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Environmental Science and Pollution Research

, Volume 24, Issue 36, pp 27905–27912 | Cite as

Morphological and morphometrical changes on adult Wistar rat testis caused by chronic sodium arsenite exposure

  • Anderson Tadeu de Araújo Ramos
  • Maria Aparecida Silva Diamante
  • Celina de Almeida Lamas
  • Heidi Dolder
  • Fabrícia de Souza PredesEmail author
Research Article

Abstract

Arsenic is a contaminant that occurs naturally in the environment, and it is related to several diseases, such as cancer and severe metabolic diseases. Sodium arsenite effects on testes rats are not fully understood regarding morphology and stereology; thus, it becomes necessary to evaluate possible changes in these parameters under low concentrations and simulating occupational exposure. Therefore, the aim of this study was to analyze the morphometrical and stereological changes on rat testis treated with sodium arsenite. The treatment was accomplished using 5 mg/kg of sodium arsenite by gastric gavage in Wistar rats, which experiment lasted 8 weeks. Organs were weighed and gonadosomatic index (GSI) was calculated. Using the software Image Pro Plus, seminiferous tubule diameter was measured, and the volume densities of testicular parenchymal components were obtained. It was counted 200 hundred spermatozoa and classified as normal or abnormal. The parameters means of control (N = 5) and treated (N = 7) groups were compared by U Mann-Whitney’s test, and the results were considered significant for P < 0.05. We observed a decrease in seminiferous tubule diameter, as well as testis weight. These finds may be related with disorders of testosterone metabolism due to activation of immunological responses of macrophage, which inhibit the steroidogenesis. Thus, we conclude that sodium arsenic does not impair the animal’s general health, but its exposure induces biochemical and tissue changes.

Keywords

Toxicology Oxidative stress Occupational exposure Male reproductive system Arsenic 

References

  1. Ahmad I, Hussain T, Akthar KM (2008) Arsenic induced microscopic changes in rat testis. Professional Med J 15(2):287–291Google Scholar
  2. Baltaci BB, Uygur R, Caglar V, Aktas C, Aydin M, Ozen OA (2016) Protective effects of quercetin against arsenic-induced testicular damage in rats. Int J Androl 48(10):1–12.  https://doi.org/10.1111/and.12561 Google Scholar
  3. Batista BL, Souza JMO, Souza SS, Junior FB (2011) Speciation of arsenic in rice and estimation of daily intake of different arsenic species by Brazilians through rice consumption. J Hazard Mater 191:342–348.  https://doi.org/10.1016/j.jhazmat.2011.04.087 CrossRefGoogle Scholar
  4. Berg A (1985) Effect of cryptorchidism on the morphology of testicular macrophages: evidence for a Leydig cell-macrophage interaction in the rat testis. Int J Androl 8:86–96CrossRefGoogle Scholar
  5. Bhushan S, Meinhardt A (2016) The macrophages in testis function. J Reprod Immunol.  https://doi.org/10.1016/j.jri.2016.06.008
  6. Carvalho FAR (2009) Testicular morphology and morphometry of adult mice submitted to chronic exposure to arsenate. Thesis, Federal University of Viçosa (in Portuguese)Google Scholar
  7. Chang SI, Jin B, Youn P, Park C, Park JD, Ryu DY (2007) Arsenic induced toxicity and the protective role of ascorbic acid in mouse testis. Toxicol Appl Pharmacol 218:196–203.  https://doi.org/10.1016/j.taap.2006.11.009 CrossRefGoogle Scholar
  8. Chiou TY, Chu ST, Tzeng WF, Huang YC, Liao CJ (2008) Arsenic trioxide impairs spermatogenesis via reducing gene expression levels in testosterone synthesis pathway. Chem Res Toxicol 21(1):1562–1569.  https://doi.org/10.1021/tx700366x CrossRefGoogle Scholar
  9. El-Missiry MA, Shalaby F (2000) Role of β-carotene in ameliorating the cadmium-induced oxidative stress in rat brain and testis. J Biochem Mol Toxicol 14(5):238–243.  https://doi.org/10.1002/1099-0461(2000)14:5<238::AID-JBT2>3.0.CO;2-X CrossRefGoogle Scholar
  10. Favareto AP, Fernandez CD, da Silva DA, Anselmo-Franci JA, Kempinas WG (2011) Persistent impairment of testicular histology and sperm motility in adult rats treated with Cisplatin at peri-puberty. Basic Clin Pharmacol Toxicol 109:85–96.  https://doi.org/10.1111/j.1742-7843.2011.00688.x CrossRefGoogle Scholar
  11. Ferreira M, Matos RC, Oliveira H, Nunes B, Pereira ML (2012) Impairment of mice spermatogenesis by sodium arsenite. Hum Exp Toxicol 31(3):290–302.  https://doi.org/10.1177/0960327111405862 CrossRefGoogle Scholar
  12. Fiorini C, Tilloy-Ellul A, Chevalier S, Charuel C, Pointis G (2004) Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 18:413–421.  https://doi.org/10.1016/j.reprotox.2004.01.002 CrossRefGoogle Scholar
  13. Fouad AA, Albuali WH, Al-Mulhim AS, Jresat L (2015) Protective effect of telmisartan treatment against arsenic-induced testicular toxicity in rats. Z Naturforsch C 70(7–8):175–181.  https://doi.org/10.1515/znc-2015-5031 Google Scholar
  14. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379–394CrossRefGoogle Scholar
  15. Hales DB (2002) Testicular macrophage modulation of Leydig cell steroidogenesis. J Reprod Immunol 57:3–18CrossRefGoogle Scholar
  16. Hossain E, Ota A, Takahashi M, Karnan S, Damdirdorj L, Konishi Y, Konishi H, Hosokawa Y (2013) Arsenic upregulates the expression of angiotensin II type I receptor in mouse aortic endothelial cells. Toxicol Lett 220:70–75.  https://doi.org/10.1016/j.toxlet.2013.04.006 CrossRefGoogle Scholar
  17. Jana K, Jana S, Samanta PK (2006) Effects of chronic exposure to sodium arsenite on hypothalamo-pituitary-testicular activities in adult rats: possible an estrogenic mode of action. Reprod Biol Endocrinol 4:9–22.  https://doi.org/10.1186/1477-7827-4-9 CrossRefGoogle Scholar
  18. Khan S, Telang AG, Malik JK (2013) Arsenic-induced oxidative stress, apoptosis and alterations in testicular steroidogenesis and spermatogenesis in Wistar rats: ameliorative effect of curcumin. WJPP 2(3):33–48Google Scholar
  19. Li Y, Wang M, Piao F, Wang X (2012) Subchronic exposure to arsenic inhibits spermatogenesis and downregulates the expression of Ddx3y in testis and epididymis of mice. Toxicol Sci 128(2):482–489.  https://doi.org/10.1093/toxsci/kfs169 CrossRefGoogle Scholar
  20. Lima GDA (2013) Fertility and epididymal morphophisiology of Wistar rats submitted to sodium arsenate and arsenite ingestion. Thesis, Federal University of Viçosa (in Portuguese)Google Scholar
  21. Maiti S, Chatterjee AK (2001) Effects on level of glutathione and some related enzymes in tissues after an acute arsenic exposure in rats and their relationship to dietary protein deficiency. Arch Toxicol 75(9):531–537.  https://doi.org/10.1007/s002040100240 CrossRefGoogle Scholar
  22. Martin LJ (2016) Cell interactions and genetic regulation that contribute to testicular Leydig cell development and differentiation. Mol Reprod Dev 83:470–487.  https://doi.org/10.1002/mrd.22648 CrossRefGoogle Scholar
  23. McWorther FY, Wang T, Nguyen P, Chung T, Liu WF (2013) Modulation of macrophage phenotype by cell shape. PNAS 110(43):17253–17258.  https://doi.org/10.1073/pnas.1308887110 CrossRefGoogle Scholar
  24. Mori H, Christensen AK (1980) Morphometric analysis of Leydig cells in the normal rat testis. J Cell Biol 84:340–354CrossRefGoogle Scholar
  25. Mosser DV, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969.  https://doi.org/10.1038/nri2448 CrossRefGoogle Scholar
  26. Nain S, Smits JEG (2006) Pathological, immunological and biochemical markers of subchronic arsenic toxicity in rats. Environ Toxicol 27:244–254.  https://doi.org/10.1002/tox.20635 CrossRefGoogle Scholar
  27. Oliveira H, Loureiro J, Filipe L, Santos C, Ramalho-Santos J, Sousa M, Pereira ML (2006) Flow citometry evaluation of lead and cadmium effects on mouse spermatogenesis. Reprod Toxicol 22:529–535.  https://doi.org/10.1016/j.reprotox.2006.03.009 CrossRefGoogle Scholar
  28. Pant N, Kumar R, Murthy RC, Srivastava SP (2001) Male reproductive effect of arsenic in mice. Biometals 14:113–117CrossRefGoogle Scholar
  29. Reddy PS, Rani GP, Sainath SB, Meena R, Supriya CH (2011) Protective effects of N-acetylcysteine against arsenic-induced oxidative stress and reprotoxicity in male mice. J Trace Elem Med Biol 25:247–253.  https://doi.org/10.1016/j.jtemb.2011.08.145 CrossRefGoogle Scholar
  30. Russell LD, França LR (1995) Building a testis. Tissue Cell 27(2):129–147CrossRefGoogle Scholar
  31. Russell LD, Ettlin RA, Sinha-Hikim AP, Clegg ED (1990) Histolocial and histopathological evaluation of the testis. Clearwater: Cache River PressGoogle Scholar
  32. Sarkar S, Hazra J, Upadhyay SN, Singh RK, Amal RC (2008) Arsenic induced toxicity on testicular tissue of mice. Indian J Physiol Pharmacol 52:84–90Google Scholar
  33. Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, Klinefelter GR, Makris SL, Perreault SD, Schrader S, Seyler D, Sprando R, Treinem KA, Veeramachaneni DNR, Wise LD (1996) Methods for assessing sperm motility, morphology and counts in the rat, rabbit, and dog: a consensus report. Reprod Toxicol 10(3):237–244CrossRefGoogle Scholar
  34. Sharma G, Kumar M (2012) Antioxidant and modulatory role of Chlorophytum borivilianum against arsenic induced testicular impairment. J Environ Sci 24(12):2159–2165CrossRefGoogle Scholar
  35. Silva FJTNP (2013) Acute effect of sodium arsenite in testicular morphology of Wistar rats. Dissertation, Federal University of São Mateus (in Portuguese)Google Scholar
  36. Souza ACF, Marchesi SC, Lima GDA, Ferraz RP, Santos FC, Matta SLP, Neves MM (2016) Effects of sodium arsenite and arsenate in histomorphometry and antioxidant enzymes activities in rats. Biol Trace Elem Res 171(2):354–362.  https://doi.org/10.1007/s12011-015-0523-0 CrossRefGoogle Scholar
  37. Sumedha NC, Miltronprabu S (2014) Diallyl trisulfide (DATS) abrogates arsenic induced testicular oxidative stress in rats. Int J Pharmacol Toxicol 2(2):30–37.  10.14419/ijpt.v2i2.2517 Google Scholar
  38. Tsao DA, Tseng WC, Chang HR (2016) RKIP expression of liver and kidney after arsenic exposure. Environ Toxicol 32(2):1079–1082.  https://doi.org/10.1002/tox.22291 Google Scholar
  39. Waghe P, Sarkar SN, Sarath TS, Kandasamy K, Choudhury S, Gupta P, Harikumar S, Mishra SK (2016) Subchronic arsenic exposure through drinking water alters lipid profile and electrolyte status in rats. Biol Trace Elem Res.  https://doi.org/10.1007/s12011-016-0851-8
  40. Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30(1):23–38CrossRefGoogle Scholar
  41. World Health Organization (2010) Exposure to arsenic: a major public health concern. http://www.who.int/ipcs/features/arsenic.pdf?ua=1
  42. Zubair M, Ahmad M, Jamil H, Deeba F (2016) Toxic effects of arsenic on semen and hormonal profile and their amelioration with vitamin E in Teddy goat bucks. Andrologia 48(10):1120–1228.  https://doi.org/10.1111/and.12564 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Anderson Tadeu de Araújo Ramos
    • 1
  • Maria Aparecida Silva Diamante
    • 2
  • Celina de Almeida Lamas
    • 2
  • Heidi Dolder
    • 2
  • Fabrícia de Souza Predes
    • 1
    Email author
  1. 1.State University of Paraná Campus ParanaguáParanáBrazil
  2. 2.Department of Structural and Functional BiologyState University of CampinasSão PauloBrazil

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