Document Type : Original Article
Authors
- Vahid Ganjiani 1
- Nasrollah Ahmadi 2
- Hassan Sharifiyazdi 1
- Abdolhamid Meimandi-Parizi 1
- Amir Mootabi-Alavi 2
- Mahmoud Hassanpour 3
- Leili Mavalizadeh 1
1 Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.
2 Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.
3 Department of Basic Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.
Abstract
The present study was conducted to determine the protective influences of Ferulago angulata aqueous extract against testicular ischemia/reperfusion (I/R) injury in rats. Twenty-eight subjects were assigned randomly into four groups: (I) sham group, (II) torsion/detorsion (T/D) group, (III) T/D followed by treatment with F. angulata (200 mg/kg, IP), (IV) intact group with only 200 mg/kg F. angulata. T/D damage was induced by 2 hours of testis rotation 720° followed by 24 hours of reperfusion injury. After reperfusion period, biochemical and hormonal parameters were measured in the serum, epididymal sperms were collected for evaluation of sperm characteristics (count, motility, viability, and abnormal morphology rate), and testes were studied histopathologically. I/R injury was associated with significant reduction in count, viability, and all sperm kinematic parameters (p < 0.05), which could be reversed significantly by F. angulata (p < 0.05) (except for some kinematic parameters). Although the abnormal morphology rate of sperms was numerically higher in the T/D group in comparison to the sham and intact groups; the difference was not statistically significant. Histopathological assessments showed that F. angulata could significantly increase the Johnsen’s score, mean seminiferous tubular diameter, and germinal epithelial cell thickness in the treatment group compared to the T/D group (p < 0.05). GPx, SOD, and testosterone were significantly reduced following torsion/detorsion compared to the sham group (p < 0.05); and the reductions were prevented significantly by F. angulata (p < 0.05) (except for SOD). MDA level was significantly increased in the T/D group in comparison to the sham and intact groups (p < 0.05), which F. angulata was not able to reverse peroxidation index. The overall results of the research suggest that F. angulata extract can be a good natural alternative to testicular I/R injury.
Keywords
Main Subjects
- Pentyala S, Lee J, Yalamanchili P, Vitkun S, Khan SA. Testicular torsion: a review. Journal of Lower Genital Tract Disease, 2001; 5: 38-47.
- Wei S-M, Yan Z-Z, Zhou J. Protective effect of rutin on testicular ischemia-reperfusion injury. Journal of Pediatric Surgery, 2011; 46: 1419-1424.
- Dejban P, Rahimi N, Takzare N, Jahansouz M, Haddadi N-S, Dehpour AR. Beneficial effects of dapsone on ischemia/reperfusion injury following torsion/detorsion in ipsilateral and contralateral testes in rat. Theriogenology, 2019; 140: 136-142.
- Sessions AE, Rabinowitz R, Hulbert WC, Goldstein MM, Mevorach RA. Testicular torsion: direction, degree, duration and disinformation. The Journal of Urology, 2003; 169: 663-665.
- Lee J-W, Kim J-I, Lee Y-A, Lee DH, Song CS, Cho YJ, Han JS. Inhaled hydrogen gas therapy for prevention of testicular ischemia/reperfusion injury in rats. Journal of Pediatric Surgery, 2012; 47: 736-742.
- Jiang D, Wu D, Zhang Y, Xu B, Sun X, Li Z. Protective effects of hydrogen rich saline solution on experimental testicular ischemia-reperfusion injury in rats. The Journal of Urology, 2012; 187: 2249-2253.
- Parlaktas B, Atilgan D, Gencten Y, Akbas A, Markoc F, Erdemir F, Ozyurt H, Uluocak N. The effects of carvedilol on ischemia-reperfusion injury in the rat testis. International Brazilian Journal of Urology, 2014; 40: 109-117.
- Turan I, Demir S, Kilinc K, Burnaz NA, Yaman SO, Akbulut K, Mentese A, Aliyazicioglu Y, Deger O Antiproliferative and apoptotic effect of Morus nigra extract on human prostate cancer cells. Saudi Pharmaceutical Journal, 2017; 25: 241-248.
- Heidari S, Akrami H, Gharaei R, Jalili A, Mahdiuni H, Golezar E. Anti-tumor activity of Ferulago angulata Boiss. extract in gastric cancer cell line via induction of apoptosis. Iranian Journal of Pharmaceutical Research, 2014; 13: 1335-1345.
- Rostami F, Ghasemi HA, Taherpour K. Effect of Scrophularia striata and Ferulago angulata, as alternatives to virginiamycin, on growth performance, intestinal microbial population, immune response, and blood constituents of broiler chickens. Poultry Science, 2015; 94: 2202-2209.
- Pirbalouti AG, Sedaghat L, Hamedi B, Tirgir F. Chemical composition and antioxidant activity of essential oils of three endemic medicinal plants of Iran. Bangladesh Journal of Botany, 2013; 42: 327-332.
- Khanahmadi M, Janfeshan K. Study on antioxidation property of Ferulago angulata plant. Asian Journal of Plant Sciences, 2006; 5: 521-526.
- Govahi R, Ghalamkari G, Toghyani M, Eghbal Saied S, Mohammadrezaei M, Shahryari M, Dehghani Abari A. Effect of Ferulago angulata sub. carduchorum on total serum antioxidant activity and some of the humoral immune responses in broiler chicks. Journal of Medicinal Herbs, 2013; 4: 119-126.
- Valipour P, Heidarian E, Khoshdel A, Gholami AM. Protective effects of hydroalcoholic extract of Ferulago angulata against gentamicin-induced nephrotoxicity in rats. Iranian Journal of Kidney Diseases, 2016; 10(4): 189-196.
- Sharifi F, Rafieirad M, Sazegar H. Effects of Ferulago angulata extract against oxidative stress induced by 6-hydroxydopamine in rats. Journal of Medicinal Plants, 2015; 14(53): 34-44.
- Mousavi-Ezmareh S-F, Mazani M, Heidarian E, Alipanah Moghadam R, Rafieian-kopaei M, Mardanian G, Rezagholizadeh L, Shamsazar A The effect of hydroalcoholic extract of Ferulago angulata on liver function parameters and antioxidant status in alloxan-induced diabetic rats. European Journal of Medicinal Plants, 2017; 20(2): 1-9.
- Zakavi I, Karimian A, Isazadeh R, Bahadoram M, Sough AJ, Valipour AA. Effect of aquatic extract of Ferulago angulata Boiss with aerobic exercises on serum levels of interleukin-10 and C-reactive protein of obese males. Crescent Journal of Medical and Biological Sciences, 2018; 5(4): 320-326.
- Farzaei F, Heydarpour F, Farzaei MH, Haghighi ZMS, Abbasabadi Z, Sadeghi E. Protective effect of Ferulago angulata (Schltdl.) Boiss. hydroalcoholic extract against acetic acid-induced colitis in rat: Role of pro-inflammatory cytokines. Pharmacognosy Research, 2018; 10(4): 391-396.
- Andrade LN, De Sousa DP. A review on anti-inflammatory activity of monoterpenes. Molecules, 2013; 18: 1227-1254.
- Ganjiani V, Tabatabaei M, Golvajouei MS. A comparative and dose-dependent evaluation on Stevia rebaudiana antimicrobial activity; A challengeable study. Journal of Medicinal plants and By-product, 2021; 10: 77-82.
- Ganjiani V, Ahmadi N, Divar MR, Sharifiyazdi H, Meimandi-Parizi A. Protective effects of crocin on testicular torsion/detorsion in rats. Theriogenology, 2021; 173: 241-248.
- Nassab GR, Bohlouli S, Ghanbari A, alilian N, Ahmadi F, Farhadi E, Shokoohinia Y, Bahrami G, Taherabadi F, Jaffari F, Hosseinzadeh L. Therapeutic effect of Ferulago angulata extract on reproductive parameters and serum testosterone levels in diabetic male rats. Journal of Reports in Pharmaceutical Sciences, 2018; 7: 1-8.
- Jahromi AR, Rasooli R, Kamali Y, Ahmadi N, Sattari E. Short-term effects of date palm extract (Phoenix dactylifera) on ischemia/reperfusion injury induced by testicular torsion/detorsion in rats. Pharmacognosy Research, 2017; 9: 69-73.
- Johnsen SG. Testicular biopsy score count–a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormone Research in Paediatrics, 1970; 1: 2-25.
- Gozukara KH, Ozcan O, Ozgur T, Kaya YS, Tutuk O. Protective effects of colchicine on testicular torsion/detorsion-induced ischemia/reperfusion injury in rats. Urology Journal, 2020; 17(3): 294-300.
- Payabvash S, Salmasi AH, Kiumehr S, Tavangar SM, Nourbakhsh B, Faghihi SH, Dehpour AR. Salutary effects of N-acetylcysteine on apoptotic damage in a rat model of testicular torsion. Urologia Internationalis, 2007; 79: 248-254.
- Turkmen S, Mentese A, Karaguzel E, Karaca Y, Kucuk A, Uzun A, Yulug E, Turedi S. A comparison of the effects of N-acetylcysteine and ethyl pyruvate on experimental testicular ischemia-reperfusion injury. Fertility and Sterility, 2012; 98: 626-631.
- Aktaş BK, Bulut Ş, Bulut S, Baykam MM, Özden C, Şenes M, Yücel D, Memiş A. The effects of N-acetylcysteine on testicular damage in experimental testicular ischemia/reperfusion injury. Pediatric Surgery International, 2010; 26: 293-298.
- Akbari G, Mard SA, Veisi A. A comprehensive review on regulatory effects of crocin on ischemia/reperfusion injury in multiple organs. Biomedicine and Pharmacotherapy, 2018; 99: 664-670.
- Tillhon M, Ortiz LMG, Lombardi P, Scovassi AI. Berberine: new perspectives for old remedies. Biochemical Pharmacology, 2012; 84: 1260-1267.
- Tabatabaei Yazdi F, Alizade Behbahani B, Heidari Sureshjani M. The comparison of antimicrobial effects of Chevil (Ferulago angulata) extract with a variety of common therapeutic antibiotics in vitro. Journal of Arak University of Medical Sciences, 2014; 17: 35-46.
- Hritcu L, Bagci E, Aydin E, Mihasan M. Antiamnesic and antioxidants effects of Ferulago angulata essential oil against scopolamine-induced memory impairment in laboratory rats. Neurochemical Research, 2015; 40: 1799-1809.
- Bohlouli S. Effect of hydroalcoholic extract of Ferollago angulata on sperm and testosterone indices in male rats. Scientific Journal of Ilam University of Medical Sciences, 2019; 27: 47-55.
- Naderi N, Souri M, Nasr Esfahani MH, Hajian M, Tanhaei Vash N. Ferulago angulata extract ameliorates epididymal sperm toxicity in mice induced by lead and diazinon. Andrology, 2020; 8: 706-718.
- Ganjiani V, Ahmadi N, Raayat Jahromi A. Protective effects of Stevia rebaudiana aqueous extract on experimental unilateral testicular ischaemia/reperfusion injury in rats. Andrologia, 2020; 52: e13469.
- Erdemir F, Parlaktaş BS, Özyurt H, Boztepe Ö, Atiş Ö, Şahin S. Antioxidant effect of melatonin in systemic circulation of rats after unilateral testicular torsion. Turkish Journal of Medical Sciences, 2008; 38: 1-6.
- Güzel M, Sönmez MF, Baştuğ O, Aras NF, Öztürk AB, Küçükaydın M, Turan C. Effectiveness of lycopene on experimental testicular torsion. Journal of Pediatric Surgery, 2016; 51: 1187-1191.
- Rafieian-Kopaei M, Shahinfard N, Rouhi-Boroujeni H, Gharipour M, Darvishzadeh-Boroujeni P. Effects of Ferulago angulata extract on serum lipids and lipid peroxidation. Evidence-Based Complementary and Alternative Medicine, 2014; https://doi.org/10.1155/2014/680856.
- Aprioku JS. Pharmacology of free radicals and the impact of reactive oxygen species on the testis. Journal of Reproduction and Infertility, 2013; 14: 158-172.
- Turner T. Acute experimental testicular torsion: no effect on the contralateral testis. Journal of Andrology, 1985; 6: 65-72.
- Aktoz T, Kanter M, Aktas C. Protective effects of quercetin on testicular torsion/detorsion‐induced ischaemia‐reperfusion injury in rats. Andrologia, 2010; 42: 376-383.
- Abdel-Gaber SA, Mohammed RK, Refaie MM. Mechanism mediating the protective effect of diacerein in ischemia-reperfusion-induced testicular injury in rats. Life Sciences, 2018; 209: 57-62.