Abstract
Triphenyltin (TPT) is an organotin compound (OT), primarily used in agriculture and in the composition of antifouling paints for ships worldwide. Studies have showed its effects as an endocrine disrupter in several organisms by preventing enzymatic expression and causing reproductive toxicity. This study aimed to evaluate the effects of exposure to TPT, via breastfeeding, on reproductive physiology in the Calomys laucha species. The experimental design was compound of five groups, two controls and three with different doses of TPT. Moreover, females were exposed by gavage to the TPT for 20 days, from the 1st day postpartum to the 21st postnatal day (PND). Then, the pups were euthanized and the kinetics, organelles, and biochemistry of the sperm were evaluated. The results presented a reduction in total motility in the groups exposed to TPT. Regarding cellular organelles analysis, a loss in membrane integrity was evidenced; the functionality of mitochondria showed diminution followed by increased acrosome reaction. In conclusion, the TPT causes alteration of the reproductive parameters, decreasing the activity and sperm quality in individuals exposed in the breastfeeding phase.
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Abdollahi M, ranjbar A, shadnia S, nikfar S, rezaie A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10:141–147
Aitken RJ, Nixo B, Lin M, Koppers AJ, Lee YH, Baker MA (2007) Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 9:554–564
Antes FG, Krupp E, Flores EMM, Dressler VL, Feldmann J (2011) Speciation and degradation of triphenyltin in typical paddy fields and its uptake into riceplants. Environ Sci Technol 45:10524–10530
Bergamini CM, Gambetti S, Dondi A, Cervellati C (2004) Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des 10:1611–1626
Bonarska-Kujawa D, Kleszczy’nska H, Przestalski S (2012) The location of organotins within the erythrocyte membrane in relation to their toxicity. EcotoxicolEnviron Saf 78:232–238
Casas JS, Couce MD, Sánchez A, Seoane R, Sordo J, Perez-Estévez A, Vázquez-López E (2018) Triphenyltin derivatives of sulfanylcarboxylic esters. J Inorg Biochem 180:163–170
Chernoff N, Stezer RW, Miller DB, Rosen MB, Rogers JM (1990) Effects of chemically induced maternal toxicity on prenatal development in the rat. Teratology 42:651–658
Colares EP (1997) Aspectos da Aspectos da fisiologia reprodutiva de Calomys laucha OLFERS, 1818 (Mammalia: Rodentia). Tese de doutorado, USP – São Paulo
Cooke GM, Fordsyth DS, Bondy GS, Tachon R, Tague B, Coady L (2008) Organotin speciation and tissue distribution in rat dams, fetus, and neonates following oral administration of tributyltin chloride. J Toxicol Environ Health A 71(6):384–395
Cox JF, Alfaro V, Montenegro V, Rodriguez-Martinez H (2006) Computer-assisted analysis of sperm motion in goats and its relationship with sperm migration in cervical mucus. Theriogenology 66:860–867
De Simplicio P, Dacasto P, Carletti M, Giannerini F, Nebbia C (2000) Changes in hepatic and renal glutathione-dependent enzyme activities in rabbits and lambs subchronically treated with triphenyltin acetate. Vet Hum Toxicol 42(3):159–162
Delgado Filho VS, Lopes PFI, Podratz PL, Gracel JB (2011) Triorganotin as a compound with potential reproductive toxicity in mammals. Braz J Med Biol Res 44(9):958–965
Domínguez-Rebolledo AE, Martínez-Pastor F, Bisbal AF, Ros-Santaella JL, García-Álvarez O, Maroto-Morales A, Soler AJ, Garde JJ, Fernández-Santos MR (2011) Response of thawed epidydimal red deer spermatozoa to increasing concentrations of hydrogen peroxide, and importance of individual male variability. Reprod Domest Anim 46:93–403
FAO Pesticide residues in food (1991) Evaluations, part I – residues. Food and Agriculture Organization of the United Nations, Rome, pp 337–371
Fent K (1996) Ecotoxicology of organotin compounds. Crit Rev Toxicol 26:1–117
Fernández-Gago R, Domínguez JC, Martínez-Pastor F (2013) Seminal plasma applied post-thawing affects boar sperm physiology: a flow cytometry study. Theriogenology 80:400–410
Fitas AL, Amaral D, Lopes L (2014) Aromatase inhibitors in male adolescents with idiopathic short stature. Revista Portuguesa de Endocrinologia. Diabetes Metab 9(1):53–58
Gao J, Ye J, Ma J, Tang L, Huang J (2014) Biosorption and biodegradation of triphenyltin by Stenotrophomonas maltophilia and their influence on cellular metabolism. J Hazard Mater 276:112–119
Gillan L, Evans G, Maxwell WMC (2005) Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63:445–457
Grote K, Stahlschimidt B, Talsness CE, Gericke C, Appel KE, Chahoud I (2004) Effects of organotin compounds on pubertal male rats. Toxicology 202:145–158
Grote K, Hobler C, Andrade AJ, Grande SW, Gericke C, Talsness CE, Appel KE, Chahoud I (2009) Sex differences in effects on sexual development in rat offspring after pre- and postnatal exposure to triphenyltin chloride. Toxicology 260(1–3):53–59
Hiroguchi T (2006) Masculinization of female gastropod mollusks induced by organotin compounds, focusing on mechanism of actions of tributyltin and triphenyltin for development of imposex. Environ Sci 13(2):77–87
Hobler C, Andrade AJM, Grande SW, Gericke C, Talsness CE, Appel KE, Chahoude I, Grote K (2010) Sex-dependent aromatase activity in rat offspring afterpre- and postnatal exposure to triphenyltin chloride. Toxicology 276:198–205
Horie Y, Watanabe H, Takanobu H, Yoshiko S, Yamagishi T, Iguchi T, Tatarazako N (2017) Effects of thiphenyltin on reproduction in Japanese medaka (Oryzias latipes) across two generations. Aquat Toxicol 192:16–23
Jenkins TG et al (2014) Intra-sample heterogeneity of sperm DNA methylation. MHR: Basic science of reproductive medicine 21(4):313–319. https://doi.org/10.1093/molehr/gau115
Kishita O, Adeeko A, Li D, Luu T, Brawer JR, Morales C (2007) In utero exposure to tributyltin chloride differentially alters male and female fetal gonad morphology and gene expression profiles in the Sprague-Dawley rat. Reprod Toxicol 23:1–11
Martínez-Alborcia MJ, Valverde A, Parrilha I, Vazquez JM, Martinez EA, Roca J (2012) Detrimental effects of non-functional spermatozoa on the freezability of functional spermatozoa from boar ejaculate. PLoS One 7:e36550
Martínez-Pastor F, Mata-Campuzano M, Álvarez-Rodriguez M, Álvarez M, Anel L, Paz P (2010) Probes and techniques for sperm evaluation by flow cytometry. Reprod Domest Anim 45:67–78
Mello MSC, Delgado IF, Favoreto AOA, Lopes CMT, Batista MM, Kempinas WDG, Paumgartten FJR (2015) Sexual maturation and fertility of mice exposed totriphenyltin during prepubertal and pubertal periods. Toxicol Rep 2:405–414
Meng PJ, Lin J, Liu LL (2009) Aquatic organotin pollution in Taiwan. J Environ Manag 90:8–15
Mills JN, Ellis BA, Childs JE, Maiztegui JL, Castro-Vasquez A (1992) Seasonal changes in mass and reproductive condition of the corn mouse (Calomys musculinus) on the Argentine pampa. J Mammal 73:876–884
Mino Y, Amano F, Yoshioka T, Konishi Y (2008) Determination of organotins in human breast milk by gas chromatography with flame photometric detection. J Health Sci 54(2):224–228
Mortimer ST (2000) CASA- practical aspects. J Androl:515–524
Petrunkina AM, Volker G, Brandt H, Topfer-Petersen E, Waberski D (2005) Functional significance of responsiveness to capacitating conditions in boar spermatozoa. Theriogenology 64:1766–1782
Reddy PS, Pushpalatha T, Sreenivasul A, Reddy P (2006) Reduction of spermatogenesis and steroidogenesis in mice after fentin and fenbutatin administration. Toxicol Lett 166(1):53–59
Silva EF, Varela Junior AS, Cardoso TF, Stefanello FM, Kalb AC, Martinez PE, Corcini CD (2016) Reproductive toxicology of 2,4 dinitrophenol in boar sperm. Toxicol in Vitro 35:31–35
Smith KS (1981) 14-C-TPTH residue levels in milk and tissues of lactating dairy cows. Cannon Laboratories, USA. Report Project of 7489 [cited in FAO, 1991]
Van Weert JM, Repping S, Van Voorhis BJ, Van Der Veen F, Bossuyt PM, Mol BW (2004) Performance of the postwash total motile sperm count as a predictor of pregnancy at the time of intrauterine insemination: a meta-analysis. Fertil Steril 11:612–620
Verstegen J, Iguer-Ouada M, Onclin K (2002) Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology 57:149–179
Wang BA, Li M, Mu YM, Lu ZH, Li JY (2006) Effects of tributyltin chloride (TBT) and triphenyltin chloride (TPT) on rat testicular Leydig cells. Zhonghua Nan Ke Xue - Natl J Androl 12:516–519
Ye JS, Yin H, Peng H, Bai JQ, Xie DP, Wang LL (2013) Biosorption and biodegradation of triphenyltin by Brevibacillus brevis. Bioresour Technol 129:236–241
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All procedures were carried out in accordance with applicable standards and in the normative resolutions and guidelines of the National Council for Control of Animal Experimentation, approved by the Ethics Committee on Animal Use (CEUA-FURG) under the number Pq017 / 2014.
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de Castro, T.F., Varela Junior, A.S., Padilha, F.F. et al. Effects of exposure to triphenyltin (TPT) contaminant on sperm activity in adulthood of Calomys laucha exposed through breastfeeding. Environ Sci Pollut Res 26, 8280–8288 (2019). https://doi.org/10.1007/s11356-019-04365-1
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DOI: https://doi.org/10.1007/s11356-019-04365-1