Tannic acid ameliorates sperm quality and testicular damage in a rat model of ischemia-reperfusion

Document Type : Original Article

Authors

1 Department of Theriogenology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

2 Department of Surgery and Diagnostic Imaging, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

3 Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract
This study evaluated the protective effects of intraperitoneal (IP) tannic acid (TA) against ischemia-reperfusion (IR) injury in a rat model of testicular torsion. Eighteen mature male Wistar rats were randomized into three groups, including sham (surgery without ischemia), IR (3 hr ischemia + 3 hr reperfusion), and IR + TA (50.00 mg kg-1 TA; 100 µL intraperitoneally 30 min before reperfusion). Testicular tissues were sampled immediately after reperfusion for biochemical assays to measure malondialdehyde (MDA), superoxide dismutase (SOD), and glutathione peroxidase (GPx) levels. Epididymides were analyzed 60 days later for sperm count, motility, viability, morphology, and DNA integrity. The IR significantly elevated MDA and sperm DNA damage while reducing SOD, GPx, sperm parameters, testicular weight, and spermatogenesis. The TA administration reversed these changes and restored the parameters to levels close to those of the sham group. Overall, intraperitoneal TA mitigated IR-induced oxidative stress and preserved reproductive function, indicating its potential therapeutic value in testicular torsion.

Keywords

Subjects

1.     Burda R, Burda J, Morochovič R. Ischemic tolerance-a way to reduce the extent of ischemia-reperfusion damage. Cells 2023; 12(6): 884. doi: 10.3390/ cells12060884.
2.     Eltzschig HK, Eckle T. Ischemia and reperfusion- -from mechanism to translation. Nat Med 2011; 17(11): 1391-1401.
3.     Wang W, Tai S, Tao J, et al. Innovative hydrogel-based therapies for ischemia-reperfusion injury: bridging the gap between pathophysiology and treatment. Mater Today Bio 2024; 29: 101295. doi: 10.1016/j.mtbio. 2024.101295.
4.     Wang F, Huang H, Wei X, et al. Targeting cell death pathways in intestinal ischemia-reperfusion injury: a comprehensive review. Cell Death Discov 2024; 10(1): 112. doi: 10.1038/s41420-024-01891-x.
5.     Widgerow AD. Ischemia-reperfusion injury: influencing the microcirculatory and cellular environment. Ann Plast Surg 2014; 72(2): 253-260.
6.     Hong Y, Boiti A, Vallone D, et al. Reactive oxygen species signaling and oxidative stress: transcriptional regulation and evolution. Antioxidants (Basel) 2024; 13(3): 312. doi: 10.3390/antiox13030312.
7.     Mandal M, Sarkar M, Khan A, et al. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) in plants- maintenance of structural individuality and functional blend. Adv Redox Res 2022; 5: 100039. doi: 10.1016/j.arres.2022.100039.
8.     Asadi N, Bahmani M, Kheradmand A, et al. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. J Clin Diagn Res 2017; 11(5): IE01-IE05.
9.     Akhigbe RE, Odetayo AF, Akhigbe TM, et al. Pathophysiology and management of testicular ischemia/reperfusion injury: lessons from animal models. Heliyon 2024; 10(5): e27760. doi: 10.1016/ j.heliyon.2024.e27760.
10. Arena S, Iacona R, Antonuccio P, et al. Medical perspective in testicular ischemia-reperfusion injury. Exp Ther Med 2017;13(5): 2115-2122.
11. Minas A, Mahmoudabadi S, Gamchi NS, et al. Testicular torsion in vivo models: mechanisms and treatments. Andrology 2023; 11(7): 1267-1285.
12. Alawamlh OAH, Smith JA, Johnson ML, et al. Molecular mechanisms in spermatogenesis. In: Smith JA, Brown KL (Eds). Molecular mechanisms in spermatogenesis. 1st ed. Cham, Switzerland: Springer 2021; 287-306.
13. Shih HJ, Chang CY, Huang IT, et al. Testicular torsion-detorsion causes dysfunction of mitochondrial oxidative phosphorylation. Andrology 2021; 9(6): 1902-1910.
14. Nguyen L, Lievano G, Ghosh L, et al. Effect of unilateral testicular torsion on blood flow and histology of contra-lateral testes. J Pediatr Surg 1999; 34(5): 680-683.
15. Cordiano R, Di Gioacchino M, Mangifesta R, et al. Malondialdehyde as a potential oxidative stress marker for allergy-oriented diseases: an update. Molecules 2023; 28(16): 5979. doi: 10.3390/molecules28165979.
16. Tugasworo D, Prasetyo A, Kurnianto A, et al. Malondialdehyde (MDA) and 8-hydroxy-2'-deoxy-guanosine (8-OHdG) in ischemic stroke: a systematic review. Egypt J Neurol Psychiatry Neurosurg 2023; 59: 87. doi: 10.1186/s41983-023-00688-6.
17. Kalogeris T, Baines CP, Krenz M, et al. Ischemia/ reperfusion. Compr Physiol 2016; 7(1): 113-170.
18. Wu L, Xiong X, Wu X, et al. Targeting oxidative stress and inflammation to prevent ischemia-reperfusion injury. Front Mol Neurosci 2020; 13: 28. doi: 10.3389/fnmol.2020.00028.
19. Meštrović J, Drmić -Hofman I, Pogorelić Z, et al. Beneficial effect of nifedipine on testicular torsion-detorsion injury in rats. Urology 2014; 84(5): 1194-1198.
20. Vaos G, Zavras N. Antioxidants in experimental ischemia-reperfusion injury of the testis: where are we heading towards? World J Methodol 2017; 7(2): 37-45.
21. Kim SW, Kim DB, Kim HS. Neuroprotective effects of tannic acid in the postischemic brain via direct chelation of Zn2. Anim Cells Syst (Seoul) 2022; 26(4): 183-191.
22. Alechinsky L, Favreau F, Cechova P, et al. Tannic acid improves renal function recovery after renal warm ischemia-reperfusion in a rat model. Biomolecules 2020; 10(3): 439. doi: 10.3390/biom10030439.
23. Soleimanzadeh A, Karvani N, Davoodi F, et al. Efficacy of silver-doped carbon dots in chemical castration: a rat model study. Sci Rep 2024; 14(1): 4132. doi: 10.1038/s41598-024-75177-8.
24. Gholizadeh MJ, Azargoun R, Shalizar-Jalali A. Comparing the efficacy of dextrose, mannitol, and saline solutions in male rabbits' chemical castration. Anim Models Exp Med 2026; 9(4): 845-850.
25. Lee JW, Kim JI, Lee YA, et al. Inhaled hydrogen gas therapy for prevention of testicular ischemia/ reperfusion injury in rats. J Pediatr Surg 2012; 47(4): 736-742.
26. Ameli M, Hashemi MS, Moghimian M, et al. Protective effect of tadalafil and verapamil on testicular function and oxidative stress after torsion/detorsion in adult male rat. Andrologia 2018; 50(6): e13068. doi: 10.1111/and.13068.
27. Mallick IH, Yang W, Winslet MC, et al. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 2004; 49(9): 1359-1377.
28. Carden DL, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J Pathol 2000; 190(3): 255-266.
29. Collard CD, Gelman S. Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 2001; 94(6): 1133-1138.
30. Mauny MP, Danarto R, Heriyanto DS. Role of methylprednisolone on mRNA expression of BAX, BCL-2 gene in testicular torsion-detorsion of male albino Wistar rats. J Med Sci 2020; 52(3): 205-213.
31. Filho DW, Torres MA, Bordin AL, et al. Spermatic cord torsion, reactive oxygen and nitrogen species and ischemia-reperfusion injury. Mol Aspects Med 2004; 25(1-2): 199-210.
32. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008; 59(1): 2-11.
33. Dokmeci D, Inan M, Basaran UN, et al. Protective effect of L-carnitine on testicular ischaemia-reperfusion injury in rats. Cell Biochem Funct 2007; 25(6): 611-618.
34. Allamaneni SS, Agarwal A, Nallella KP, et al. Characterization of oxidative stress status by evaluation of reactive oxygen species levels in whole semen and isolated spermatozoa. Fertil Steril 2005; 83(3): 800-803.
35. Dogan C, Halici Z, Topcu A, et al. Effects of amlodipine on ischaemia/reperfusion injury in the rat testis. Andrologia 2016; 48(4): 441-452.
36. Ranade AV, Tripathi Y, Rajalakshmi R, et al. Effect of vitamin E administration on histopathological changes in rat testes following torsion and detorsion. Singapore Med J 2011; 52(10): 742-746.
37. Kheradmand A, Dezfoulian O, Tarrahi MJ. Ghrelin attenuates heat-induced degenerative effects in the rat testis. Regul Pept 2011; 167(1): 97-104.
38. Agarwal A, Tvrda E, Sharma R. Relationship amongst teratozoospermia, seminal oxidative stress and male infertility. Reprod Biol Endocrinol 2014; 12: 45. doi: 10.1186/1477-7827-12-45.
39. Ma Q, Shao H, Feng Y, et al. A new bioluminescent imaging technology for studying oxidative stress in the testis and its impacts on fertility. Free Radic Biol Med 2018; 124: 51-60.
40. Motamedi S, Asghari A, Jahandideh A, et al. Effects of Echinacea purpurea extract on sperm characteristics and hematology following testicular ischemia-reperfusion injury in rat. CMJB 2018; 5(2): 119-122.
41. Farombi EO, Adedara IA, Ebokaiwe AP, et al. Nigerian Bonny light crude oil disrupts antioxidant systems in testes and sperm of rats. Arch Environ Contam Toxicol 2010; 59(1): 166-174.
42. Kurcer Z, Hekimoglu A, Aral F, et al. Effect of melatonin on epididymal sperm quality after testicular ischemia/ reperfusion in rats. Fertil Steril 2010; 93(5): 1545-1549.
43. Hekimoglu A, Kurcer Z, Aral F, et al. Lycopene, an antioxidant carotenoid, attenuates testicular injury caused by ischemia/reperfusion in rats. Tohoku J Exp Med 2009; 218(2): 141-147.
44. Taati M, Moghadasi M, Dezfoulian O, et al. The effect of ghrelin pretreatment on epididymal sperm quality and tissue antioxidant enzyme activities after testicular ischemia/reperfusion in rats. J Physiol Biochem 2012; 68(1): 91-97.
45. Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis 2000; 21(3): 361-370.
46. Taati M, Moghadasi M, Dezfoulian O, et al. Effects of ghrelin on testicular ischemia/reperfusion-induced injury. Acta Med Iran 2016; 54(1): 32-38.
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983; 16(2): 109-110.
48. Tuglu D, Yuvanc E, Yilmaz E, et al. The antioxidant effect of dexmedetomidine on testicular ischemia-reperfusion injury. Acta Cir Bras 2015; 30(6): 414-421.
49. Azizollahi S, Babaei H, Derakhshanfar A, et al. Effects of co-administration of dopamine and vitamin C on ischaemia-reperfusion injury after experimental testicular torsion-detorsion in rats. Andrologia 2011; 43(2): 100-105.
50. Ozbal S, Ergur BU, Erbil G, et al. The effects of α-lipoic acid against testicular ischemia-reperfusion injury in rats. ScientificWorldJournal 2012; 2012: 489248. doi: 10.1100/2012/489248.
Volume 17, Issue 9
September 2026
Pages 639-645

  • Receive Date 26 September 2025
  • Revise Date 03 November 2025
  • Accept Date 15 November 2025