J Appl Biomed 16:370-377, 2018 | DOI: 10.1016/j.jab.2018.08.002

Pre-pregnancy stress suppressed the reproductive systems in parents and changed sex ratio in offspring

Maryam Mahmoodkhania, Ehsan Saboorya,b,*, Shiva Roshan-Milania,b, Negar Azizia, Mojtaba Karimipourc, Hojjat Sayyadib, Yousef Rasmid
a Urmia University of Medical Sciences, School of Medicine, Department of Physiology, Urmia, Iran
b Urmia University of Medical Sciences, Neurophysiology Research Center, Urmia, Iran
c Urmia University of Medical Sciences, Faculty of Medicine, Department of Anatomical Sciences, Urmia, Iran
d Urmia University of Medical Sciences, Cellular and Molecular Research Center, Urmia, Iran

This study aimed to investigate the effect of stress during spermatogenesis and oogenesis on reproductive performance in adult rats and sex ratio in offspring. The rats were subjected to predatory stress (exposed to a cat) twice a day for 50 (male) and 15 (female) consecutive days. At the end of the stress procedure, a number of control and stressed rats were considered to examine reproductive parameters and the rest was coupled as follows: both male and female control, male stressed/female control, male control/female stressed, and both male and female stressed. After parturition, the pups were counted, weighed, and gendered. Stress significantly increased the number of female pups in each litter (P= 0.034). In parents, stress reduced sperm quality (mobility, number, and morphology), testicular parameters (SI, STET, sloughing, and detachment), and thickness of vaginal epithelium in all phases of the estrous cycle. Serum testosterone and 17-B estradiol levels decreased significantly in stressed parents. These results emphasize the suppressive influence of stress during spermatogenesis and oogenesis on the performance of the organs of the reproductive system in parents and its consequence on sex ratio in offspring.

Keywords: Predatory stress; Pre-gestation; Reproductive functions; Sex hormones

Received: February 18, 2018; Revised: July 23, 2018; Accepted: August 20, 2018; Published: November 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Mahmoodkhani M, Saboory E, Roshan-Milani S, Azizi N, Karimipour M, Sayyadi H, Rasmi Y. Pre-pregnancy stress suppressed the reproductive systems in parents and changed sex ratio in offspring. J Appl Biomed. 2018;16(4):370-377. doi: 10.1016/j.jab.2018.08.002.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Ahmadzadeh, R., Saboory, E., Roshan-Milani, S., Pilehvarian, A.A., 2011. Predator and restraint stress during gestation facilitates pilocarpine-induced seizures in prepubertal rats. Dev. Psychobiol. 53, 806-812. Go to original source... Go to PubMed...
    2. Aitken, R.J., Krausz, C., 2001. Oxidative stress, DNA damage and the Y chromosome. Reproduction 122, 497-506. Go to original source... Go to PubMed...
    3. Almeida, S., Petenusci, S., Anselmo-Franci, J., Rosa-E-Silva, A., Lamano-Carvalho, T., 1998. Decreased spermatogenic and androgenic testicular functions in adult rats submitted to immobilization-induced stress from prepuberty. Braz. J. Med. Biol. Res. 31, 1443-1448. Go to original source... Go to PubMed...
    4. Bachmann, G.A., Nevadunsky, N.S., 2000. Diagnosis and treatment of atrophic vaginitis. Am. Fam. Physician 61, 3090-3096. Go to PubMed...
    5. Bakhtiary, Z., Shahrooz, R., Ahmadi, A., Zarei, L., 2015. Protective effects of ethyl pyruvate on sperm quality in cyclophosphamide treated mice. Iran. J. Reprod. Med. 13, 291.
    6. Campbell, P., Pottinger, T., Sumpter, J., 1992. Stress reduces the quality of gametes produced by rainbow trout. Biol. Reprod. 47, 1140-1150. Go to original source... Go to PubMed...
    7. Catalano, R., Bruckner, T., Anderson, E., Gould, J.B., 2005. Fetal death sex ratios: a test of the economic stress hypothesis. Int. J. Epidemiol. 34, 944-948. Go to original source... Go to PubMed...
    8. Collodel, G., Moretti, E., Fontani, V., Rinaldi, S., Aravagli, L., Saragò, G., et al., 2008. Effect of emotional stress on sperm quality. Indian J. Med. Res. 128, 254.
    9. Cooke, P.S., Buchanan, D.L., Lubahn, D.B., Cunha, G.R., 1998. Mechanism of estrogen action: lessons from the estrogen receptor-α knockout mouse. Biol. Reprod. 59, 470-475. Go to original source... Go to PubMed...
    10. Ebrahimi, L., Saboory, E., Roshan-Milani, S., Hashemi, P., 2014. Effect of prenatal forced-swim stress and morphine co-administration on pentylentetrazolinduced epileptic behaviors in infant and prepubertal rats. Dev. Psychobiol. 56, 1179-1186. Go to original source... Go to PubMed...
    11. Forozanfard, F., Mesdaghinia, E., Tabasi, Z., Sehat, M., Totonian, S., 2014. Prediction of preterm labor based on vaginal pH and cervical length in low risk population during the second trimester of pregnancy. KAUMS J. (FEYZ) 18, 260-266.
    12. Galea, L., McEwen, B., Tanapat, P., Deak, T., Spencer, R., Dhabhar, F., 1997. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81, 689-697. Go to original source... Go to PubMed...
    13. Gholipoor, P., Saboory, E., Ghazavi, A., Kiyani, A., Roshan-Milani, S., Mohammadi, S., et al., 2017. Prenatal stress potentiates febrile seizure and leads to long-lasting increase in cortisol blood levels in children under 2 years old. Epilepsy Behav. 72, 22-27. Go to original source... Go to PubMed...
    14. Gruntenko, N., Bownes, M., Terashima, J., Sukhanova, M.Z., Raushenbach, I.Y., 2003. Heat stress affects oogenesis differently in wild-type Drosophila virilis and a mutant with altered juvenile hormone and 20-hydroxyecdysone levels. Insect Mol. Biol. 12, 393-404. Go to original source... Go to PubMed...
    15. Hansen, D., Møller, H., Olsen, J., 1999. Severe periconceptional life events and the sex ratio in offspring: follow up study based on five national registers. BMJ 319, 548-549. Go to original source... Go to PubMed...
    16. Hashemi, P., Roshan-Milani, S., Saboory, E., Ebrahimi, L., Soltanineghad, M., 2016. Interactive effects of prenatal exposure to restraint stress and alcohol on pentylenetetrazol-induced seizure behaviors in rat offspring. Alcohol 56, 51-57. Go to original source... Go to PubMed...
    17. Hou, G., Xiong, W., Wang, M., Chen, X., Yuan, T.F., 2014. Chronic stress influences sexual motivation and causes damage to testicular cells in male rats. J. Sex. Med. 11, 653-663. Go to original source... Go to PubMed...
    18. James, W.H., 1996. Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. J. Theor. Biol. 180, 271-286. Go to original source... Go to PubMed...
    19. James, W.H., 2008. Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. J. Endocrinol. 198, 3-15. Go to original source... Go to PubMed...
    20. Kalantari Hesari, A., Shahrooz, R., Ahmadi, A., Malekinejad, H., Saboory, E., 2015. Crocin prevention of anemia-induced changes in structural and functional parameters of mice testes. J. Appl. Biomed. 13, 213-223. Go to original source...
    21. Kalantaridou, S., Makrigiannakis, A., Zoumakis, E., Chrousos, G., 2004. Stress and the female reproductive system. J. Reprod. Immunol. 62, 61-68. Go to original source... Go to PubMed...
    22. Khillare, B., Shrivastav, T., 2003. Spermicidal activity of Azadirachta indica (neem) leaf extract. Contraception 68, 225-229. Go to original source... Go to PubMed...
    23. Krackow, S., 1995. Potential mechanisms for sex ratio adjustment in mammals and birds. Biol. Rev. Camb. Philos. Soc. 70, 225-241. Go to original source... Go to PubMed...
    24. Liu, Y.-X., Cheng, Y.-N., Miao, Y.-L., Wei, D.-L., Zhao, L.-H., Luo, M.-J., et al., 2012. Psychological stress on female mice diminishes the developmental potential of oocytes: a study using the predatory stress model. PLoS One 7, e48083. Go to original source... Go to PubMed...
    25. Mahdi, A.A., Shukla, K.K., Ahmad, M.K., Rajender, S., Shankhwar, S.N., Singh, V., et al., 2011. Withania somnifera improves semen quality in stress-related male fertility. Evid. Complement. Alternat. Med. 2011, 576962. Go to original source... Go to PubMed...
    26. Maines, M.D., Ewing, J.F., 1996. Stress response of the rat testis: in situ hybridization and immunohistochemical analysis of heme oxygenase-1 (HSP32) induction by hyperthermia. Biol. Reprod. 54, 1070-1079. Go to original source... Go to PubMed...
    27. McGrady, A., 1984. Effects of psychological stress on male reproduction: a review. Arch. Androl. 13, 1-7. Go to original source... Go to PubMed...
    28. Ornoy, A., Yacobi, S., Yaffee, P., 2003. A simple method of culture of 11.5-day-old rat embryos in DMEM/F12 and 20% fetal bovine serum. J. Anat. 203, 419-423. Go to original source... Go to PubMed...
    29. Pérez-Crespo, M., Pintado, B., Gutiérrez-Adán, A., 2008. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol. Reprod. Dev. 75, 40-47. Go to original source... Go to PubMed...
    30. Pickering, A., Pottinger, T., Carragher, J., Sumpter, J., 1987. The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 68, 249-259. Go to original source... Go to PubMed...
    31. Potemina, T., 2008. Impairment of spermatogenesis in male rats during stress. Bull. Exp. Biol. Med. 145, 700-702. Go to original source... Go to PubMed...
    32. Rai, J., Pandey, S., Srivastava, R., 2003. Effect of immobilization stress on spermatogenesis of albino rats. J. Anat. Soc. India 52, 55-57.
    33. Ralph, C., Lehman, M., Goodman, R., Aj, T., 2016. Impact of psychosocial stress on gonadotrophins and sexual behaviour in females: role for cortisol? Reproduction 152, R1-R14. Go to original source... Go to PubMed...
    34. Saboory, E., Ebrahimi, L., Roshan-Milani, S., Hashemi, P., 2015. Interaction of prenatal stress and morphine alters prolactin and seizure in rat pups. Physiol. Behav. 149, 181-186. Go to original source... Go to PubMed...
    35. Sadaghiani, M.M., Saboory, E., 2010. Prenatal stress potentiates pilocarpine-induced epileptic behaviors in infant rats both time and sex dependently. Epilepsy Behav. 18, 166-170. Go to original source... Go to PubMed...
    36. Shors, T.J., Pickett, J., Wood, G., Paczynski, M., 1999. Acute stress persistently enhances estrogen levels in the female rat. Stress 3, 163-171. Go to original source... Go to PubMed...
    37. Shukla, K.K., Mahdi, A.A., Ahmad, M.K., Jaiswar, S.P., Shankwar, S.N., Tiwari, S.C., 2010. Mucuna pruriens reduces stress and improves the quality of semen in infertile men. Evid. Complement. Alternat. Med. 7, 137-144. Go to original source... Go to PubMed...
    38. Song, S., 2015. Privation, stress, and human sex ratio at birth. Early Hum. Dev. 91, 823-827. Go to original source... Go to PubMed...
    39. Tapanainen, J., Tilly, J., Vihko, K., Hsueh, A., 1993. Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors. Mol. Endocrinol. 7, 643-650. Go to original source... Go to PubMed...
    40. Tavassoli, E., Saboory, E., Teshfam, M., Rasmi, Y., Roshan-Milani, S., Ilkhanizadeh, B., et al., 2013. Effect of prenatal stress on density of NMDA receptors in rat brain. Int. J. Dev. Neurosci. 31, 790-795. Go to original source... Go to PubMed...
    41. Terrell, M.L., Hartnett, K.P., Marcus, M., 2011. Can environmental or occupational hazards alter the sex ratio at birth? A systematic review. Emerg. Health Threats J. 4, 7109. Go to original source... Go to PubMed...
    42. Tilbrook, A., Turner, A., Clarke, I., 2000. Effects of stress on reproduction in nonrodent mammals: the role of glucocorticoids and sex differences. Rev. Reprod. 5, 105-113. Go to original source... Go to PubMed...
    43. Wilson, C.B., Ebenezer, P.J., McLaughlin, L.D., Francis, J., 2014. Predator exposure/ psychosocial stress animal model of post-traumatic stress disorder modulates neurotransmitters in the rat hippocampus and prefrontal cortex. PLoS One 9, e89104. Go to original source... Go to PubMed...
    44. Wingfield, J., Sapolsky, R., 2003. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 15, 711-724. Go to original source... Go to PubMed...

    Return to the content