Mercury at environmental relevant levels affects spermatozoa function and fertility capacity in bovine sperm

References

• Agarwal, A., M. Arafa, R. Chandrakumar, A. Majzoub, S. Al Said, and H. Elbardisi. 2017. A multicenter study to evaluate oxidative stress by oxidation-reduction potential, a reliable and reproducible method. Andrology 5:939–45. doi:10.1111/andr.12395.
   PubMed Web of Science ®Google Scholar
• Agarwal, A., G. Virk, C. Ong, and S. S. Du Plessis. 2014. Effect of oxidative stress on male reproduction. World J. Mens. Health 32:1–17. doi:10.5534/wjmh.2014.32.1.1.
   PubMedGoogle Scholar
• Ali, S. F., C. P. LeBel, and S. C. Bondy. 1992. Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13:637–48.
   PubMed Web of Science ®Google Scholar
• Alves, A. C., M. S. Monteiro, A. L. Machado, M. Oliveira, A. Boia, A. Correia, N. Oliveira, A. M. V. M. Soares, and S. Loureiro. 2017. Mercury levels in parturient and newborns from Aveiroo region Portugal. J. Toxicol. Environ. Health Part A 80:697–709. doi:10.1080/15287394.2017.1286926.
   PubMed Web of Science ®Google Scholar
• Arabi, M. 2005. Bull spermatozoa under mercury stress. Reprod. Domest. Anim. 40:454–59. doi:10.1111/j.1439-0531.2005.00607.x.
   PubMed Web of Science ®Google Scholar
• Arabi, M., and M. S. Heydarnejad. 2007. In vitro mercury exposure on spermatozoa from normospermic individuals. J. Biol. Sci. 10:2448–53. doi:10.3923/pjbs.2007.2448.2453.
   Google Scholar
• Arrifano, G. P. F., R. C. R. Martín-Doimeadios, M. Jiménez-Moreno, V. Ramírez-Mateos, N. F. S. Silva, J. R. Souza-Monteiro, M. Augusto- Oliveira, R. S. O. Paraense, B. M. Macchi, and J. L. M. Do Nascimento. 2017. Large-scale projects in the Amazon and human exposure to mercury: The case study of the Tucuruí. Ecotoxicol. Environ. Saf. 147:299–305. doi:10.1016/j.ecoenv.2017.08.048.
   PubMed Web of Science ®Google Scholar
• Barbosa, J. F. 2017. Toxicology of metals and metalloids: Promising issues for future studies in environmental health and toxicology. J. Toxicol. Environ. Health Part A 80:137–44. doi:10.1080/15287394.2016.1259475.
   PubMed Web of Science ®Google Scholar
• Barth, A. D., and R. J. Oko. 1989. Abnormal morphology of bovine spermatozoa. 1 ed. Iowa, USA: State University Press.
   Google Scholar
• Benzie, I. F., and J. J. Strain. 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal. Biochem. 239:70–77. doi:10.1006/abio.1996.0292.
   PubMed Web of Science ®Google Scholar
• Bergamo, P., Volpe, M. G., Lorenzetti, S., Mantovani, A., Notari, T., Cocca, E., et al. 2016. Human semen as an early, sensitive biomarker of highly polluted living environment in healthy men: A pilot biomonitoring study on trace elements in blood and semen and their relationship with sperm quality and RedOx status. Reprod. Toxicol. 66:1–9. doi:10.1016/j.reprotox.2016.07.018.
   PubMed Web of Science ®Google Scholar
• Boujbiha, M. A., K. Hamden, F. Guermazi, A. Bouslama, A. Omezzine, A. Kammoun, and A. E. Feki. 2009. Testicular toxicity in mercuric chloride treated rats: Association with oxidative stress. Reprod. Toxicol. 28:81–89. doi:10.1016/j.reprotox.2009.03.011.
   PubMed Web of Science ®Google Scholar
• Branco, V., S. Caito, M. Farina, J. T. Da Rocha, M. Aschner, and C. Carvalho. 2017. Biomarkers of mercury toxicity: Past, present and future trends. J Toxicol Environ. Health B 20:119–54. doi:10.1080/10937404.2017.1289834.
   PubMed Web of Science ®Google Scholar
• Buck Louis, G. M., Sundaram, R., Schisterman, E. F., Sweeney, A. M., Lynch, C. D., and Gore-Langton, R. E. 2012. Heavy metals and couple fecundity, the LIFE Study. Chemosphere 87:1201–07. doi:10.1016/j.chemosphere.2012.01.017.
   PubMed Web of Science ®Google Scholar
• Carneiro, M. F. H., D. Grotto, and F. Barbosa Jr. 2014. Inorganicand methylmercury levels in plasma are differentially associated with age, gender, and oxidative stress markers in a population exposed to mercury through fish consumption. J. Toxicol. Environ. Health Part A 77:69–79. doi:10.1080/15287394.2014.865584.
   PubMed Web of Science ®Google Scholar
• Castellini, C., Mourvakia, E., Sartini, B., Cardinali, R., Moretti, E., and Collodel, G. 2009. In vitro toxic effects of metal compounds on kinetic traits and ultrastructure of rabbit spermatozoa. Reprod. Toxicol. 27:46–54. doi:10.1016/j.reprotox.2008.12.003.
   PubMed Web of Science ®Google Scholar
• Castilhos, Z., Rodrigues-Filho, S., Cesar, R., Rodrigues, A. P., Villasbôas, R., and Jesus, I. 2015. Human exposure and risk assessment associated with mercury contamination in artisanal gold mining areas in the Brazilian Amazon. Environ. Sci Pollut. Res. Int. 22:11255–64. doi:10.1007/s11356-015-4340-y.
   PubMed Web of Science ®Google Scholar
• Celeghini, E. C. C., A. F. C. Andrade, C. F. Raphael, J. Nascimento, J. S. Ticianelli, and R. P. Arruda. 2010. Damage assessment of the equine sperm membranes by fluorimetric technique. Braz. Arch. Biol. Technol. 53:1285–92. doi:10.1590/S1516-89132010000600004.
   Web of Science ®Google Scholar
• Choy, C. M., Q. S. Yeung, C. M. Briton-Jones, C. K. Cheung, C. W. Lam, and C. J. Haines. 2002. Relationship between semen parameters and mercury concentrations in blood and in seminal fluid from subfertile males in Hong Kong. Fertil. Steril. 78:426–28. doi:10.1016/s0015-0282(02)03232-6.
   PubMed Web of Science ®Google Scholar
• Clarkson, T., and L. Magos. 2006. The toxicology of mercury and its chemical compounds. Crit. Rev. Toxicol. 36:609–62. doi:10.1080/10408440600845619.
   PubMed Web of Science ®Google Scholar
• Cole, D. C., B. Wainman, L. H. Sanin, J. P. Weber, H. Muggah, and S. Ibrahim. 2006. Environmental contaminant levels and fecundability among non-smoking couples. Reprod. Toxicol. 22:13–19. doi:10.1016/j.reprotox.2005.12.001.
   PubMed Web of Science ®Google Scholar
• Da Silva, R. R., B. J. Castelo, S. M. T. Thomaz, and A. Cesar. 2017. Minamata Convention: Analysis of the socio-environmental impacts of a long-term solution. Saúde Debate 41:50–62. doi:10.1590/0103-11042017S205.
   Google Scholar
• Gordon, I. R. 2003. Laboratory production of cattle embryos, 576. Biotechnology in Agriculture Series. Oxford, UK: CABI Publishing.
   Google Scholar
• Guimarães, A. C., F. G. Leivas, F. W. Santos, E. B. Schwengber, A. B. Giotto, and C. I. Machado. 2014. Reduction of centrifugation force in discontinuous Percoll gradients increases in vitro fertilization rates without reducing bovine sperm recovery. Anim. Reprod. Sci. 146:103–10. doi:10.1016/j.anireprosci.2014.02.016.
   PubMed Web of Science ®Google Scholar
• Hatef, A., S. M. H. Alavi, I. A. E. Butts, T. Policar, and O. Linhart. 2011. Mechanism of action of mercury on sperm morphology, adenosine triphosphate content, and motility in Perca fluviatilis (Percidae; Teleostei). Environ. Toxicol. Chem. 30:905–14. doi:10.1002/etc.461.
   PubMed Web of Science ®Google Scholar
• Heath, J. C., Y. Abdelmageed, T. D. Braden, and H. O. Goyal. 2012. The effects of chronic ingestion of mercuric chloride on fertility and testosterone levels in male Sprague Dawley rats. J. Biomed. Biotechnol. 815186. doi:10.1155/2012/815186.
   PubMedGoogle Scholar
• Idrovo, A. J., L. H. Sanín, and D. C. Cole. 2005. Evaluation of time-to-pregnancy as a measure in environmental epidemiology. Biomedica. 25:398–411.
   PubMedGoogle Scholar
• Kalender, S., F. G. Uzun, F. Demir, M. Uzunhisarcikli, and A. Aslanturk. 2013. Mercuric chloride-induced testicular toxicity in rats and the protective role of sodium selenite and vitamin E. Food Chem. Toxicol. 55:456–62. doi:10.1016/j.fct.2013.01.024.
   PubMed Web of Science ®Google Scholar
• Khoury, E. D. T., G. S. Souza, L. C. L. Silveira, C. A. Costa, A. A. Araújo, and M. C. N. Pinheiro. 2013. Neurological manifestations in riverine populations from areas exposed to mercury in the Brazilian Amazon. Cad. Saúde Pública 29:2307–18. doi:10.1590/0102-311X00158012.
   PubMed Web of Science ®Google Scholar
• Kim, K., V. Y. Fujimoto, P. J. Parsons, A. J. Steuerwald, R. W. Browne, and M. S. Bloom. 2014. Recent cadmium exposure among male partners may affect oocyte fertilization during in vitro fertilization (IVF). J. Assist. Reprod. Genet. 27:463–68. doi:10.1007/s10815-010-9437-0.
   Google Scholar
• Kollár, T., E. Kása, A. Ferincz, B. Urbányi, Z. Csenki-Bakos, and A. Horváth. 2018. Development of an in vitro toxicological test system based on zebrafish (Danio rerio) sperm analysis. Sci. Pollut. Res. Int. 25:14426–36. doi:10.1007/s11356-018-1613-2.
   PubMed Web of Science ®Google Scholar
• Langbeen, A., H. F. M. De Porte, E. Bartholomeus, J. L. M. R. Leroy, and P. E. J. Bols. 2015. Bovine in vitro reproduction models can contribute to the development of (female) fertility preservation strategies. Theriogenology 84:477–89. doi:10.1016/j.theriogenology.2015.04.009.
   PubMed Web of Science ®Google Scholar
• Levine, H., N. Jørgensen, A. Martino-Andrade, J. Mendiola, D. Weksler-Derri, and I. Mindlis. 2017. Temporal trends in sperm count: A systematic review and meta-regression analysis. Human Reprod. Update 23:646–59. doi:10.1093/humupd/dmx022.
   PubMed Web of Science ®Google Scholar
• Lomeo, A. M., and A. M. Giamberso. 1991. Water-test: A simple method to assess sperm-membrane integrity. Int. J. Androl. 14:278–82.
   PubMedGoogle Scholar
• Lorschieder, F. L., M. J. Vimy, and A. O. Summers. 1995. Mercury exposure from “silver” tooth filling: Emerging evidence questions a traditional dental paradigm. FASEB J. 9:504–08. doi:10.1096/fasebj.9.7.7737458.
   PubMed Web of Science ®Google Scholar
• Martinez, C. S., A. G. Escobar, J. G. D. Torres, D. S. Brum, F. W. Santos, M. J. Alonso, M. Salaices, D. V. Vassallo, F. M. A. Peçanha, F. G. Leivas, et al. 2014b. Chronic exposure to low dioses of mercury impairs sperm quality and induces oxidative dstress in rats. J. Toxicol. Environ. Health Part A 77:143–54. doi:10.1080/15287394.2014.867202.
   PubMed Web of Science ®Google Scholar
• Martinez, C. S., F. M. Peçanha, D. S. Brum, F. W. Santos, J. L. Franco, and A. P. P. Zemolin. 2016. Reproductive dysfunction after mercury exposure at low levels: Evidence for a role of glutathione peroxidase (GPx) 1 and GPx4 in male rats. Reprod. Fertil. Dev. doi:10.1071/RD16310.
   Web of Science ®Google Scholar
• Martinez, C. S., J. G. D. Torres, F. M. Peçanha, J. A. Anselmo-Franci, D. V. Vassallo, and M. Salaices. 2014a. 60-Day chronic exposure to low concentrations of HgCl2 impairs sperm quality: Hormonal imbalance and oxidative stress as potential routes for reproductive dysfunction in rats. PLoSOne 9:e111202. doi:10.1371/journal.pone.0111202.
   PubMed Web of Science ®Google Scholar
• Mínguez-Alarcóna, L., M. C. Afeichea, P. L. Williams, M. Arvizud, C. Tanrikute, and C. J. Amarasiriwardenag. 2017. Hair mercury (Hg) levels, fish consumption and semen parameters among men attending a fertility center International. J. Hyg. Environ. Health. doi:10.1016/j.ijheh.2017.10.014.
   Web of Science ®Google Scholar
• Mortimer, S. T. 2000. CASA-practical aspects. J. Androl. 21:515–24.
   PubMedGoogle Scholar
• Muthu, K., and P. Krishnamoorthy. 2012. Effect of vitamin C and vitamin E on mercuric chloride-induced reproductive toxicity in male rats. Biochem. Pharmacol. 1:102–07. doi:10.4172/2167-0501.1000102.
   Google Scholar
• National Academy of Sciences. 2000. Toxicological effects of methylmercury. National Research Council, Washington, DC, USA.
   Google Scholar
• Ohkawa, H., N. Ohishi, and K. Yagi. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351–58.
   PubMed Web of Science ®Google Scholar
• Oliveira, C. S., V. A. Oliveira, L. M. Costa, T. P. Pedroso, M. M. Fonseca, J. S. Bernardi, T. L. Fiuza, and M. E. Pereira. 2016. Inorganic mercury exposure in drinking water alters essential metal homeostasis in pregnant rats without altering rat pup behavior. Reprod. Toxicol. 65:18–23. doi:10.1016/j.reprotox.2016.06.013.
   PubMed Web of Science ®Google Scholar
• Organização Pan-Americana da Saúde - OPAS. 2011. Cooperação Técnica entre Brasil, Bolívia e Colômbia: Teoria e Prática para o Fortalecimento da Vigilância em Saúde de Populações Expostas a Mercúrio. Brasília, Brazil.
   Google Scholar
• Parrish, J. J., A. Krogenaes, and J. L. Susko-Parrish. 1995. Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44:859–69.
   PubMed Web of Science ®Google Scholar
• Parrish, J. J., J. L. Susko-Parrish, M. L. Leibfried-Rutledge, E. S. Critser, W. H. Eyestone, and N. L. First. 1986. Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25:591–600.
   PubMed Web of Science ®Google Scholar
• Rao, M. V., and B. Gangadharan. 2008. Antioxidative potential of melatonin against mercury induced intoxication in spermatozoa in vitro. Toxicol. In Vitro 22:935–42. doi:10.1016/j.tiv.2008.01.014.
   PubMed Web of Science ®Google Scholar
• Rim, K. T. 2017. Reproductive toxic chemicals at work and efforts to protect workers’ health: A literature review. Saf. Health Work 8:143–50. doi:10.1016/j.shaw.2017.04.003.
   PubMed Web of Science ®Google Scholar
• Rizzetti, D. A., C. S. Martinez, A. G. Escobar, T. M. Silva, J. A. Uranga-Ocio, and F. M. Peçanha. 2017. Egg white-derived peptides prevent male reproductive dysfunction induced by mercury in rats. Food Chem. Toxicol. 100:253–64. doi:10.1016/j.fct.2016.12.038.
   PubMed Web of Science ®Google Scholar
• Santos, R. R., E. Schoevers, and B. A. J. Roelen. 2014. Usefulness of bovine and porcine IVM/IVF models for reproductive toxicology. Reprod. Biol. Endocrinol. 12:117. doi:10.1186/1477-7827-12-117.
   PubMed Web of Science ®Google Scholar
• Silva, F., C. T. Teixeira, W. R. Scarano, A. P. A. Favareto, C. D. B. Fernandez, D. Grotto, F. Barbosa Jr., and W. G. Kempinas. 2011. Effects of methylmercury on male reproductive functions in Wistar rats. Reprod. Toxicol. 31:431–39. doi:10.1016/j.reprotox.2011.01.002.
   PubMed Web of Science ®Google Scholar
• Takeda, S. H. K., R. Kuno, F. Barbosa, and N. Gouveia. 2017. Trace element levels in blood and associated factors in adults living in the metropolitan area of Sao Paulo, Brazil. J. Trace. Elem. Med. Biol. 44:307–14. doi:10.1016/j.jtemb.2017.09.005.
   PubMed Web of Science ®Google Scholar
• Tessaro, I., Modina, S. C., Crotti, G., Franciosi, F., Colleoni, S., and Lodde, V. 2015. Transferability and interlaboratory variability assessment of the in vitro bovine oocyte fertilization test. Reprod. Toxicol. 51:106–13. doi:10.1016/j.reprotox.2015.01.001.
   PubMed Web of Science ®Google Scholar
• UNEP, United Nations Environment Programme. 2013. Global mercury assessment: sources, emissions, releases and environmental transport. Geneva, Switzerland: Chemicals Branch.
   Google Scholar
• Vasconcelos, A. B., M. A. Santana, A. M. Santos, M. M. Santoro, and M. A. Lagares. 2010. Metabolic evaluation of cooled equine spermatozoa. Andrologia 42:106–11. doi:10.1111/j.1439-0272.2009.00963.x.
   PubMed Web of Science ®Google Scholar
• Verstegen, J., M. Iguer-Ouada, and K. Onclin. 2002. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology 57:149–79.
   PubMed Web of Science ®Google Scholar
• Yoisungnern, T., Y.-J. Choi, J. W. Han, M.-H. Kang, J. Das, and S. Gurunathan. 2015b. Internalization of silver nanoparticles into mouse spermatozoa results in poor fertilization and compromised embryo development. Sci Rep 5:11170. doi:10.1038/srep11170.
   PubMed Web of Science ®Google Scholar
• Yoisungnern, T., J. Das, Y.-J. Choi, R. Parnpai, and J.-H. Kim. 2015a. Effect of hexavalent chromium-treated sperm on in vitro fertilization and embryo development. Toxicol. Ind. Health. doi:10.1177/0748233715579805.
   PubMed Web of Science ®Google Scholar
• Zafar, A., S. A. M. A. S. Eqani, N. Bostan, A. Cincinelli, F. Tahir, and S. T. A. Shah. 2015. Toxic metals signature in the human seminal plasma of Pakistani population and their potential role in male infertility. Environ. Geochem. Health 37:515–27. doi:10.1007/s10653-014-9666-8.
   PubMed Web of Science ®Google Scholar
• Zhang, Q. F., Y. W. Li, Z. H. Liu, and Q. L. Chen. 2016. Reproductive toxicity of inorganic mercury exposure in adult zebrafish: Histological damage, oxidative stress, and alterations of sex hormone and gene expression in the hypothalamic-pituitary-gonadal axis. Aquat. Toxicol. 177:417–24. doi:10.1016/j.aquatox.2016.06.018.
   PubMed Web of Science ®Google Scholar