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Phytoestrogen treatment induces testis alterations in dogs. Potential use in population control

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Abstract

Dog overpopulation is considered a human health risk; they are the terrestrial vector of rabies and reservoirs for other human diseases. Surgical neutering and intratesticular injections have been used in male dogs. Physiological and morphological alterations in reproductive organs can be induced by phytoestrogens. Our goal was to evaluate the effect of oral coumestrol on dog ejaculates and testis histology. Two groups of 5 healthy adult dogs were used. One coumestrolcontaining biscuit was given once a week for a 4 week period to the experimental group. Ejaculates were obtained and evaluated. After treatment, testis were obtained and processed for histology. Compared to controls, treated dogs have reduced tubules (462 ± 1.4 vs 336 ± 2 μ2), spermatogenic epithelium (49.1 ± 0.01 vs 13.3 ± 0.01 μ2), and lumen opening (891 ± 1.4 vs 530 ± 26.9 μ). Ejaculates from treated animals have increased numbers of abnormal spermatozoa and reduced sperm concentration.

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References

  1. Aslantas, O., Ozdemir, V., Kilic, S., and Babur, C., 2005. Seroepidemiology of leptospirosis, toxoplasmosis and leishmaniasis in dogs in Ankara, Turkey. Veterinary Parasitology, 129: 187–191. doi:10.1016/j.vetpar.2004.11.037

  2. Atanassova, N., McKinell, C., Turner, K., Walker, M., Fisher, S., Morley, M., Millar, M.R., Groome, N.P., and Sharpe, R.M., 2000. Comparative effect of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology 141: 3898–3907. doi:10.1210/en.141.10.3898

  3. Ax, R.L., Dally, M.R., Didion, B.A., Lenz, R.W., Love, C.C., Varner, D.D., Hafez, B., and Bellin, M.E. 2000. Semen evaluation. In B. Hafez, E.S.E. Hafez (eds).Reproduction in farm animals, 7th edition, Blackwell, New York, pp 365–375.

  4. Brod, C.S., Aleixo, J.A., Jouglard, S.D., Fernandes, C.P., Teixeira, J.L., and Dellagostino, O.A., 2005. Evidence of dog as a reservoir for human leptospirosis: a serovar isolation, molecular characterization and its use in serological survey. Revista de la.Sociedad Brasileira de Medicina Tropical 38: 294–300. doi:10.1590/S0037-86822005000400003

  5. Chamley, L.W., and Clarke, G.N., 2002. Antisperm antibodies and conception. Seminars in Immunopathology 29: 169–184. doi:10.1007/s00281-007-0075-2

  6. Chausieaux, O.E., Abel, M.H., Baxter, F.O., Khaled, W., Ellis, P.J.I., Charlton, H.M., and Affara, N.A., 2008. Hypogonadal mouse, a model to study the effect of the endogenous lack of gonadotrophins on apoptosis. Biology of Reproduction 78:77–90. doi:10.1095/biolreprod.107.060970

  7. Couse, J.F., Mahato, D., Eddy, E.M., and Korach, K.S., 2001. Molecular mechanism of estrogen action in the male: insights from the estrogen receptor null mice. Reproduction, Fertility and Development 13: 211–219. doi:10.1071/RD00128

  8. Delbes, G., Levacher, C., Pairault, C., Racine, C., Duquenne, C., Krust, A., and Habert, R., 2004. Estrogen receptor β-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 145: 3395–3403. doi:10.1210/en.2003-1479

  9. D’Occhio, M.J., Aspden, W.J., and Trigo, T.E., 2001. Sustained testicular atrophy in bulls actively immunized against GnRH: potential to control carcase characteristics. Animal Reproduction Science 66: 47–58. doi:10.1016/S0378-4320(01)00091-4

  10. Earl, E.R., Waterston, M.M., Aughey, E., Harvey, M.J., Matschke, C., Colston, A., and Ferro, V.A., 2006. Evaluation of two GnRH-I based vaccine formulations on the testes function of entire Suffolk cross ram lambs. Vaccine 24: 3172–3183. doi:10.1016/j.vaccine.2006.01.041

  11. Fahim, M.S., Wang, M., Sutcu, M.F., Fahim, Z., and Youngquist, R.S., 1993. Sterilization of dogs with intra-epididymal injection of zinc-arginine. Contraception 47:107–122. doi:10.1016/0010-7824(93)90113-L

  12. Fraser, L.R., Beyret, E., Milligan, S.R., and Adeoya-Osiguwa, 2006. A. Effects of estrogenic xenobiotics on human and mouse spermatozoa. Human Reproduction 21: 1184–1193. doi:10.1093/humrep/dei486

  13. Freshman, J.L., 2002. Semen Collection and Evaluation. Clinical Techniques in Small Animal Practice 17:104–107. doi:10.1053/svms.2002.34326

  14. Gioberchio, G., 2005. A special relationship. Prospects in Health 10:24–29.

  15. Hall, J.M., and McDonell, D.P., 1999. The estrogen receptor β-isoform (ERβ) of the human estrogen receptor modulates ERα transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140: 5566–5578. doi:10.1210/en.140.12.5566

  16. Hardy, C.M., and Braid, A.L., 2007. Vaccines for immunological control of fertility in animals. Review du Science et Technology 26: 461–470.

  17. Herbert, C., and Trigg, T., 2005. Applications of GnRh in the control and management of fertility in female animals. Animal Reproduction Science 88: 141–153. doi:10.1016/j.anireprosci.2005.05.007

  18. Immegart, H.M., and Threlfall, W.R., 2000. Evaluation of intratesticular injection of glycerol for non-surgical sterilization of dogs. American Journal of Veterinary Research 61: 544–549. doi:10.2460/ajvr.2000.61.544

  19. Iseki, S., and Mori, T., 1986. Methyl green-pyronin stain distinguishes proliferating from differentiated nonproliferating cell nuclei after acid denaturation of DNA. Journal of Histochemistry and Cytochemistry 34: 683–687.

  20. Jacob, D.A., Temple, J.L., Patisaul, H.B., Young, L.J., and Rissman, E.F., 2001. Coumestrol antagonizes neuroendocrine actions of estrogen via the estrogen receptor α. Experimental Biology and Medicine 226: 301–306.

  21. Jana, K., and Samanta, P.K., 2007. Sterilization of male stray dogs with a single intratesticular injection of calcium chloride: a dose-dependent study. Contraception 75: 390–400. doi:10.1016/j.contraception.2007.01.022

  22. Johnston, S.D., Kustriz, M.V.R., and Olson, P.N.S., 2001. Semen collection, evaluation, and preservation. In S. D. Johnston, M.V.R. Kustriz, and P.N.S. Olson, (eds). Canine and Feline Theriogenology. W.B. Saunders, Philadelphia, pp 287–306.

  23. Kutzler, M.A., 2005. Semen collection in the dog. Theriogenology 64: 747–754. doi:10.1016/j.theriogenology.2005.05.023

  24. Liu, I.K., Turner, J.W., Van Leeuwen, E.M., Flanagan, D.R., Hedrick, J.L., Murata, K., Lane, V.M., and Morales-Levy, M.P., 2005. Persistence of anti-zonae pellucidae antibodies following single inoculation of porcine zonae pellucidae in the domestic equine. Reproduction 129: 181–190. doi:10.1530/rep.1.00168

  25. Meltzer, M.I., and Rupprecht, C.E., 1998. A review of the economics of the prevention and control of rabies. Part 2: Rabies in dogs, livestock and wildlife. Pharmacoeconomics 14: 481–498. doi:10.2165/00019053-199814050-00003

  26. Naz, R.K., and Chauhan, S.C., 2002. Human sperm-specific peptide vaccine that causes long-term reversible contraception. Biology of Reproduction 67: 674–680. doi:10.1095/biolreprod67.2.674

  27. Naz, R.K., Gupta, S.K., Gupta, J.C., Vyas, H.K., and Talwar, A.G., 2005. Recent advances in contraceptive vaccine development: a minireview. Human Reproduction 20: 3271–3283. doi:10.1093/humrep/dei256

  28. O’Donnell, L., Robertson, K.M., Jones, M.E., and Simpson, E.R., 2001. Estrogens and spermatogenesis. Endocrine Reviews 22: 289–318. doi:10.1210/er.22.3.289

  29. Parizek, J., 1960. Sterilization of the male by cadmium salts. Journal of Reproduction and Fertility 1: 294–309.

  30. Patisaul, H.B., Whitten, P.L., and Young, L.J. 1999. Regulation of estrogen receptor beta mRNA in the brain: opposite effects of 17β-estradiol and the phytoestrogen, coumestrol. Molecular Brain Research 67: 165–171. doi:10.1016/S0169-328X(99)00058-3

  31. Pike, A.C.W., Brzozowski, A.M., Hybbard, R.E., Bonn, T., Thorsell, A.-G., Engstrom, O., Ljunggren, J., Gustafsson, J.-A., and Carlquist, M., 1999. Structure of the ligand-binding domain of oestrogen receptor beta in the presence of partial agonist and full antagonist. EMBO Journal 18(17):4608–4618. doi:10.1093/emboj/18.17.4608

  32. Razandi, M., Pedram, A., Merchenthaler, I.J., Greene, G.L., and Levin, E.R., 2004. Plasma membrane estrogen receptors exist and functions as dimers. Molecular Endocrinology 18: 2854–2865. doi:10.1210/me.2004-0115

  33. Rubel, D., and Wisnivesky, C., 2005. Magnitude and distribution of canine fecal contamination and helminth eggs in two areas of different urban structure, Greater Buenos Aires, Argentina. Veterinary Parasitology 133:339–347. doi:10.1016/j.vetpar.2005.06.002

  34. Serrano, H., Garcia-Suarez, M.D., 2001. Ovarian alterations in bitches induced by active immunization with porcine oocyte proteins. Veterinaria Mexico 32:221–224.

  35. Serrano, H., Perez-Rivero, J.J., Aguilar-Setien, A., de Paz, O., and Villa-Godoy, A., 2007. Vampire bat reproductive control by a naturally occurring phytoestrogen. Reproduction, Fertility and Development 19: 470–472. doi:10.1071/RD06100

  36. Sharpe, R.M., and Skakkebaek, N.E., 1993. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 341:1392–1395. doi:10.1016/0140-6736(93)90953-E

  37. Srivastava, N., Santhanam, R., Sheela, P., Mukund, S., Thakral, S.S., Malik, B.S., and Gupta, S.K., 2002. Evaluation of the immunocontraceptive potential of Escherichia coli-expressed recombinant dog ZP2 and ZP3 in a homologous animal model. Reproduction 123: 847–857. doi:10.1530/rep.0.1230847

  38. Tepsumethanon, V., Wilde, H., and Hemachudha, T. 2005. Intratesticular injection of a balanced zinc solution for permanent sterilization of dogs. Journal of the Medical Association of Thailand 88:686–689.

  39. Valiente, C., Corrada, Y., de la Sota, P.E., Geres, P.G., and Gobello, C., 2007. Effect of GnRH antagonist, acyline, on canine testicular characteristics. Theriogenology 68: 687–692. doi:10.1016/j.theriogenology.2007.05.062

  40. Wang, M., 2002. Neutersol: Intratesticular injection induces sterility in dogs. In Proceedings of the Society for non-surgical methods in pet population control. Pine Mountain, GA.19–21 April 2002. The Alliance for Contraception in Cats and Dogs, Portland Or, pp 62–65.

  41. Whitten, P.L., Russell, E., and Naftolin, F., 1992. Effects of a normal, human-concentration, phytoestrogen diet on rat uterine growth. Steroids 57: 98–106. doi:10.1016/0039-128X(92)90066-I

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Correspondence to Hector Serrano.

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Perez-Rivero, J., Martinez-Maya, J., Perez-Martinez, M. et al. Phytoestrogen treatment induces testis alterations in dogs. Potential use in population control. Vet Res Commun 33, 87–95 (2009). https://doi.org/10.1007/s11259-008-9077-3

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Keywords

  • Canine overpopulation
  • Contraception
  • Testis alterations
  • Phytoestrogens
  • Coumestrol