvalcaba M, Araujo L, et al. Ultrafine titanium dioxide nanoparticles induce cell death in human bronchial epithelial cells. J Exp Nanosci 2008; 3(3): 171-183.
  10. Weir A, Westerhoff P, Fabricius L, et al. Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol 2012; 46(4): 2242-2250.
  11. Singh S, Shi T, Duffin R, et al. Endocytosis, oxidative stress and IL-8 expression in human lung epithelial cells upon treatment with fine and ultrafine TiO2: role of the specific surface area and of surface methylation of the particles. Toxicol Appl Pharmacol 2007; 222(2):141-151.
  12. Sager TM, Kommineni C, Castranova V. Pulmonary response to intratracheal instillation of ultrafine versus fine titanium dioxide: role of particle surface area. Part Fibre Toxicol 2008; 5: 17. doi: 10.1186/ 1743-8977-5-17.
  13. Falck GCM, Lindberg HK, Suhonen S, et al. Genotoxic effects of nanosized and fine TiO2. Hum Exp Toxicol 2009; 28(6-7):339-352.
  14. Khorsandi L, Orazizadeh M, Mansouri E, et al. Morpho-metric and stereological assessment of the effects of titanium dioxide nanoparticles on the mouse testicular tissue. Bratisl Lek Listy 2016; 117(11): 659-664.
  15. Hess RA, Chen P. Computer tracking of germ cells in the cycle of the seminiferous epithelium and prediction of changes in cycle duration in animals commonly used in reproductive biology and toxicology. J Androl 1992; 13(3): 185-190.
  16. Mozafari AA, Shahrooz R, Ahmadi A, et al. Protective effect of ethyl pyruvate on mice sperm parameters in phenylhydrazine induced hemolytic anemia. Vet Res Forum 2016; 7(1): 63-68.
  17. Badkoobeh P, Parivar K, Kalantar SM, et al. Effect of nano-zinc oxide on doxorubicin-induced oxidative stress and sperm disorders in adult male Wistar rats. Iran J Reprod Med. 2013; 11(5): 355-364.
  18. Ahmadi A, Chafjiri SB, Sadrkhanlou RA. Effect of Satureja khuzestanica essential oil against fertility disorders induced by busulfan in female mice. Vet Res Forum 2017; 8(4): 281-286.
  19. Narayana K, Verghese S, Jacob SS. l-Ascorbic acid partially protects two cycles of cisplatin chemo-therapy-induced testis damage and oligo-astheno-teratospermia in a mouse model. Exp Toxicol Pathol 2009; 61(6): 553-563.
  20. Jafari A, Baghaei A, Solgi R, et al. An electro-cardiographic, molecular and biochemical approach to explore the cardioprotective effect of vasopressin and milrinone against phosphide toxicity in rats. Food Chem Toxicol 2015; 80: 182-192.
  21. Hu ML. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol 1994; 233: 380-385.
  22. Jafari A, Rasmi Y, Hajaghazadeh M, et al. Hepato-protective effect of thymol against subchronic toxicity of titanium dioxide nanoparticles: Biochemical and histological evidences. Environ Toxicol Pharmacol 2018; 58: 29-36.
  23. Warheit DB, Webb TR, Sayes CM, et al. Pulmonary instillation studies with nanoscale TiO2 rods and dots in rats: toxicity is not dependent upon particle size and surface area. Toxicol Sci 2006; 91(1):227-236.
  24. Orazizadeh M, Khorsandi L, Absalan F, et al. Effect of beta-carotene on titanium oxide nanoparticles-induced testicular toxicity in mice. J Assist Reprod Genet 2014; 31(5): 561-568.
  25. Guo LL, Liu XH, Qin DX, et al. Effects of nanosized titanium dioxide on the reproductive system of male mice [Chinese]. Zhonghua Nan Ke Xue 2009; 15(6): 517-522.
  26. Khaki A, Heidari M, Ghaffari Novin M, et al. Adverse effects of ciprofloxacin on testis apoptosis and sperm parameters in rats. Iran J Reprod Med 2008; 6(2): 71-76.
  27. Working P, Chellman G. The testis, spermatogenesis and the excurrent duct system. In: Scialli AR, Zinaman MJ (Eds). Reproductive toxicology and infertility. New York, USA: McGraw Hill. 1993:55-76.
  28. Miura N, Ohtani K, Hasegawa T, et al. Hazardous effects of titanium dioxide nanoparticles on testicular function in mice. Fund Toxicol Sci 2014; 1(3): 81-85.
  29. Wyrobek AJ, Gordon LA, Burkhart JG, et al. An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals. A report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutat Res 1983; 115(1): 1-72.
  30. Saacke RG. What is a BSE–SFT standards: the relative importance of sperm morphology: an opinion. Proc Soc Theriogenol 2001; 81-87.
  31. Narayana K, D’Souza UJA, Seetharama Rao K. Ribavirin-induced sperm shape abnormalities in Wistar rat. Mutat Res 2002; 513(1-2): 193-196.
  32. Giri S, Prasad SB, Giri A, et al. Genotoxic effects of malathion: an organophosphorus insecticide, using three mammalian bioassays in vivo. Mutat Res 2002; 514(1-2): 223-231.
  33. Bruce WR, Heddle JA. The mutagenic activity of 61 agents as determined by the micronucleus, Salmonella, and sperm abnormality assays. Can J Genet Cytol 1979; 21(3): 319-334.
  34. Kubo-Irie M, Shinkai Y, Matsuzawa S, et al. Prenatal exposure to rutile-type alumina-coated titanium dioxide nanoparticles impairs mouse spermatogenesis. Fundam Toxicol Sci 2016; 3(2): 67-74.
  35. Lewis SEM, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res 2005; 322(1): 33-41.
  36. Zini A. Are sperm chromatin and DNA defects relevant in the clinic? Syst Biol Reprod Med 2011; 57(1-2): 78-85.
  37. Morgan AM, El-Hamid MAI, Noshy PA. Reproductive toxicity investigation of titanium dioxide nanoparticles in male albino rats. World J Pharm Pharmaceut Sci. 2015; 4(10): 34-49.
  38. Ozokutan BH, Küçükaydın M, Muhtaroğlu S, et al. The role of nitric oxide in testicular ischemia-reperfusion injury. J Pediatr Surg 2000; 35(1): 101-103.
  39. Komatsu T, Tabata M, Kubo-Irie M, et al. The effects of nanoparticles on mouse testis Leydig cells in vitro. Toxicol In Vitro 2008; 22(8): 1825-1831.
  40. Gao G, Ze Y, Zhao X, et al. Titanium dioxide nano-particle-induced testicular damage, spermatogenesis suppression, and gene expression alterations in male mice. J Hazard Mater 2013; 258-259: 133-143.
  41. Jia F, Sun Z, Yan X, et al. Effect of pubertal nano-TiO2 exposure on testosterone synthesis and spermato-genesis in mice. Arch Toxicol 2014; 88(3):781-788.
  42. Hess RA, Nakai M. Histopathology of the male reproductive system induced by the fungicide benomyl. Histol Histopathol 2000; 15: 207-224.
  43. Bhattacharya K, Davoren M, Boertz J, et al. Titanium dioxide nanoparticles induce oxidative stress and DNA-adduct formation but not DNA-breakage in human lung cells. Part Fibre Toxicol 2009; 6: 17. doi: 10.1186/ 1743-8977-6-17.
  44. Miura N, Ohtani K, Hasegawa T, et al. High sensitivity of testicular function to titanium nanoparticles. J Toxicol Sci 2017; 42(3): 359-366.
Veterinary Research Forum
Volume 11, Issue 4
December 2020
Pages 401-408
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History
  • Receive Date: 11 July 2018
  • Revise Date: 26 October 2018
  • Accept Date: 03 November 2018
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