Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
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Protective effect of platelet-rich plasma against structural and functional changes of the adult rat testis in carbimazole-induced hypothyroidism

  • Hossein Bordbar (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Masoud Sattar-Shamsabadi (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Farzaneh Dehghani (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Fatemeh Karimi (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences)
  • Received : 2023.11.14
  • Accepted : 2024.01.10
  • Published : 2024.09.30
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Abstract

Objective: Hypothyroidism (HT) influences spermatogenesis and is associated with male infertility. Platelet-rich plasma (PRP), a biological product rich in growth factors, promotes tissue repair. In this study, the likely protective effects of PRP on testicular tissue damage in carbimazole (CBZ)-induced HT were evaluated. Methods: Forty male rats were divided into four groups. HT was induced by administering CBZ (1.35 mg/kg orally, for 45 days). Two doses of PRP (40 µL each, locally injected into the testis on days 15 and 30) were also given. After 45 days, blood samples were taken from the heart to measure triiodothyronine (T3), thyroxine (T4), and testosterone levels, and semen analysis was performed. For stereological assessment, the left testis was removed, fixed, embedded, sectioned, and stained with hematoxylin and eosin. The right testis was excised to evaluate antioxidant levels. Results: CBZ was demonstrated to induce HT, characterized by significant reductions in T3 and T4. HT was associated with decreased testicular weight, impaired sperm parameters, reduced testosterone concentration, diminished antioxidant activity, reduced volumes of testicular components, and lower total numbers of testicular cells of various types. When HT samples were treated with PRP, improvement was observed for all of these changes. This protective effect could be attributed to the growth factors present in PRP. Conclusion: PRP appears to prevent the structural changes in the testes and the deterioration in sperm quality caused by CBZ-induced HT. This protective effect is likely due to mitigation of oxidative damage and elevation of testosterone levels.

Keywords

Acknowledgement

This article was part of the dissertation written by Masoud Sattar-Shamsabadi, M.Sc., a student of anatomy. The authors would like to express their gratitude to Dr. Nasrin Shokrpour at the Research Consultation Center (RCC) for her invaluable assistance in editing this manuscript.

References

  1. Mintziori G, Duntas LH, Veneti S, Goulis DG. Metabolic, oxidative and psychological stress as mediators of the effect of COVID-19 on male infertility: a literature review. Int J Environ Res Public Health 2022;19:5277.
  2. Singh R, Hamada AJ, Agarwal A. Thyroid hormones in male reproduction and fertility. Open Reprod Sci J 2011;3:98-104. https://doi.org/10.2174/1874255601103010098
  3. Unnikrishnan AG, Menon UV. Thyroid disorders in India: an epidemiological perspective. Indian J Endocrinol Metab 2011;15:S78-81. https://doi.org/10.4103/2230-8210.83329
  4. Fadlalla MB, Wei Q, Fedail JS, Mehfooz A, Mao D, Shi F. Effects of hyper- and hypothyroidism on the development and proliferation of testicular cells in prepubertal rats. Anim Sci J 2017;88:1943-54. https://doi.org/10.1111/asj.12883
  5. Nascimento Gomes S, do Carmo Correa DE, de Oliveira IM, Bargi-Souza P, Degraf Cavallin M, Dobner Mariano D, et al. Imbalanced testicular metabolism induced by thyroid disorders: new evidences from quantitative proteome. Endocrine 2020;67:209-23. https://doi.org/10.1007/s12020-019-01989-8
  6. Jalilvand N, Hosseini M, Beheshti F, Ebrahimzadeh-Bideskan A. Protective effect of PPARγ agonist pioglitazone, on testicular tissue and sperm parameters in hypothyroid rats. Toxin Rev 2021;40:267-76. https://doi.org/10.1080/15569543.2018.1564775
  7. Amra EA, El Rehim SAA, Lashein FM, Shoaeb HS. Effect of a bradykinin potentiating factor separated from honey bee venom on thyroid gland and testis in hypothyroid white rats. J Basic Appl Zool 2022;83:1.
  8. Arafa MA, Gouda ZA, El-Naseery NI, Abdel-Nour HM, Hanafy SM, Mohamed AF, et al. Bone marrow-derived mesenchymal stem cells ameliorate the pancreatic changes of chemically induced hypothyroidism by carbimazole in male rats. Cells Tissues Organs 2018;206:144-56. https://doi.org/10.1159/000497297
  9. La Vignera S, Vita R, Condorelli RA, Mongioi LM, Presti S, Benvenga S, et al. Impact of thyroid disease on testicular function. Endocrine 2017;58:397-407. https://doi.org/10.1007/s12020-017-1303-8
  10. Nikoobakht MR, Aloosh M, Nikoobakht N, Mehrsay AR, Biniaz F, Karjalian MA. The role of hypothyroidism in male infertility and erectile dysfunction. Urol J 2012;9:405-9.
  11. Negro R, Greco G. Levothyroxine but not selenium increases endothelial progenitor cell counts in patients with hypothyroidism. Eur Thyroid J 2016;5:100-5. https://doi.org/10.1159/000445945
  12. Chakrabarti SK, Ghosh S, Banerjee S, Mukherjee S, Chowdhury S. Oxidative stress in hypothyroid patients and the role of antioxidant supplementation. Indian J Endocrinol Metab 2016;20:674-8. https://doi.org/10.4103/2230-8210.190555
  13. Dehghani F, Sotoude N, Bordbar H, Panjeshahin MR, Karbalay-Doust S. The use of platelet-rich plasma (PRP) to improve structural impairment of rat testis induced by busulfan. Platelets 2019;30:513-20. https://doi.org/10.1080/09537104.2018.1478400
  14. Kutluhan MA, Ozsoy E, Sahin A, Urkmez A, Topaktas R, Toprak T, et al. Effects of platelet-rich plasma on spermatogenesis and hormone production in an experimental testicular torsion model. Andrology 2021;9:407-13. https://doi.org/10.1111/andr.12895
  15. Sekerci CA, Tanidir Y, Sener TE, Sener G, Cevik O, Yarat A, et al. Effects of platelet-rich plasma against experimental ischemia/reperfusion injury in rat testis. J Pediatr Urol 2017;13:317.
  16. Sharara FI, Lelea LL, Rahman S, Klebanoff JS, Moawad GN. A narrative review of platelet-rich plasma (PRP) in reproductive medicine. J Assist Reprod Genet 2021;38:1003-12. https://doi.org/10.1007/s10815-021-02146-9
  17. Bader R, Ibrahim JN, Moussa M, Mourad A, Azoury J, Azoury J, et al. In vitro effect of autologous platelet-rich plasma on H2 O2-induced oxidative stress in human spermatozoa. Andrology 2020;8:191-200. https://doi.org/10.1111/andr.12648
  18. Ibrahim AA, Mohammed NA, Eid KA, Abomughaid MM, Abdelazim AM, Aboregela AM. Hypothyroidism: morphological and metabolic changes in the testis of adult albino rat and the amelioration by alpha-lipoic acid. Folia Morphol (Warsz) 2021;80:352-62. https://doi.org/10.5603/FM.a2020.0071
  19. Dehghani F, Hassanpour A, Poost-Pasand A, Noorafshan A, Karbalay-Doust S. Protective effects of L-carnitine and homogenized testis tissue on the testis and sperm parameters of busulfan-induced infertile male rats. Iran J Reprod Med 2013;11:693-704.
  20. Bordbar H, Esmaeilpour T, Dehghani F, Panjehshahin MR. Stereological study of the effect of ginger's alcoholic extract on the testis in busulfan-induced infertility in rats. Iran J Reprod Med 2013;11:467-72.
  21. Bordbar H, Yahyavi SS, Noorafshan A, Aliabadi E, Naseh M. Resveratrol ameliorates bisphenol A-induced testicular toxicity in adult male rats: a stereological and functional study. Basic Clin Androl 2023;33:1.
  22. Kar A, Panda S, Singh M, Biswas S. Regulation of PTU-induced hypothyroidism in rats by caffeic acid primarily by activating thyrotropin receptors and by inhibiting oxidative stress. Phytomed Plus 2022;2:100298.
  23. Prathima P, Venkaiah K, Pavani R, Daveedu T, Munikumar M, Gobinath M, et al. α-Lipoic acid inhibits oxidative stress in testis and attenuates testicular toxicity in rats exposed to carbimazole during embryonic period. Toxicol Rep 2017;4:373-81. https://doi.org/10.1016/j.toxrep.2017.06.009
  24. 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
  25. Karimi F, Noorafshan A, Karbalay-Doust S, Naseh M. Sleep deprivation induces structural changes in the adult rat testis: the protective effects of olive oil. Clin Exp Reprod Med 2023;50:19-25. https://doi.org/10.5653/cerm.2022.05624
  26. 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
  27. von Bartheld CS. Distribution of particles in the Z-axis of tissue sections: relevance for counting methods. Neuroquantology 2012;10:66-75.
  28. Pal P, Mukhopadhyay PK. Fluoride induced testicular toxicities in adult Wistar rats. Toxicol Mech Methods 2021;31:383-92. https://doi.org/10.1080/15376516.2021.1891489
  29. Cooke PS, Zhao YD, Hansen LG. Neonatal polychlorinated biphenyl treatment increases adult testis size and sperm production in the rat. Toxicol Appl Pharmacol 1996;136:112-7. https://doi.org/10.1006/taap.1996.0013
  30. Francois Xavier KN, Patrick Brice DD, Modeste WN, Esther N, Albert K, Pierre K, et al. Preventive effects of Aframomum melegueta extracts on the reproductive complications of propylthiouracil-induced hypothyroidism in male rat. Andrologia 2019;51:e13306.
  31. Ni FD, Hao SL, Yang WX. Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis. Cell Death Dis 2019;10:541.
  32. Lara NL, Silva VA, Chiarini-Garcia H, Garcia SK, Debeljuk L, Hess RA, et al. Hypothyroidism induced by postnatal PTU (6-n-propyl-2-thiouracil) treatment decreases Sertoli cell number and spermatogenic efficiency in sexually mature pigs. Gen Comp Endocrinol 2020;299:113593.
  33. Mancini D, Dameri RP, Bonollo E. Looking for synergies between accounting and information technologies. In: Mancini D, Dameri RP, Bonollo E, editors. Strengthening information and control systems: the synergy between information technology and accounting models. Springer; 2016. p. 1-12.
  34. Wang Q, Hong W, Chen S, Zhang Q. Variation with semilunar periodicity of plasma steroid hormone production in the mudskipper Boleophthalmus pectinirostris. Gen Comp Endocrinol 2008;155:821-6. https://doi.org/10.1016/j.ygcen.2007.10.008
  35. Algaidi SA, Faddladdeen KA, Alrefaei GI, Qahl SH, Albadawi EA, ALmohaimeed HM, et al. Thymoquinone protects the testes of hypothyroid rats by suppressing pro-inflammatory cytokines and oxidative stress and promoting SIRT1 testicular expression. Front Pharmacol 2022;13:1040857.
  36. Divakaruni AS, Wiley SE, Rogers GW, Andreyev AY, Petrosyan S, Loviscach M, et al. Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proc Natl Acad Sci U S A 2013;110:5422-7. https://doi.org/10.1073/pnas.1303360110
  37. Farbman AI, Buchholz JA. Transforming growth factor-alpha and other growth factors stimulate cell division in olfactory epithelium in vitro. J Neurobiol 1996;30:267-80. https://doi.org/10.1002/(SICI)1097-4695(199606)30:2<267::AID-NEU8>3.0.CO;2-3
  38. Abdulla AK, Rebai T, Al-Delemi DH. Protective effects of autologous platelet-rich plasma (PRP) on the outcome of cryopreservation in rabbit sperm. Cell Mol Biol (Noisy-le-grand) 2022;68:113-21. https://doi.org/10.14715/cmb/2022.68.4.14
  39. Feng CW, Bowles J, Koopman P. Control of mammalian germ cell entry into meiosis. Mol Cell Endocrinol 2014;382:488-97. https://doi.org/10.1016/j.mce.2013.09.026