DOI QR코드

DOI QR Code

Zearalenone Altered the Serum Hormones, Morphologic and Apoptotic Measurements of Genital Organs in Post-weaning Gilts

  • Chen, X.X. (Department of Animal Sciences and Technology, Shandong Agricultural University) ;
  • Yang, C.W. (College of Life science, Shandong Agricultural University) ;
  • Huang, L.B. (Department of Animal Sciences and Technology, Shandong Agricultural University) ;
  • Niu, Q.S. (Department of Animal Sciences and Technology, Shandong Agricultural University) ;
  • Jiang, Shuzhen (Department of Animal Sciences and Technology, Shandong Agricultural University) ;
  • Chi, F. (Amlan International)
  • Received : 2014.05.07
  • Accepted : 2014.09.05
  • Published : 2015.02.01

Abstract

The present study was aimed at investigating the adverse effects of dietary zearalenone (ZEA) (1.1 to 3.2 mg/kg diet) on serum hormones, morphologic and apoptotic measurements of genital organs in post-weaning gilts. A total of twenty gilts ($Landrace{\times}Yorkshire{\times}Duroc$) weaned at 21 d with an average body weight of $10.36{\pm}1.21kg$ were used in the study. Gilts were fed a basal diet with an addition of 0, 1.1, 2.0, or 3.2 mg/kg purified ZEA for 18 d ad libitum. Results showed that 3.2 mg/kg ZEA challenged gilts decreased (p<0.05) the serum levels of luteinizing hormone, however, serum levels of prolactin in gilts fed the diet containing 2.0 mg/kg ZEA or more were increased (p<0.05) compared to those in the control. Linear effects on all tested serum hormones except progesterone were observed as dietary ZEA levels increased (p<0.05). Gilts fed ZEA-contaminated diet showed increase (p<0.05) in genital organs size, hyperplasia of submucosal smooth muscles in the corpus uteri in a dose-dependent manner. However, the decreased numbers of follicles in the cortex and apoptotic cells in the ovarian were observed in gilts treated with ZEA in a dose-dependent manner. Degeneration and structural abnormalities of genital organs tissues were also observed in the gilts fed diet containing 1.1 mg/kg ZEA or more. Results suggested that dietary ZEA at 1.1 to 3.2 mg/kg can induce endocrine disturbance and damage genital organs in post-weaning gilts.

Keywords

References

  1. Alexopoulos, C. 2001. Association of Fusarium mycotoxicosis with failure in applying an induction of parturition program with PGF2-alpha and oxytocin in sows. Theriogenology 55:1745-1757. https://doi.org/10.1016/S0093-691X(01)00517-9
  2. Blaney, B. J., R. C. Bloomfield, and C. J. Moore. 1984. Zearalenone intoxication of pigs. Aust. Vet. J. 61:24-27. https://doi.org/10.1111/j.1751-0813.1984.tb07126.x
  3. Chang, K., H. J. Kurtz, and C. J. Mirocha. 1979. Effects of the mycotoxin zearalenone on swine reproduction. Am. J. Vet. Res. 40:1260-1267.
  4. Chaytor, A. C., J. A. Hansen, E. van Heugten, M. T. See, and S. W. Kim. 2011. Occurrence and decontamination of mycotoxins in swine feed. Asian Australas. J. Anim. Sci. 24:723-738. https://doi.org/10.5713/ajas.2011.10358
  5. Etienne, M. and M. Jemmali. 1982. Effects of zearalenone (F2) on estrous activity and reproduction in gilts. J. Anim. Sci. 55:1-10. https://doi.org/10.2527/jas1982.5511
  6. Etienne, M. and J. Y. Dourmad. 1994. Effects of zearalenone or glucosinolates in the diet on reproduction in sows: A review. Livest. Prod. Sci. 40:99-113. https://doi.org/10.1016/0301-6226(94)90040-X
  7. EFSA. 2004. Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to zearalenone as undesirable substance in animal feed. EFSA J. 89:1-35.
  8. Gajecka, M., L. Rybarczykb, W. Zwierzchowskia, E. Jakimiuka, L. Zielonkaa, K. Obremskia, and M. Gajecki. 2011. The effect of experimental, long-term exposure to low-dose zearalenone mycotoxicosis on the histological condition of ovaries in sexually immature gilts. Theriogenology 75:1085-1094. https://doi.org/10.1016/j.theriogenology.2010.11.017
  9. Jiang, S. Z., Z. B. Yang, W. R. Yang, B. Q .Yao, H. Zhao, F. X. Liu, C. C. Chen, and F. Chi. 2010. Effects of feeding purified zearalenone contaminated diets with or without clay enterosorbent on growth, nutrient availability, and genital organs in post-weaning female pigs. Asian Australas. J. Anim. Sci. 23:74-81. https://doi.org/10.5713/ajas.2010.90242
  10. Jiang, S. Z., Z. B. Yang, W. R. Yang, J. Gao, F. X. Liu, J. Broomhead, and F. Chi. 2011. Effects of purified zearalenone on growth performance, organ size, serum metabolites, and oxidative stress in postweaning gilts. J. Anim. Sci. 89:3008-3015. https://doi.org/10.2527/jas.2010-3658
  11. Jiang, S. Z., Z. B. Yang, W. R. Yang, S. J. Wang, F. X. Liu, L. A. Johnston, F. Chi, and Y. Wang. 2012. Effect of purified zearalenone with or without modified montmorillonite on nutrient availability, genital organs and serum hormones in post-weaning piglets. Livest. Sci. 144:110-118. https://doi.org/10.1016/j.livsci.2011.11.004
  12. Kaliamurthy, J., P. Geraldine, and P. A. Thomas. 1997. Effects of Zearalenone on food consumption, growing rate, organ weight and serum testosterone level in male rats. J. Environ. Biol. 18:115-120.
  13. LeBlanc, G. A., L. J. Bain, and V. S. Wilson. 1997. Pesticides: multiple mechanisms of demasculinization. Mol. Cell Endocrinol. 126:1-5. https://doi.org/10.1016/S0303-7207(96)03968-8
  14. Milano, G. D., D. Becu-Villalobos, and M. O. Tapia. 1995. Effects of long-term zearalenone administration on spermatogenesis and serum luteinizing hormone, follicle-stimulating hormone, and prolactin values in male rats. Am. J. Vet. Res. 56:954-958.
  15. Minervini, F., M. E. Dell Aquila, F. Maritato, P. Minoia, and A. Visconti. 2001. Toxic effects of the mycotoxin zearalenone and its derivatives on in vitro maturation of bovine oocytes and 17 Beta-estradiol levels in mural granulosa cell cultures. Toxicol. In Vitro 15:489-495. https://doi.org/10.1016/S0887-2333(01)00068-6
  16. Mitak, M., T. Gojmerac, B. Mandic, and Z. Cvetnic. 2001. Changes in serum concentration of 17-beta estradiol in female rats during estrous cycle after treatment with atrazine and zearalenone. Vet. Med. 46:145-148.
  17. Mueller, S. O., S. Simon, K. Chae, M. Metzler, and K. S. Korach. 2004. Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor a (ER$\alpha$) and ER$\beta$ in human cells. Toxicol. Sci. 80:14-25. https://doi.org/10.1093/toxsci/kfh147
  18. NRC (National Research Council). 1998. Nutrient Requirements of Swine. 10th ed. National Academy Press, Washington, DC, USA.
  19. Obremski, K., M. Gajecki, W. Zwierzchowski, L. Zielonka, I. Otrocka-Domagala, T. Rotkiewicz, A. Mikolajczyk, M. Gajecka, and M. Polak. 2003. Influence of zearalenone on reproductive system cell proliferation in gilts. Pol. J. Vet. Sci. 6:239-245.
  20. Price, W. D., R. A. Lowell, and D. G. McChsney. 1993. Naturally occurring toxins in feedstuffs: Center for Veterinary Medicine Perspective. J. Anim. Sci. 71:2556-2562. https://doi.org/10.2527/1993.7192556x
  21. Rainey, M. R., R. C. Tubbs, L. W. Bennett, and N. M. Cox. 1990. Prepubertal exposure to dietary zearalenone alters hypothalamo-hypophysial function but does not impair postpubertal reproductive function of gilts. J. Anim. Sci. 68:2015-2022. https://doi.org/10.2527/1990.6872015x
  22. SAS Institute. 2003. SAS/STAT User's Guide: Version 9.1th ed. SAS Institute Inc., Cary, NC, USA.
  23. Silva, J. R. V., R. van den Hurk, M. H. T. de Matos, R. R. dos Santos, C. Pessoa, M. O. de Moraes, and J. R. de Figueiredo. 2004. Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61:1691-1704. https://doi.org/10.1016/j.theriogenology.2003.09.014
  24. Tiemann, U., W. Tomeka, F. Schneider, and J. Vanselowb. 2003. Effects of the mycotoxins $\alpha$- and $\beta$-zearalenol on regulation of progesterone synthesis in cultured granulosa cells from porcine ovaries. Reprod. Toxicol. 17:673-681. https://doi.org/10.1016/j.reprotox.2003.07.001
  25. Ueno, Y. 1991. Biochemical mode of action of mycotoxins. In: Mycotoxins and Animal Foods (Eds. J. E. Smith and R. S. Henderson). CRS Press, Boston, MA, USA. p. 437-453.
  26. Wasowicz, K., M. Gajecka, J. Calkal, E. Jakimiuk, and M. Gajecki. 2005. Influence of chronic administration of zearalenoneon on the processes of apoptosis in the porcine ovary. Vet. Med-Czech. 50:531-536.
  27. Yang, H. H., R. J. Aulerich, W. Helferich, B. Yamini, K. C. Chou, E. R. Miller, and S. J. Bursian. 1995. Effects of zearalenone and/or tamoxifen on swine and mink reproduction. J. Appl. Toxicol. 15:223-232. https://doi.org/10.1002/jat.2550150314
  28. Yang, J., Y. Zhang, Y. Wang, and S. Cui. 2007. Toxic effects of zearalenone and α-zearalenol on the regulation of steroidogenesis and testosterone production in mouse Leydig cells. Toxicol. In Vitro 21:558-565. https://doi.org/10.1016/j.tiv.2006.10.013
  29. Yu, Z., L. Zhang, D. Wu, and F. Liu. 2005. Anti-apoptotic action of zearalenone in MCF-7 cells. Ecotoxicol. Environ. Saf. 62:441-446. https://doi.org/10.1016/j.ecoenv.2004.10.003
  30. Zhang, H., H. Nagasshima, and T. Goto. 1997. Natural occurrence of mycotoxins in corn, samples from high and low risk areas for human esophageal cancer in China. Mycotoxin 44:29-35.
  31. Zinedine, A., J. M. Soriano, J. C. Molto, and J. Manes. 2007. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food Chem. Toxicol. 45:1-18. https://doi.org/10.1016/j.fct.2006.07.030
  32. Zwierzchowski, W., M. Przybylowcz, K. Obremski, L. Zielonka, E. Skorska-Wyszynska, M. Gajecka, M. Polak, E. Jakimiuk, B. Jana, L. Rybarczyk, and M. Gajecki. 2005. Level of zearalenone in blood serum and lesions in ovarian follicles of sexually immature gilts in the course of zearalenone micotoxicosis. Pol. J. Vet. Sci. 8:209-218.

Cited by

  1. Exploration of intrinsic and extrinsic apoptotic pathways in zearalenone-treated rat sertoli cells vol.31, pp.12, 2015, https://doi.org/10.1002/tox.22175
  2. Alleviation of mycotoxin biodegradation agent on zearalenone and deoxynivalenol toxicosis in immature gilts vol.9, pp.1, 2018, https://doi.org/10.1186/s40104-018-0255-z
  3. The determination of zearalenone and its major metabolites in endometrial cancer tissues vol.410, pp.5, 2018, https://doi.org/10.1007/s00216-017-0807-7
  4. Risks for animal health related to the presence of zearalenone and its modified forms in feed vol.15, pp.7, 2015, https://doi.org/10.2903/j.efsa.2017.4851
  5. Toxic effects of zearalenone on gametogenesis and embryonic development: A molecular point of review vol.119, pp.None, 2018, https://doi.org/10.1016/j.fct.2018.06.003
  6. Comparative study of stress response, growth and development of uteri in post‐weaning gilts challenged with zearalenone and estradiol benzoate vol.103, pp.6, 2019, https://doi.org/10.1111/jpn.13195
  7. Zearalenone-induced aberration in the composition of the gut microbiome and function impacts the ovary reserve vol.244, pp.None, 2015, https://doi.org/10.1016/j.chemosphere.2019.125493
  8. Protective effect of resveratrol against toxicity induced by the mycotoxin, zearalenone in a rat model vol.146, pp.None, 2015, https://doi.org/10.1016/j.fct.2020.111840
  9. Dose-Effect of Zearalenone on the Localization and Expression of Growth Hormone, Growth Hormone Receptor, and Heat Shock Protein 70 in the Ovaries of Post-weaning Gilts vol.8, pp.None, 2021, https://doi.org/10.3389/fvets.2021.629006
  10. Zearalenone perturbs the circadian clock and inhibits testosterone synthesis in mouse Leydig cells vol.84, pp.3, 2015, https://doi.org/10.1080/15287394.2020.1841699
  11. Impact of Fusarium-Derived Mycoestrogens on Female Reproduction: A Systematic Review vol.13, pp.6, 2015, https://doi.org/10.3390/toxins13060373
  12. Zearalenone exposure affects the Wnt/β-catenin signaling pathway and related genes of porcine endometrial epithelial cells in vitro vol.34, pp.6, 2015, https://doi.org/10.5713/ajas.20.0292
  13. Ameliorative effect of resveratrol and its nano-formulation on estrogenicity and apoptosis induced by low dose of zearalenone in male Wistar rats vol.36, pp.21, 2015, https://doi.org/10.1557/s43578-021-00425-w
  14. Zearalenone Exposure Triggered Cecal Physical Barrier Injury through the TGF-β1/Smads Signaling Pathway in Weaned Piglets vol.13, pp.12, 2015, https://doi.org/10.3390/toxins13120902