Advances in Clinical and Experimental Medicine

Title abbreviation: Adv Clin Exp Med
JCR Impact Factor (IF) – 1.736
5-Year Impact Factor – 2.135
Index Copernicus  – 168.52
MEiN – 70 pts

ISSN 1899–5276 (print)
ISSN 2451-2680 (online)
Periodicity – monthly

Download original text (EN)

Advances in Clinical and Experimental Medicine

2018, vol. 27, nr 5, May, p. 591–597

doi: 10.17219/acem/68896

Publication type: original article

Language: English

Download citation:

  • BIBTEX (JabRef, Mendeley)
  • RIS (Papers, Reference Manager, RefWorks, Zotero)

The protective effect of Gingko biloba in a rat model of ovarian ischemia/reperfusion injury: Improvement in histological and biochemical parameters

Nuri Yildirim1,A,D,F, Deniz Simsek1,C,D, Semir Kose2,C,E, Alkim Gulsah Sahingoz Yildirim3,B,E, Cagri Guven1,C,E, Gurkan Yigitturk4,B,E, Oytun Erbas5,A,E,F

1 Department of Obstetrics and Gynecology, Ege University, Izmir, Turkey

2 Department of Obstetrics and Gynecology, Dokuz Eylul University, Izmir, Turkey

3 Department of Obstetrics and Gynecology, Tepecik Maternity and Research Hospital, Izmir, Turkey

4 Department of Histology and Embryology, Ege University, Izmir, Turkey

5 Department of Physiology, Bilim University, Istanbul, Turkey


Background. Ovarian torsion is one of the most common gynecological emergencies, which especially affects women of reproductive age.
Objectives. We aimed to evaluate the effect of Ginkgo biloba (GB) supplementation in ovarian ischemia/ reperfusion injury in an experimental torsion/de-torsion rat model.
Material and Methods. This study was carried out in the Ege University Faculty of Medicine in Izmir, Turkey. Thirty mature female Sprague-Dawley albino rats were randomly divided into 5 groups: in Group 1 (control), the abdominal wall was only opened and closed; in the torsion group (Group 2), ischemia was induced for 3 h, using atraumatic vascular clips to create a torsion model; in the torsion/GB group (Group 3), the rats were given 80 mg/kg (oral gavage) of GB 30 min before torsion was induced and the torsion model was formed; in the torsion/de-torsion group (Group 4), the rats underwent 3 h of ischemia and then the vascular clips were removed and reperfusion took place for 3 h; in the torsion/de-torsion/GB group (Group 5), the rats underwent 3 h of ischemia followed by GB (oral gavage) 30 min prior to a 3-h reperfusion period. Ovarian tissue damage was evaluated by a histopathological scoring system. Ovarian tissue malondialdehyde (MDA) and plasma pentraxin-3 were measured.
Results. In comparison with the sham group, both the torsion and torsion/de-torsion groups had significantly higher scores for follicular degeneration, vascular congestion, edema, hemorrhage, and leukocyte infiltration. Ginkgo biloba significantly decreased these scores in both groups. Ovarian malondialdehyde and plasma pentraxin 3 were significantly higher both in the torsion and torsion/de-torsion groups compared with the sham group. Ginkgo biloba decreased these levels significantly both in the torsion/GB and torsion/de-torsion/GB groups.
Conclusion. Supplementing GB during a surgical procedure decreases ischemia/reperfusion injury to an ovary in an experimental rat model based on histopathological parameters, tissue malondialdehyde, and plasma pentraxin-3 levels.

Key words

malondialdehyde, ischemia/reperfusion injury, ovarian torsion, Ginkgo biloba, pentraxin-3

References (33)

  1. Hibbard LT. Adnexal torsion. Am J Obstet Gynecol. 1985;152(4):456–461.
  2. Mashiach S, Bider D, Moran O, Goldenberg M, Ben-Rafael Z. Adnexal torsion of hyperstimulated ovaries in pregnancies after gonadotropin therapy. Fertil Steril. 1990;53(1):76–80.
  3. Houry D, Abbott JT. Ovarian torsion: A fifteen-year review. Ann Emerg Med. 2001;38(2):156–159.
  4. Huchon C, Fauconnier A. Adnexal torsion: A literature review. Eur J Obstet Gynecol Reprod Biol. 2010;150(1):8–12.
  5. Jennings RB, Murry CE, Steenbergen C Jr, Reimer KA. Development of cell injury in sustained acute ischemia. Circulation. 1990;82(3):II2–12.
  6. Diamond JM, Wigfield CH. Role of innate immunity in primary graft dysfunction after lung transplantation. Curr Opin Organ Transplant. 2013;18(5):518–523.
  7. Zhu H, Cui D, Liu K, et al. Long pentraxin PTX3 attenuates ischemia reperfusion injury in a cardiac transplantation model. Transpl Int. 2014;27(1):87–95.
  8. Ergenoglu M, Erbaş O, Akdemir A, et al. Attenuation of ischemia/reperfusion-induced ovarian damage in rats: Does edaravone offer protection? Eur Surg Res. 2013;51(1–2):21–32.
  9. Yildirim N, Yigitturk G, Sahingoz Yildirim AG, et al. Octreotide protects ovary against ischemia-reperfusion injury in rats: Evaluation of histological and biochemical parameters. J Obstet Gynaecol Res. 2015;41(10):1591–1597.
  10. Akdemir A, Erbas O, Gode F, et al. Protective effect of oxytocin on ovarian ischemia-reperfusion injury in rats. Peptides. 2014;55:126–130.
  11. Wada K, Ishigaki S, Ueda K, et al. Studies on the constitution of edible and medicinal plants. I. Isolation and identification of 4-O-methylpyridoxine, toxic principle from the seed of Ginkgo biloba L. Chem Pharm Bull. 1988;36(5):1779–1782.
  12. Oyama Y, Fuchs PA, Katayama N, Noda K. Myricetin and quercetin, the flavonoid constituents of Ginkgo biloba extract, greatly reduce oxidative metabolism in both resting and Ca(2+)-loaded brain neurons. Brain Res. 1994;635(1–2):125–129.
  13. Benzi G, Moretti A. Are reactive oxygen species involved in Alzheimer’s disease? Neurobiol Aging. 1995;16(4):661–674.
  14. Guo RZ, Liu XG, Gao W, et al. A strategy for screening antioxidants in Ginkgo biloba extract by comprehensive two-dimensional ultra high performance liquid chromatography. J Chromatogr A. 2015; 27(1422):147–154.
  15. Guven S, Muci E, Unsal MA, et al. The effects of carbon dioxide pneumoperitoneum on ovarian blood flow, oxidative stress markers, and morphology during laparoscopy: A rabbit model. Fertil Steril. 2010;93(4):1327–1332.
  16. Tukozkan N, Erdamar H, Seven I. Measurement of total malondialdehyde in plasma and tissues by high-performance liquid chromatography and thiobarbituric acid assay. Firat Medical Journal. 2006;11(2): 88–92.
  17. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
  18. Saraste A, Pulkki K, Kallajoki M, et al. Apoptosis in human acute myocardial infarction. Circulation. 1997;95(2):320–323.
  19. Cannon RO 3rd. Mechanisms, management and future directions for reperfusion injury after acute myocardial infarction. Nat Clin Pract Cardiovasc Med. 2005;2(2):88–94.
  20. Ude C, Schubert-Zsilavecz M, Wurglics M. Ginkgo biloba extracts: A review of the pharmacokinetics of the active ingredients. Clin Pharmacokinet. 2013;52(9):727–749.
  21. Isah T. Rethinking Ginkgo biloba L. Medicinal uses and conservation. Pharmacogn Rev. 2015;9(18):140–148.
  22. Nakanishi K. Terpene trilactones from Ginkgo biloba: From ancient times to the 21st century. Bioorg Med Chem. 2005;13(17):4987–5000.
  23. Ding XP, Qi J, Chang YX, et al. Quality control of flavonoids in Ginkgo biloba leaves by high-performance liquid chromatography with diode array detection and on-line radical scavenging activity detection. J Chromatogr A. 2009;1216(11):2204–2210.
  24. Janssens D, Michiels C, Delaive E, et al. Protection of hypoxiainduced ATP decrease in endothelial cells by Ginkgo biloba extract and bilobalide. Biochem Pharmacol. 1995;50(7):991–999.
  25. Smith JV, Luo Y. Studies on molecular mechanisms of Ginkgo biloba extract. Appl Microbiol Biotechnol. 2004;64(4):465–472.
  26. Zheng LT, Ock J, Kwon B, Suk K. Suppressive effects of flavonoid fisetin on lipopolysaccharide-induced microglial activation and neurotoxicity. Int Immunopharmacol. 2008;8(3):484–494.
  27. Pizzorno JE, Murray MT. A Textbook of Natural Medicine . Seattle: John Bastyr College Publications; 1985.
  28. Das A, Shanker G, Nath C, et al. A comparative study in rodents of standardized extracts of Bacopa monniera and Ginkgo biloba: Anticholinesterase and cognitive enhancing activities. Pharmacol Biochem Behav. 2002;73(4):893–900.
  29. Yallapragada PR, Velaga MK. Effect of Ginkgo biloba extract on lead-induced oxidative stress in different regions of rat brain. J Environ Pathol Toxicol Oncol. 2015;34(2):161–173.
  30. Leistner E, Drewke C. Ginkgo biloba and ginkgotoxin. J Nat Prod. 2010;73(1):86–92.
  31. Shimizu T, Suzuki S, Sato A, et al. Cardio-protective effects of pentraxin-3 produced from bone marrow-derived cells against ischemia/reperfusion injury. J Mol Cell Cardiol. 2015;2828(15):30084–30085.
  32. Hansson GK, Libby P. The immune response in atherosclerosis: A double-edged sword. Nat Rev Immunol. 2006;6(7):508–519.
  33. Akman L, Erbas O, Terek MC, et al. The long pentraxin-3 is a useful marker for diagnosis of ovarian torsion: An experimental rat model. J Obstet Gynaecol. 2015;15:1–4.