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Sleep deprivation induces structural changes in the adult rat testis: The protective effects of olive oil

  • Fatemeh Karimi (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Ali Noorafshan (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Saied Karbalay-Doust (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Maryam Naseh (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences)
  • Received : 2022.08.21
  • Accepted : 2022.11.29
  • Published : 2023.03.31

Abstract

Objective: Sleep deprivation (SD) is a common problem in today's stressful lifestyle and have physiological consequences, including reproductive dysfunction and infertility. As an antioxidant, olive oil may be effective in reducing testicular and spermatological damage by decreasing the production of free radicals. Methods: This study investigated the effects of olive oil on sperm quality and testicular structure using stereological methods to assess rats with SD. Results: When comparing SD group to grid floor+distilled water (GR) group, we found that the sperm count and motility, as well as the percentage of slow progressive sperm was significantly lower in SD group (p<0.05), but the percentage of immotile sperm was higher (p<0.01). However, no improvement was observed in sperm count or motility after concomitant treatment of SD group with olive oil. Stereological examinations revealed no significant change in the total volumes of the seminiferous tubules, interstitial tissue, and germinal epithelium in the study groups. Conversely, the total number of testicular cell types was significantly lower in SD group than in GR group. Although the total number of Sertoli and Leydig cells was significantly higher in the S +olive oil group than in the untreated SD group, no significant difference in the total number of other testicular cell types was observed between the two groups. Conclusion: SD potentially induced structural changes in testis that affected sperm count and motility. However, olive oil only improved the total number of Sertoli and Leydig cells in the animals with SD and did not improve sperm count and motility.

Keywords

Acknowledgement

The authors would like to thank Ms. A. Keivanshekouh at the Research Consultation Center of Shiraz University of Medical Sciences for improving the use of English in the manuscript.

References

  1. Rajaratnam SM, Arendt J. Health in a 24-h society. Lancet 2001;358:999-1005. https://doi.org/10.1016/S0140-6736(01)06108-6
  2. Ibarra-Coronado EG, Pantaleon-Martinez AM, Velazquez-Moctezuma J, Prospero-Garcia O, Mendez-Diaz M, Perez-Tapia M, et al. The bidirectional relationship between sleep and immunity against infections. J Immunol Res 2015;2015:678164.
  3. Aldabal L, Bahammam AS. Metabolic, endocrine, and immune consequences of sleep deprivation. Open Respir Med J 2011;5:31-43. https://doi.org/10.2174/1874306401105010031
  4. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, McCarley RW, et al. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 2006;23:2739-48. https://doi.org/10.1111/j.1460-9568.2006.04808.x
  5. Kim EY, Mahmoud GS, Grover LM. REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus. Neurosci Lett 2005;388:163-7. https://doi.org/10.1016/j.neulet.2005.06.057
  6. Lee DS, Choi JB, Sohn DW. Impact of sleep deprivation on the hypothalamic-pituitary-gonadal axis and erectile tissue. J Sex Med 2019;16:5-16. https://doi.org/10.1016/j.jsxm.2018.10.014
  7. Wittert G. The relationship between sleep disorders and testosterone in men. Asian J Androl 2014;16:262-5. https://doi.org/10.4103/1008-682X.122586
  8. Jensen TK, Andersson AM, Skakkebaek NE, Joensen UN, Blomberg Jensen M, Lassen TH, et al. Association of sleep disturbances with reduced semen quality: a cross-sectional study among 953 healthy young Danish men. Am J Epidemiol 2013;177:1027-37. https://doi.org/10.1093/aje/kws420
  9. Cho JW, Duffy JF. Sleep, sleep disorders, and sexual dysfunction. World J Mens Health 2019;37:261-75. https://doi.org/10.5534/wjmh.180045
  10. Kalmbach DA, Arnedt JT, Pillai V, Ciesla JA. The impact of sleep on female sexual response and behavior: a pilot study. J Sex Med 2015;12:1221-32. https://doi.org/10.1111/jsm.12858
  11. Villafuerte G, Miguel-Puga A, Rodriguez EM, Machado S, Manjarrez E, Arias-Carrion O. Sleep deprivation and oxidative stress in animal models: a systematic review. Oxid Med Cell Longev 2015;2015:234952.
  12. Ghosh D, Das Sarkar S, Maiti R, Jana D, Das UB. Testicular toxicity in sodium fluoride treated rats: association with oxidative stress. Reprod Toxicol 2002;16:385-90. https://doi.org/10.1016/S0890-6238(02)00038-2
  13. Waterman E, Lockwood B. Active components and clinical applications of olive oil. Altern Med Rev 2007;12:331-42.
  14. Covas MI. Olive oil and the cardiovascular system. Pharmacol Res 2007;55:175-86. https://doi.org/10.1016/j.phrs.2007.01.010
  15. Franco MN, Galeano-Diaz T, Lopez O, Fernandez-Bolanos JG, Sanchez J, De Miguel C, et al. Phenolic compounds and antioxidant capacity of virgin olive oil. Food Chem 2014;163:289-98. https://doi.org/10.1016/j.foodchem.2014.04.091
  16. Owen RW, Giacosa A, Hull WE, Haubner R, Spiegelhalder B, Bartsch H. The antioxidant/anticancer potential of phenolic compounds isolated from olive oil. Eur J Cancer 2000;36:1235-47. https://doi.org/10.1016/S0959-8049(00)00103-9
  17. El-Kholy TA, Al-Abbadi HA, Qahwaji D, Al-Ghamdi AK, Shelat VG, Sobhy HM, et al. Ameliorating effect of olive oil on fertility of male rats fed on genetically modified soya bean. Food Nutr Res 2015;59:27758.
  18. AL-Ani KH. Protective influence of olive oil on reproductive parameters in male rat treated with cadmium. J Biosci Biotechnol 2013;2:500-5.
  19. Kamali AM, Noorafshan A, Karimi F, Karbalay-Doust S. Methodological aspects of REM sleep-deprivation and stereological protocols in the brain-stem respiratory nuclei. J Adv Med Sci Appl Technol 2016;2:283-6. https://doi.org/10.18869/nrip.jamsat.2.3.283
  20. Noorafshan A, Karimi F, Karbalay-Doust S, Kamali AM. Using curcumin to prevent structural and behavioral changes of medial prefrontal cortex induced by sleep deprivation in rats. EXCLI J 2017;16:510-20.
  21. Aminsharifi A, Hekmati P, Noorafshan A, Karbalay-Doost S, Nadimi E, Aryafar A, et al. Scrotal cooling to protect against cisplatin-induced spermatogenesis toxicity: preliminary outcome of an experimental controlled trial. Urology 2016;91:90-8. https://doi.org/10.1016/j.urology.2015.12.062
  22. Mandarim-de-Lacerda CA. Stereological tools in biomedical research. An Acad Bras Cienc 2003;75:469-86. https://doi.org/10.1590/S0001-37652003000400006
  23. Tschanz S, Schneider JP, Knudsen L. Design-based stereology: planning, volumetry and sampling are crucial steps for a successful study. Ann Anat 2014;196:3-11. https://doi.org/10.1016/j.aanat.2013.04.011
  24. Wreford NG. Theory and practice of stereological techniques applied to the estimation of cell number and nuclear volume in the testis. Microsc Res Tech 1995;32:423-36. https://doi.org/10.1002/jemt.1070320505
  25. von Bartheld CS. Distribution of particles in the Z-axis of tissue sections: relevance for counting methods. Neuroquantology 2012;10:66-75.
  26. Smith LB, Walker WH. The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 2014;30:2-13. https://doi.org/10.1016/j.semcdb.2014.02.012
  27. Choi JH, Lee SH, Bae JH, Shim JS, Park HS, Kim YS, et al. Effect of sleep deprivation on the male reproductive system in rats. J Korean Med Sci 2016;31:1624-30. https://doi.org/10.3346/jkms.2016.31.10.1624
  28. Ajibare AJ, Ayodele OD, Olayaki LA. Mifepristone ameliorates sleep deprivation-induced oxidative stress in the testis of rats. Afr J Biomed Res 2020;23:239-45.
  29. Breen KM, Karsch FJ. New insights regarding glucocorticoids, stress and gonadotropin suppression. Front Neuroendocrinol 2006;27:233-45. https://doi.org/10.1016/j.yfrne.2006.03.335
  30. Olayaki LA, Sulaiman SO, Anoba NB. Vitamin C prevents sleep deprivation-induced elevation in cortisol and lipid peroxidation in the rat plasma. Niger J Physiol Sci 2015;30:5-9.
  31. Abd El-Aziz EA, Mostafa DG. Impact of sleep deprivation and sleep recovery on reproductive hormones and testicular oxidative stress in adult male rats. AAMJ 2012;10:1.
  32. Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP. Glucocorticoid induces apoptosis in rat leydig cells. Endocrinology 2002;143:130-8. https://doi.org/10.1210/endo.143.1.8604
  33. Frungieri MB, Zitta K, Pignataro OP, Gonzalez-Calvar SI, Calandra RS. Interactions between testicular serotoninergic, catecholaminergic, and corticotropin-releasing hormone systems modulating cAMP and testosterone production in the golden hamster. Neuroendocrinology 2002;76:35-46. https://doi.org/10.1159/000063682
  34. Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Rev 2008;12:197-210. https://doi.org/10.1016/j.smrv.2007.07.007
  35. Park SP, Lopez-Rodriguez F, Wilson CL, Maidment N, Matsumoto Y, Engel J Jr. In vivo microdialysis measures of extracellular serotonin in the rat hippocampus during sleep-wakefulness. Brain Res 1999;833:291-6. https://doi.org/10.1016/S0006-8993(99)01511-5
  36. Almeer RS, Abdel Moneim AE. Evaluation of the protective effect of olive leaf extract on cisplatin-induced testicular damage in rats. Oxid Med Cell Longev 2018;2018:8487248.