Українська English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2023; 69(6): 97-107


Stress-induced disorders of reproductive functions

A.G. Reznikov

    SI V.P. Komisarenko Institute of Endocrinology and Metabolism, National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz69.06.097


Abstract

The review provides a pathophysiological analysis of what is currently known about the impact of acute and chronic stress on the functional state of the male and female reproductive systems. The relevance of research on the negative effects of stress on the reproductive system has increased significantly in recent years due to the COVID-19 pandemic and even more so after Russia’s aggression against Ukraine. Stress disrupts gamete maturation, libido, sexual behavior, mating, fertilization, pregnancy and delivery. In the structure of the etiology of these disorders, psycho-social stress prevails. The characteristics of stress-induced disorders of the reproductive system have features depending on the lifestyle of future parents, as well as on the period of life, starting from the embryonic to the end of the reproductive age. The hypothalamicpituitary-adrenocortical and hypothalamic-pituitary-gonadal systems, as well as oxidative-nitrosative stress, play a leading role in the pathogenesis of stress-induced disorders of the reproductive system. Modern data on the pathogenesis of stress-induced reproductive disorders should be the basis of preventive and therapeutic strategies.

Keywords: stress; reproduction; ovaries; testes; hypothalamus; pituitary gland; adrenal glands.

References

  1. Laatikainen TJ. Corticotropin-releasing hormone and opioid peptides in reproduction and stress. Ann Med. 1991;23(5):489-96. CrossRef PubMed
  2. Moberg GP. How behavioral reproduction in stress disrupts the endocrine control of domestic animals. J Dairy Sci. 1991 Jan;74(1):304-11. CrossRef PubMed
  3. Bancroft J. Impact of environment, stress, occupational, and other hazards on sexuality and sexual behavior. Environ Health Perspect Suppl. 1993;101(Suppl. 2):101-7. CrossRef PubMed PubMedCentral
  4. Negro-Vilar A. Stress and other environmental factors affecting fertility in men and women: Overview. Environ Health Perspect Suppl. 1993;101(Suppl. 2):59-64. CrossRef PubMed PubMedCentral
  5. Reznikov AG, Pishak VP, Nosenko ND, Tkachuk SS Myslitsky VF.. Prenatal stress and neuroendocrine pathology. Chernivtsi: Medakademia. 2004.
  6. Baraboy VA. Stress: nature, biological role, mechanisms, outcomes. Kyiv: Phytosociocenter. 2006.
  7. Baraboy VA, Reznikov AG. Physiology, biochemistry and psychology of stress. Kyiv: Interservice. 2013. [Ukrainian].
  8. Selye H. The general adaptation syndrome and the disease of adaptation. J Clin Endocr. 1946 Feb;6:117-230. CrossRef PubMed
  9. Tilbrook AJ, Turner AI, Clarke IJ. Stress and reproduction: Sentral mechanisms and sex differences in non-rodent species. Stress. 2002 Jun;5(2):83-100. CrossRef PubMed
  10. Tatarchuk TF. Stress and reproductive function of women. Int Endocrin J. 2006;3(5):2-9.
  11. Nordkap L, Priskorn L, Bräuner EV, Hansen ÅM, Bang AK, Holmboe SA, et al. Impact of psychological stress measured in three different scales on testis function: A cross-sectional study of 1362 young men. Andrology. 2020 Nov;8(6):1674-86. CrossRef PubMed
  12. Shatkovska AS, Grigorenko AP, Horbatyuk OG, Binkovska AM. Stress-induced disorders of the hypothalamic-pituitary and peripheral endocrine systems in a woman's body. Med Aspects Women Health. 2021;4(139):23-7. [Ukrainian].
  13. Martelli M, Zingaretti L, Salvio G, Bracci M, Santarelli L. Influence of work on andropause and menopause: A systematic review. Int J Environ Res. Publ Health. 2021;18:10074. CrossRef PubMed PubMedCentral
  14. Kassi E, Kyrou I, Tsigos C, Chrousos G. Stress, endocrine physiology and pathophysiology. De Groot LJ, BeckPeccoz P, Chrousos G, et al. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.; 2000- www. endotext.org. 92 p.
  15. Reznikov AG. Endocrinological aspects of stress. Int Endocrin J. 2007;4(10):103-11.
  16. Aitken RJ. Oxidative stress and reproductive function. Reproduction. 2022;164 E5-E8. CrossRef PubMed
  17. Aitken RJ, Bromfield EG, Gibb Z. The impact of oxidative stress on reproduction: a focus on gametogenesis and fertilization. Reproduction. 2022;164:F79-F94. CrossRef PubMed
  18. Chatterton RT. The role of stress in female reproduction: animal and human considerations. Int J Fertil. 1990 JanFeb;35(1):8-13.
  19. McCosh RB, O'Bryne KT.,Karsch FJ.,Breen KM. Regulation of the GnRH neuron during stress. J Neuroendocrinol. 2022 May;34(5): e13098. CrossRef PubMed PubMedCentral
  20. Whirledge Sh, Cidlowski JA. Glucocorticoids, stress, and fertility. Minerva Endocrinol. 2010 Jun;35(2):109-25.
  21. Geraghty AC, Kaufer D. Glucocorticoid regulation of reproduction. Adv Exp Med Biol. 2015;872:253-78. CrossRef PubMed
  22. Oyola MG, Handa RJ. Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes: sex differences in regulation of stress responsivity. Stress. 2017 Sep; 20(5): 476-94. CrossRef PubMed PubMedCentral
  23. Tronko MD, Mykosha OS, Kovzun OI, Pushkarev VM. Regulators of adrenal cortex function. Kyiv: DoctorMedia LLC. 2009. [Ukrainian].
  24. Reznikov AG, Nosenko ND, Sinitsyn PV, Tarasenko LV, Limareva AA, Polyakova LI. Disorders of neuroendocrine regulation of reproduction and adaptation in female rats under conditions of experimental hyperandrogenism. Clin Exp Pathol, 2013;2(44):3-8. [Ukrainian].
  25. Nepomnaschy PA, Kathleen B, Welch KB, Daniel S, McConnell DS, Bobbi S, et al. Cortisol levels and very early pregnancy loss in humans. PNAS. 2006 Mar 7; 103(10):3938-42. CrossRef PubMed PubMedCentral
  26. Tatarchuk TF, Cosey NV, Tutchenko TN. Treatment of stress-induced luteal phase deficiency. Women Health.2016;3 (109):18-23. CrossRef
  27. Zhabchenko IA, Korniets NG, Kovalenko TM, TertychnaTelyuk SV, Lishchenko IS, Bondarenko OM. War, stress, pregnancy: how to reconcile problematic issues? Reprod Health Woman. 2023;1(64):1-8. [Ukrainian].
  28. Petersen KU, Hærvig KK, Bonde JP, Hougaard KS, Toft G, Ramlau-Hansen CH, et al. Fetal exposure to maternal stress and male reproductive function in a cohort of young adults. Fertil Steril. 2022 Jun;117(6):1255-65. CrossRef PubMed
  29. Bräuner EV, Hansen ÅM , Doherty DA, Dickinson JE, Handelsman DJ, Hickey M, et al. The association between in-utero exposure to stressful life events during pregnancy and male reproductive function in a cohort of 20-year-old offspring: The raine study. Hum Reprod. 2019;Jul 8;34(7):1345-55.
  30. Bräuner EV, Koch T, Juul A, Doherty DA, Hart R, Hickey M. Prenatal exposure to maternal stressful life events and earlier age at menarche: The Raine Study. Hum Reprod 2021a;Jun 18;36(7):1959-69. CrossRef PubMed
  31. Bräuner EV, Koch T, Doherty DA, Dickinson J.E, JuulA, Hart R, Hickey M. The association between in utero exposure to maternal psychological stress and female reproductive function in adolescence: A prospective cohort study. Comprehens Psychoneuroendocrinol. 2021;5:100026. CrossRef PubMed PubMedCentral
  32. Sergienko LYu. Socio-emotional stress of mothers in the early stages of pregnancy as a cause of endocrinopathies and disorders in hormone-dependent systems of offspring (experimental study). Kharkiv. 2013. [Ukrainian].
  33. Piquer B, Ruz F, Barra R, Lara HE. Gestational sympathetic stress programs the fertility of offspring: A rat multi-generation study. Int J Environ Res Publ Health. 2022;19:3044. CrossRef PubMed PubMedCentral
  34. Reznikov AG. Perinatal programming of the disorders of endocrine function and behavior. Kyiv: Naukova Dumka. 2019. [Ukrainian].
  35. Sanchez-Garrido MA, Garcia-Galiano D, Tena-Sempere M. Early programming of reproductive health and fertility: novel neuroendocrine mechanisms and implications in reproductive medicine. Hum Reprodn Update. 2022;28(3):346-75. CrossRef PubMed PubMedCentral
  36. Pallarés ME, Adrover E, Baier CJ, Bourguignon NS, Monteleone MC, Brocco MA, et al. Prenatal maternal restraint stress exposure alters the reproductive hormone profile and testis development of the rat male offspring. Stress. 2013 Jul;16(4):429-40. CrossRef PubMed
  37. Reznikov AG. Hormone-neurotransmitter imprinting in the neuroendocrine control of reproduction. Harwood: Harwood Acad Publ. 1994.
  38. Reznikov A, Sachynska O, Lymareva A, Faliush O Developmental, behavioral and endocrine alterations in male rats at early and late postnatal life following in utero exposure to low dose Di-n-butylphthalate. Toxicol Res. 2021;37:173-81. CrossRef PubMed PubMedCentral
  39. Reznikov A, Sachynska O, Lymareva A, Faliush O, Perchyk I. Endocrine and behavioral effects in male rats after birth with their pregnant mother taking ibuprofen. Fiziol Zh. 2022;68(6):3-11. CrossRef
  40. Reznikov AG, Sachynska OV, Lymareva AA, Polyakova LI. Sexual behavior, profile of steroid hormones, and morphology of the medial preoptic nuclei in F1 male rat progeny prenatally exposed to low-dose bisphenol A. Neurophysiology, 2020 Aug;52(5):388-96. CrossRef
  41. Dorner G, Schenk B, Schmiedel B, Ahrens L. Stressful events in prenatal life of bi- and homosexual men. Exp Clin Endocrinol. 1983;81:83-7. CrossRef PubMed
  42. Ellis L, Cole-Harding S. The effects of prenatal stress, and of prenatal alcohol and nicotine exposure, on human sexual orientation. Physiol Behav. 2001 Sep;74(1-2):213-26. CrossRef PubMed
  43. Aiken CE, Tarry-Adkins JL, Spiroski AM, Nuzzo AM, Ashmore TJ, Rolfo A,. Chronic gestational hypoxia accelerates ovarian aging and lowers ovarian reserve in next-generation adult rats. FASEB J. 2019 Jun;33(6):7758-66. CrossRef PubMed PubMedCentral
  44. Medeiros LDS, Rodrigues PDS, Santos DNL, SilvaSampaio AC, Kirsten TB, Suffredini IB, et al. Prenatal restraint stress downregulates the hypothalamic kisspeptidergic system transcripts genes, reduces the estrogen plasma levels, delayed the onset of puberty, and reduced the sexual behavior intensity in female rats. Physiol Behav. 2023 Mar 1;260:114055. CrossRef PubMed
  45. Plana-Ripoll O, Li J, Kesmodel US, Olsen J, Parner E, Basso O. Maternal stress before and during pregnancy and subsequent infertility in daughters: a nationwide population-based cohort study. Hum Reprod. 2016 Feb;31(2):454-62. CrossRef PubMed
  46. Zheng X, Li Z, Wang G, Wang H, Zhou Y, Zhao X, et al. Sperm epigenetic alterations contribute to inter and transgenerational effects of paternal exposure to long-term psychological stress via evading offspring embryonic reprogramming. Cell Discov. 2021; 7(1):101. CrossRef PubMed PubMedCentral
  47. Romeo RD, Patel R, Pham L, So VM. Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice. Neurosci Biobehav Rev. 2016 Nov; 70:206-16. CrossRef PubMed PubMedCentral
  48. Romeo RD, Sciortino RK. Age-dependent changes in hormonal stress reactivity following repeated restraint stress throughout adolescence in male rats. Stress. 2021;24(5):496-503. CrossRef PubMed
  49. Kann RB, Romeo RD. Pubertal changes in the pituitary and adrenal glands of male and female rats: Relevance to stress reactivity. Neurobiol Stress. 2022 May;18:100457. CrossRef PubMed PubMedCentral
  50. Gibson MES, Fleming N, Zuijdwijk C, Dumont T. Where have the periods gone? The evaluation and management of functional hypothalamic amenorrhea. J Clin Res Pediatr Endocrinol. 2020;12(Suppl 1):18-27. CrossRef PubMed PubMedCentral
  51. Gleason JL, Shenassa ED, Thoma ME. Stressful life events, the incidence of infertility, and the moderating effect of maternal responsiveness: a longitudinal study. J Dev Orig Health Dis. 2021 Jun;12(3):465-73. CrossRef PubMed
  52. Hager M, Dewailly D, Marculescu R, Ghobrial S, Parry JP, Ott J. Stress and polycystic ovarian morphology in functional hypothalamic amenorrhea: a retrospective cohort study. Reprod Biol Endocrinol. 2023;21:42. CrossRef PubMed PubMedCentral
  53. Hernández-Arteaga E, Hernández-González M, BonillaJaime H, Guevara MA, Ågmo A. Pubertal stress decreases sexual motivation and suppresses the relation between cerebral thetarhythms and testosterone levels in adult male rats. Brain Res. 2020 Oct;1745:146937. CrossRef PubMed
  54. Almeida SA, Kempinas WG, Carvalho TL. Sexual behavior and fertility of male rats submitted to prolonged immobilization-induced stress. Braz J Med Biol Res. 2000 Sept;33(9):1105-9. CrossRef PubMed
  55. Almeida SA, Petenusci SO, Anselmo-Franci JA, Rosa e Silva AA, Carvalho TL. Chronic immobilization-induced stress increases plasma testosterone and delays testicular maturation in pubertal rats. Andrologia, 2000;32:7-11. CrossRef PubMed
  56. Almeida AS, Petenusci SO, Anselmo-Franci JA, Rosa e Silva AA, Carvalho TL. Decreased spermatogenic and androgenic testicular functions in adult rats submitted to immobilization-induced stress from prepuberty. Braz J Med Biol Res. 1998;31:1443-8. CrossRef PubMed
  57. Kaplowitz ET, Savenkova M, Karatsoreos IN, Romeo RD. Somatic and neuroendocrine changes in response to chronic corticosterone exposure during adolescence in male and female rats. J Neuroendocrin. 2016 Feb;28(2):12336. CrossRef PubMed
  58. Kinsey-JonesJS, Li XF, Knox AMI, Lin YS, Milligan SR, Lightman SL, et al. Corticotrophin-releasing factor alters the timing of puberty in the female rat. J Neuroendocrin. 2010; Feb;22(2):102-9. CrossRef PubMed
  59. Sinclair D, Purves-Tyson TD, Allen KM, Weickert CS. Impacts of stress and sex hormones on dopamine neurotransmission in the adolescent brain. Psychopharmacology (Berl). 2014 Jan; 231(8):1581-99. CrossRef PubMed PubMedCentral
  60. Kercmar J, Tobet SA, Majdic G. Social isolation during puberty affects female sexual behavior in mice. Front Behav Neurosci. 2014 Sept; Article 337. CrossRef PubMed PubMedCentral
  61. Horbatiuk OH, Shatkovska AS, Hryhorenko AP, Vaskiv OV, Bets IO, Kustovska IM, et al. Features of women's reproductive dysfunctions associated with prolonged stressful situations. Zaporozh Med J. 2019; 21(6):764-9. [Ukrainian]. CrossRef
  62. Burlaka O, Vagner V. Menstrual disorders in the aspect of stress-associated disorders of reproductive health of female military personnel in the ATO/OOS zone. PMGP. May 2021;6(2):e0602290. [Ukrainian].
  63. Schenker MB, Eaton M, Green R, Samuels S. Self-reported stress and reproductive health of female lawyers. J Occup Environ Med. 1997 Jun;39(6):556-68. CrossRef PubMed
  64. Bae J, Park S, Kwon J-W. Factors associated with menstrual cycle irregularity and menopause. BMC Women Health. 2018;18:36. CrossRef PubMed PubMedCentral
  65. Palomba S, Daolio J, Romeo S, Battaglia FA, Marci R, La Sala GB. Lifestyle and fertility: the influence of stress and quality of life on female fertility. Reprod Biol Endocrinol. 2018 Dec 2;16(1):113. CrossRef PubMed PubMedCentral
  66. Appleyard CB, Flores I, Torres-Reverón A. The link between stress and endometriosis: from animal models to the clinical scenario. Reprod Sci. 2020 Sep;27(9):1675-86. CrossRef PubMed PubMedCentral
  67. Fontana L, Garzia E, Marfia G, Galiano V, Miozzo M. Epigenetics of functional hypothalamic amenorrhea. Front Endocrinol (Lausanne). 2022 Aug;13:953431. CrossRef PubMed PubMedCentral
  68. Hillcoat A, Prakash J, Martin L, Zhang Y, Rosa G, Tiemeier H, et al. Trauma and female reproductive health across the lifecourse: motivating a research agenda for the future of women's health. Hum Reprod. 2023 Aug;38(8):1429-44. CrossRef PubMed
  69. Prasad Sh, Tiwari M, Pandey AN, Shrivastav TG, Chaube ShK. Impact of stress on oocyte quality and reproductive outcome. J Biomed Sci. 2016; 23:36. CrossRef PubMed PubMedCentral
  70. Zhou FJ, Cai YN, Dong YZ. Stress increases the risk of pregnancy failure in couples undergoing IVF. Stress. 2019 Jul;22(4):414-20. CrossRef PubMed
  71. Bodenmann G, Atkins DC, Schär M, Poffet V. The association between daily stress and sexual activity. J Fam Psychol. 2010 Jun;24(3):271-9. CrossRef PubMed
  72. Wells SY, Glassman LH, Talkovsky AM, Chatfield MA, Sohn MJ, Morland LA, et al. Examining changes in sexual functioning after cognitive processing therapy in a sample of women trauma survivors. Women Health Iss. 2019 Jan-Feb;29(1):72-9. CrossRef PubMed
  73. Hevesi K, Gergely Hevesi B, Kolba TN, Rowland DL. Selfreported reasons for having difficulty reaching orgasm during partnered sex: relation to orgasmic pleasure. J Psychosom Obstet Gynaecol. 2020 Jun;41(2):106-15. CrossRef PubMed
  74. An GH, Chen XW, Ch, Zhang L, Wei MF, Chen JJ, et al. Pathophysiological changes in female rats with estrous cycle disorder induced by long-term heat stress. BioMed Res Int. 2020:Article ID 4701563. CrossRef PubMed PubMedCentral
  75. Casillas F, Flores-González A, Juárez-Rojas L, López A, Betancourt M, Casas E, et al. Chronic stress decreases fertility parameters in female rats. Syst Biol Reprod Med. 2023 Jun;69(3):234-44. CrossRef PubMed
  76. Kim J, You S. High housing density-induced chronic stress diminishes ovarian reserve via granulosa cell apoptosis by angiotensin II overexpression in mice. Int J Mol Sci. 2022; 23: 8614. CrossRef PubMed PubMedCentral
  77. Kobeissi L, Inhorn MC, Hannoun AB, Hammoud N, Awwad J, Abu-Musa AA. Civil war and male infertility in Lebanon. Fertil Steril. 2008 Aug;90(2):340-5. CrossRef PubMed
  78. Madhu NR, Sarkar B, Slama P, Jha NK, Ghorai SK, Jana SK, Govindasamy K, et al. Effect of environmental stressors, xenobiotics, and oxidative stress on male reproductive and sexual health. Adv Exp Med Biol. 2022;1391:33-58. CrossRef PubMed
  79. Nordkap L, Jensen TK, Hansen ÅM, Lassen TH, Bang AK, Joensen UN, et al. Psychological stress and testicular function: a cross-sectional study of 1,215 Danish men. Fertil Steril. 2016 Jan;105(1):174-87.e1-2. CrossRef PubMed
  80. Santiago J, Santos MAS, Fardilha M, Silva JV. Stress response pathways in the male germ cells and gametes. Mol Hum Reprod. 2020 Jan;26(1):1-13. CrossRef PubMed
  81. Bird ER, Piccirillo M, N Garcia, R Blais, S Campbell. Relationship between post-traumatic stress disorder and sexual difficulties: A systematic review of veterans and military personnel. J Sex Med. 2021 Aug;18(8): 1398-426. CrossRef PubMed PubMedCentral
  82. Fontanesi L, Marchetti D, Limoncin E, Rossi R, Nimbi FM, Mollaioli D, et al. Hypersexuality and trauma: a mediation and moderation model from psychopathology to problematic sexual behavior. J Affect Disord. 2021 Feb15;281:631-7. CrossRef PubMed
  83. Gak IA, Radovic SM, Dukic AR, Janjic MM, Stojkov-Mimic NJ, Kostic TS, et al. Stress triggers mitochondrial biogenesis to preserve steroidogenesis in Leydig cells. Biochim Biophys Acta. 2015 Oct;1853(10, Part A):2217-27. CrossRef PubMed
  84. Lin H , Yuan K, Zhou H, Bu T, Su H, Liu Sh, et al. Time-course changes of steroidogenic gene expression and steroidogenesis of rat Leydig cells after acute immobilization stress. Int J Mol Sci. 2014;15:21028-44. CrossRef PubMed PubMedCentral

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.