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Basic Research

Effect of ozone versus naringin on testicular injury in experimentally induced ulcerative colitis in adult male albino rats

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Pages 439-461 | Received 13 Sep 2022, Accepted 30 Sep 2022, Published online: 11 Oct 2022

References

  • Turnaye H, Krausz C, Oates RD. Concepts in diagnosis and therapy for male reproductive impairment. Lancet Diabetes Endocrinol. 2017 Jul 1;5(7):554–564. doi:10.1016/S2213-8587(16)30043-2.
  • Alboghobeish S, Mahdavinia M, Zeidooni L, et al. Efficiency of naringin against reproductive toxicity and testicular damages induced by bisphenol A in rats. Iran J Basic Med Sci. 2019 Mar;22(3):315. doi:10.22038/ijbms.2019.29757.7184.
  • Park YE, Kim TO. Sexual dysfunction and fertility problems in men with inflammatory bowel disease. World J Mens Health. 2020 Jul;38(3):285. doi:10.5534/wjmh.190007.
  • Levesque BG, Sandborn WJ, Ruel J, Feagan BG, Sands BE, Colombel JF. Converging goals of treatment of inflammatory bowel disease from clinical trials and practice. Gastroenterology. 2015 Jan 1;148(1):37–51. 10.1053/j.gastro.2014.08.003.
  • Lopez J, Grinspan A. Fecal microbiota transplantation for inflammatory bowel disease. Gastroenterol Hepatol. 2016 Jun;12(6):374.
  • Chen B, She S, Li D, et al. Role of miR-19a targeting TNF-α in mediating ulcerative colitis. Scand J Gastroenterol. 2013 Jul 1;48(7):815–824. 10.3109/00365521.2013.800991.
  • Piechota-Polanczyk A, Fichna J. The role of oxidative stress in pathogenesis and treatment of inflammatory bowel diseases. Naunyn Schmiedebergs Arch Pharmacol. 2014 Jul;387(7):605–620. doi:10.1007/s00210-014-0985-1.
  • Farombi EO, Adedara IA, Awoyemi OV, et al. Dietary protocatechuic acid ameliorates dextran sulphate sodium-induced ulcerative colitis and hepatotoxicity in rats. Food Funct. 2016;7(2):913–921. doi:10.1039/C5FO01228G.
  • Sands K, Jansen R, Zaslau S, Greenwald D. the safety of therapeutic drugs in male inflammatory bowel disease patients wishing to conceive. Aliment Pharmacol Ther. 2015 May;41(9):821–834. doi:10.1111/apt.13142.
  • Vavricka SR, Rogler G, Gantenbein C, et al. Chronological order of appearance of extraintestinal manifestations relative to the time of IBD diagnosis in the Swiss inflammatory bowel disease cohort. Inflamm Bowel Dis. 2015 Aug 1;21(8):1794–1800. 10.1097/MIB.0000000000000429.
  • Trivedi PP, Jena GB. Ulcerative colitis-induced hepatic damage in mice: studies on inflammation, fibrosis, oxidative DNA damage and GST-P expression. Chem Biol Interact. 2013 Jan 25;201(1–3):19–30. 10.1016/j.cbi.2012.12.004.
  • Ajayi BO, Adedara IA, Ajani OS, Oyeyemi MO, Farombi EO. [6]-Gingerol modulates spermatotoxicity associated with ulcerative colitis and benzo [a] pyrene exposure in BALB/c mice. J Basic Clin Physiol Pharmacol. 2018 Jun 1;29(3):247–256. 10.1515/jbcpp-2017-0140.
  • Chang YL, Lo HY, Cheng SP, et al. The potential of a single injection of hUCMSCs in relevant testis injury and related severity of DSS induced acute and chronic colitis. Res Sq. 2021. doi:10.21203/rs.3.rs-270686/v1.
  • Parmar AR, Trivedi PP, Jena GB. Dextran sulfate sodium-induced ulcerative colitis leads to testicular toxicity in mice: role of inflammation, oxidative stress and DNA damage. Reprod Toxicol. 2014 Nov 1;49:171–184. 10.1016/j.reprotox.2014.08.004.
  • Lichtenstein GR, Abreu MT, Cohen R, Tremaine W. American gastroenterological association institute technical review on corticosteroids, immunomodulators, and infliximab in inflammatory bowel disease. Gastroenterology. 2006 Mar 1;130(3):940–987. 10.1053/j.gastro.2006.01.048.
  • Khan RA, Ahmad B, Ahmad M, Ali A, Naz I, Fahim M. Management of Ralstonia solanacearum (Smith) Yabuuchi wilt in tomato (Solanum Lycopersicum L.) with dried powder of the medicinal plant Withania somnifera (L.) Dunal. Pak. J. Bot. 2019 Feb 1;51(1):297–306. doi:10.1016/j.freeradbiomed.2018.05.093.
  • Abaza MS, Orabi KY, Al-Quattan E, Al-Attiyah RA. Growth inhibitory and chemo-sensitization effects of naringenin, a natural flavanone purified from Thymus vulgaris, on human breast and colorectal cancer. Cancer Cell Int. 2015 Dec;15(1):1–9. doi:10.1186/s12935-015-0194-0.
  • Wang C, Fan RQ, Zhang YX, Nie H, Li K. Naringenin protects against isoniazid-and rifampicin-induced apoptosis in hepatic injury. World J Gastroenterol. 2016 Nov 11;22(44):9775. 10.3748/wjg.v22.i44.9775.
  • Sahin Z, Ozkaya A, Cuce G, Uckun M, Yologlu E. Investigation of the effect of naringenin on oxidative stress‐related alterations in testis of hydrogen peroxide‐administered rats. J Biochem Mol Toxicol. 2017 Sep;31(9):e21928. doi:10.1002/jbt.21928.
  • Adana MY, Akang EN, Peter AI, et al. Naringenin attenuates highly active antiretroviral therapy‐induced sperm DNA fragmentations and testicular toxicity in Sprague‐Dawley rats. Andrology. 2018 Jan;6(1):166–175. doi:10.1111/andr.12439.
  • Galiè M, Costanzo M, Nodari A, et al. Mild ozonisation activates antioxidant cell response by the Keap1/Nrf2 dependent pathway. Free Radical Biol Med. 2018 Aug 20;124:114–121.
  • Aydogdu İ, Ilbey Y, Coban G, et al. Does ozone administration have a protective or therapeutic effect against radiotherapy-induced testicular injury? J Can Res Ther. 2019;15(S1):76–81.doi:10.4103/jcrt.JCRT_322_17.
  • Al‐Saadi H, Potapova I, Rochford ET, Moriarty TF, Messmer P. Ozonated saline shows activity against planktonic and biofilm growing Staphylococcus aureus in vitro: a potential irrigant for infected wounds. Int Wound J. 2016 Oct;13(5):936–942. doi:10.1111/iwj.12412.
  • Zeng J, Lei L, Zeng Q, et al. Ozone therapy attenuates NF-κB-mediated local inflammatory response and activation of Th17 cells in treatment for psoriasis. Int J Biol Sci. 2020;16(11):1833. doi:10.7150/ijbs.41940.
  • Zanardi I, Borrelli E, Valacchi G, Travagli V, Bocci V. Ozone: a multifaceted molecule with unexpected therapeutic activity. Curr Med Chem. 2016 Feb 1;23(4):304–314. 10.2174/0929867323666151221150420.
  • Tusat M, Mentese A, Demir S, Alver A, Imamoglu M. Medical ozone therapy reduces oxidative stress and testicular damage in an experimental model of testicular torsion in rats. Int braz j Urol. 2017 Nov;43(6):1160–1166. doi:10.1590/s1677-5538.ibju.2016.0546.
  • Aksu EH, Kandemir FM, Küçükler S. Protective effect of naringin on methotrexate-induced testicular apoptosis and autophagy Via reducing oxidative stress in male rats. Fırat Üniversitesi Sağlık Bilimleri Veteriner Dergisi. 2018;32(3):179–183.
  • Osman N, Adawi D, Ahrne S, Jeppsson B, Molin G. Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig Dis Sci. 2004 Feb;49(2):320–327. doi:10.1023/B:DDAS.0000017459.59088.43.
  • Tokuyasu N, Shomori K, Amano K, et al. Indirubin, a constituent of the Chinese herbal medicine Qing-Dai, attenuates dextran sulfate sodium-induced murine colitis. Yonago Acta Med. 2018;61(2):128–136. doi:10.33160/yam.2018.06.005.
  • Salem EA, Salem NA, Hellstrom WJ. Therapeutic effect of ozone and rutin on Adriamycin‐induced testicular toxicity in an experimental rat model. Andrologia. 2017 Feb;49(1):e12603. doi:10.1111/and.12603.
  • Wen L, Gao Q, Ma CW, et al. Effect of polysaccharides from Tremella fuciformis on UV-induced photoaging. Journal Funct Foods. 2016 Jan 1;20:400–410. 10.1016/j.jff.2015.11.014.
  • Teilmann AC, Nygaard Madsen A, Holst B, Hau J, Rozell B, Abelson KS. Physiological and pathological impact of blood sampling by retro-bulbar sinus puncture and facial vein phlebotomy in laboratory mice. PLoS One. 2014 Nov 26;9(11):e113225. 10.1371/journal.pone.0113225.
  • Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979 Jun 1;95(2):351–358. 10.1016/0003-2697(79)90738-3.
  • Ghani MA, Barril C, Bedgood JDR, Prenzler PD. Measurement of antioxidant activity with the thiobarbituric acid reactive substances assay. Food Chem. 2017 Sep 1;230:195–207. doi:10.1016/j.foodchem.2017.02.127.
  • Kiernan J. Histological and Histochemical Methods: Theory and Practice. 5th ed. United Kingdom: Scoin publisher; 2015:111–162.
  • Suvarna KS, Layton C, Bancroft JD, editors. Bancroft’s Theory and Practice of Histological Techniques E-Book. Oxford: Elsevier Health Sciences,2018Feb: 381–426 and 493–538.
  • Johnsen SG. Testicular biopsy score count- a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones. 1970;1:225.
  • Saied NM, Darwish SK. A possible ameliorating effects of Tribulus terrestris on testicular dysfunction induced by xenoestrogens exposure in adult rats. Curr Sci Int. 2015;4(1):7389.
  • Yousaf B, Liu G, Wang R, et al. Bisphenol A exposure and healing effects of Adiantum capillus-veneris L plant extract (APE) in Bisphenol A-induced reproductive toxicity in albino rats. Environ Sci Pollut Res. 2016;23(12):645–657. doi:10.1007/s11356-016-6330-0.
  • Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallogr Section D. 2010 Apr 1;66(4):486–501. 10.1107/S0907444910007493.
  • Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2017 Dec 23;390(10114):2769–2778. 10.1016/S0140-6736(17)32448-0.
  • Grosen A, Bungum M, Christensen LA, et al. Semen quality and sperm DNA integrity in patients with severe active inflammatory bowel disease and effects of tumour necrosis factor-alpha inhibitors. J Crohn’s Colitis. 2019 Apr 26;13(5):564–571. 10.1093/ecco-jcc/jjy198.
  • Xiao Y, Xu B, Bordiga M, et al. Cyanidin-3-O-glucoside supplement improves sperm quality and spermatogenesis in a mice model of ulcerative colitis. Nutrients. 2022 Feb 25;14(5):984. 10.3390/nu14050984.
  • Darnaud M, Dos Santos A, Gonzalez P, et al. Enteric delivery of regenerating family member 3 alpha alters the intestinal microbiota and controls inflammation in mice with colitis. Gastroenterology. 2018 Mar 1;154(4):1009–1023. 10.1053/j.gastro.2017.11.003.
  • Islam J, Sato S, Watanabe K, et al. Dietary tryptophan alleviates dextran sodium sulfate-induced colitis through aryl hydrocarbon receptor in mice. J Nutr Biochem. 2017 Apr 1;42:43–50. doi:10.1016/j.jnutbio.2016.12.019.
  • Wang A, Keita ÅV, Phan V, et al. Targeting mitochondria-derived reactive oxygen species to reduce epithelial barrier dysfunction and colitis. Am J Pathol. 2014 Sep 1;184(9):2516–2527. 10.1016/j.ajpath.2014.05.019.
  • Menconi A, Hernandez-Velasco X, Vicuna EA, et al. Histopathological and morphometric changes induced by a dextran sodium sulfate (DSS) model in broilers. Poult Sci. 2015 May 1;94(5):906–911. 10.3382/ps/pev054.
  • Homa ST, Vassiliou AM, Stone J, et al. A comparison between two assays for measuring seminal oxidative stress and their relationship with sperm DNA fragmentation and semen parameters. Genes (Basel). 2019 Mar 19;10(3):236. 10.3390/genes10030236.
  • Ahmed SM, Abdelrahman SA, Shalaby SM. Evaluating the effect of silver nanoparticles on testes of adult albino rats (histological, immunohistochemical and biochemical study). J Mol Histol. 2017 Feb;48(1):9–27. doi:10.1007/s10735-016-9701-4.
  • Toocheck C, Clister T, Shupe J, et al. Mouse spermatogenesis requires classical and nonclassical testosterone signaling. Biol Reprod. 2016 Jan 1;94(1):11. 10.1095/biolreprod.115.132068.
  • Sakr SA, Mahran HA, Abo-El-Yazid SM. Effect of fenugreek seeds extract on cyclophosphamide-induced histomorphometrical, ultrastructural and biochemical changes in testes of albino mice. Toxicol Ind Health. 2012 Apr;28(3):276–288. doi:10.1177/0748233711412427.
  • Colpi GM, Contalbi GF, Nerva F, Sagone P, Piediferro G. Testicular function following chemo–radiotherapy. Eur J Obstet Gynecol Reprod Biol. 2004 Apr 5;113:S2–6. doi:10.1016/j.ejogrb.2003.11.002.
  • Nash S, Rahman MS. Short‐term heat stress impairs testicular functions in the American oyster, Crassostrea virginica: molecular mechanisms and induction of oxidative stress and apoptosis in spermatogenic cells. Mol Reprod Dev. 2019 Oct;86(10):1444–1458. doi:10.1002/mrd.23268.
  • Uyar A, Yaman T, Dogan A, et al. Is methotrexate induced testicular damage preventable using nettle seed extract: a histopathological, immunohistochemical, biochemical and spermatological examination. Fresenius Environ Bull. 2018 Jan 1;27(4):2320–2331.
  • Vidal JD, Whitney KM. Morphologic manifestations of testicular and epididymal toxicity. Spermatogenesis. 2014 Mar 4;4(2):e979099. 10.4161/21565562.2014.979099.
  • Murphy CJ, Richburg JH. Implications of Sertoli cell induced germ cell apoptosis to testicular pathology. Spermatogenesis. 2014 Mar 4;4(2):e979110. 10.4161/21565562.2014.979110.
  • Mahmoud AM, Nor-Eldin EK, Elsayed HM. The possible protective effect of Omega 3 fatty acids against bisphenol A induced disruption of pituitary-testicular axis in albino rat. biochemical, histological and immunohistochemical study. Egypt J Histol. 2019 Mar 1;42(1):215–228. 10.21608/ejh.2018.5474.1030.
  • Celik E, Oguzturk H, Sahin N, Turtay MG, Oguz F, Ciftci O. Protective effects of hesperidin in experimental testicular ischemia/reperfusion injury in rats. Arch Med Sci. 2016 Oct 1;12(5):928–934. doi:10.5114/aoms.2015.47697.
  • Kurus M, Bay Karabulut AY, Taslidere EL, Otlu O. Preventive effects of resveratrol against azoxymethane‐induced testis injury in rats. Andrologia. 2017 Aug;49(6):e12674. doi:10.1111/and.12674.
  • Ogedengbe OO, Jegede AI, Onanuga IO, et al. Adjuvant potential of virgin coconut oil extract on antiretroviral therapy‐induced testicular toxicity: an ultrastructural study. Andrologia. 2018 Apr;50(3):e12930. doi:10.1111/and.12930.
  • Farag EA, Yousry MM. Effect of mobile phone electromagnetic waves on rat testis and the possible ameliorating role of Naringenin: a histological study. Egypt J Histol. 2018 Mar 1;41(1):108–121. 10.21608/EJH.2018.7526.
  • Lu WP, Mei XT, Wang Y, Zheng YP, Xue YF, Xu DH. Zn (II)–curcumin protects against oxidative stress, deleterious changes in sperm parameters and histological alterations in a male mouse model of cyclophosphamide-induced reproductive damage. Environ Toxicol Pharmacol. 2015 Mar 1;39(2):515–524. 10.1016/j.etap.2014.12.014.
  • Moghimian M, Soltani M, Abtahi H, Shokoohi M. Effect of vitamin C on tissue damage and oxidative stress following tunica vaginalis flap coverage after testicular torsion. J Pediatr Surg. 2017 Oct 1;52(10):1651–1655. 10.1016/j.jpedsurg.2017.07.001.
  • Kapoor R, Kakkar P. Naringenin accords hepatoprotection from streptozotocin induced diabetes in vivo by modulating mitochondrial dysfunction and apoptotic signaling cascade. Toxicol Rep. 2014 Jan 1;1:569–581. doi:10.1016/j.toxrep.2014.08.002.
  • Kwatra M, Kumar V, Jangra A, et al. Ameliorative effect of naringin against doxorubicin-induced acute cardiac toxicity in rats. Pharm Biol. 2016 Apr 2;54(4):637–647. 10.3109/13880209.2015.1070879.
  • Sharma P, Huq AU, Singh R. Cypermethrin-induced reproductive toxicity in the rat is prevented by resveratrol. J Hum Reprod Sci. 2014 Apr;7(2):99. doi:10.4103/0974-1208.138867.
  • Ganaie MA. The protective effects of naringenin on testes gonadotoxicity induced by cisplatin in rats. Bull Env Pharmacol Life Sci. 2015 Dec 1;5:15–21.
  • Isik A, Peker K, Gursul C, et al. The effect of ozone and naringin on intestinal ischemia/reperfusion injury in an experimental model. Int J Surg. 2015 Sep 1;21:38–44. doi:10.1016/j.ijsu.2015.07.012.
  • Jiang B, Su Y, Chen Q, et al. Protective effects of ozone oxidative postconditioning on long-term injury after renal ischemia/reperfusion in rat. Transplantation Proc 2020 Jan 1 (Vol. 52, No. 1, pp. 365–372). Elsevier. 10.1016/j.transproceed.2019.10.004.
  • Yong L, Lyu X, Huang C, Xu Y. Effect of local ozone treatment on inflammatory cytokine, growth cytokine and apoptosis molecule expression in anal fistula wound. J Hainan Med Univ. 2017;23(14):153–156.
  • Sagai M, Bocci V. Mechanisms of action involved in ozone therapy: is healing induced via a mild oxidative stress? Med Gas Res. 2011 Dec;1(1):1–8. doi:10.1186/2045-9912-1-29.
  • Smith AJ, Oertle J, Warren D, Prato D. Ozone therapy: a critical physiological and diverse clinical evaluation with regard to immune modulation, anti-infectious properties, anti-cancer potential, and impact on anti-oxidant enzymes. Open J Mol Integrative Physiol. 2015;5(3):37.doi:10.4236/ojmip.2015.53004.
  • Di Filippo C, Trotta MC, Maisto R, et al. Daily Oxygen/O3 treatment reduces muscular fatigue and improves cardiac performance in Rats subjected to prolonged high intensity physical exercise. Oxid Med Cell Longev. 2015 Jan 1;2015:1–11. doi:10.1155/2015/190640.
  • Seyedian SS, Nokhostin F, Malamir MD. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life. 2019 Apr;12(2):113. doi:10.25122/jml-2018-0075.
  • Moghadam MT, Dadfar R, Khorsandi L. The effects of ozone and melatonin on busulfan-induced testicular damage in mice. JBRA Assist Reprod. 2021 Apr 27;25(2):176–184. doi: 10.5935/1518-0557.20200081.

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