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A new approach to prevent ischemia/reperfusion injury in a rat model: remote ischemic conditioning

  • Gynecologic Oncology
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the effect of remote ischemic conditioning (RIC) on ovarian ischemia/reperfusion injury in a rat model.

Methods

A total of 36 Wistar albino rats with a body weight of 220–250 g were used for this study. Right adnexal torsion was performed for 180 min, and at the end of the period, the adnex was released and the abdomen was reclosed for 180 min for reperfusion. Torsion and detorsion procedures were applied to all rats except group 1 (sham, control). The right lower extremity was tied to perform remote tissue ischemia in groups 3, 4, 5, and 6. The goal of the procedure, which was purplish discoloration and pulselessness of the extremity, was maintained. After 5 min of ischemia, reperfusion was achieved for 5 min. Repeating this procedure 3 times was defined as hypoxia attacks (RIC). Retrieved ovaries were examined for tissue injury with biochemical, histopathologic, and immunohistochemical analysis.

Results

Unlike the control group, vascular congestion, hemorrhage, edema, and inflammatory cell infiltration were observed in group 2 (only I/R [ischemia/reperfusion]). In groups 3 (I/R + RIC), 4 (I/R + RIC), 5 (I/R + RIC), and 6 (I/R + RIC), edema and inflammatory cell infiltration were not observed. However, vascular congestion and hemorrhage that were detected in these groups were higher than in group 1 (Control) and less than in group 2 (I/R). The Caspase-3 Index was found to be increased in all groups compared to group 1 (P < .001). However, the increase in the RIC-performed groups was significantly less than in group 2. The apoptotic index, which was determined by the TUNEL, was also found to be increased in all groups compared to group 1 (P < .001). When the comparison was made in relation to group 2, the decrease of AI in RIC-performed groups was statistically significant, except the decrease in group 6 (P = .29).

Conclusions

It is not clinically conceivable to prepare the tissue for pre-ischemia in ovarian torsion. However, the RIC application, which will be initiated if torsion is suspected when arrangements are made for surgery, might be a simple, effective, and inexpensive approach to prevent I/R injury in the clinic.

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References

  1. McWilliams GD, Hill MJ, Dietrich CS 3rd (2008) Gynecologic emergencies. Surg Clin North Am 88(2):265–283, vi. https://doi.org/10.1016/j.suc.2007.12.007

    Article  PubMed  Google Scholar 

  2. Somuncu S, Cakmak M, Dikmen G, Akman H, Kaya M (2008) Ischemia-reperfusion injury of rabbit ovary and protective effect of trapidil: an experimental study. Pediatr Surg Int 24(3):315–318. https://doi.org/10.1007/s00383-007-2079-3

    Article  PubMed  Google Scholar 

  3. Hibbard LT (1985) Adnexal torsion. Am J Obstet Gynecol 152(4):456–461

    Article  CAS  PubMed  Google Scholar 

  4. Oelsner G, Cohen SB, Soriano D, Admon D, Mashiach S, Carp H (2003) Minimal surgery for the twisted ischaemic adnexa can preserve ovarian function. Hum Reprod 18(12):2599–2602

    Article  PubMed  Google Scholar 

  5. Galinier P, Carfagna L, Delsol M, Ballouhey Q, Lemasson F, Le Mandat A, Moscovici J, Guitard J, Pienkowski C, Vaysse P (2009) Ovarian torsion. Management and ovarian prognosis: a report of 45 cases. J Pediatr Surg 44(9):1759–1765. https://doi.org/10.1016/j.jpedsurg.2008.11.058

    Article  PubMed  Google Scholar 

  6. Borekci B, Gundogdu C, Altunkaynak BZ, Calik M, Altunkaynak ME, Unal D, Unal B (2009) The protective effect of dehydroepiandrosterone on ovarian tissues after torsion-detorsion injury: a stereological and histopathological study. Eurasian J Med 41(1):22–27

    PubMed  PubMed Central  Google Scholar 

  7. Zhai Y, Petrowsky H, Hong JC, Busuttil RW, Kupiec-Weglinski JW (2013) Ischaemia-reperfusion injury in liver transplantation—from bench to bedside. Nat Rev Gastroenterol Hepatol 10(2):79–89. https://doi.org/10.1038/nrgastro.2012.225

    Article  CAS  Google Scholar 

  8. Limani P, Linecker M, Oberkofler CE, Barmettler G, Kaech A, Graf R, Humar B, Clavien PA (2016) Remote ischemic preconditioning: a novel strategy in rescuing older livers from ischemia-reperfusion injury in a rodent model. Ann Surg 264(5):797–803. https://doi.org/10.1097/sla.0000000000001765

    Article  PubMed  Google Scholar 

  9. Wang S, Li H, He N, Sun Y, Guo S, Liao W, Liao Y, Chen Y, Bin J (2017) Impact of remote ischaemic preconditioning on major clinical outcomes in patients undergoing cardiovascular surgery: a meta-analysis with trial sequential analysis of 32 randomised controlled trials. Int J Cardiol 227:882–891. https://doi.org/10.1016/j.ijcard.2016.11.278

    Article  PubMed  Google Scholar 

  10. Xia M, Ding Q, Zhang Z, Feng Q (2017) Remote limb ischemic preconditioning protects rats against cerebral ischemia via HIF-1alpha/AMPK/HSP70 pathway. Cell Mol Neurobiol 37(6):1105–1114. https://doi.org/10.1007/s10571-016-0444-2

    Article  CAS  PubMed  Google Scholar 

  11. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol Med 26(9–10):1231–1237

    Article  CAS  Google Scholar 

  12. Kruger E, Heller DS (1999) Adnexal torsion. A clinicopathologic review of 31 cases. J Reprod Med 44(2):71–75

    CAS  PubMed  Google Scholar 

  13. Calis P, Bozdag G, Karakoc Sokmensuer L, Kender N (2015) Does ischemia-reperfusion injury affect ovarian reserve and follicle viability in a rat model with adnexal torsion? Eur J Obstet Gynecol Reprod Biol 185:126–130. https://doi.org/10.1016/j.ejogrb.2014.12.006

    Article  CAS  PubMed  Google Scholar 

  14. Rody A, Jackisch C, Klockenbusch W, Heinig J, Coenen-Worch V, Schneider HP (2002) The conservative management of adnexal torsion—a case-report and review of the literature. Eur J Obstet Gynecol Reprod Biol 101(1):83–86

    Article  CAS  PubMed  Google Scholar 

  15. Granger DN, Kvietys PR (2015) Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol 6:524–551. https://doi.org/10.1016/j.redox.2015.08.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ozsoy AZ, Nursal AF, Arici A, Butun I, Uysal M, Irmak Sapmaz H, Kunt Isguder C, Yilmaz Dogru H, Tas U (2016) Effects of carvedilol on an ischemia/reperfusion model: biochemical, histopathological and immunohistochemical evaluation. J Obstet Gynaecol Res 42(9):1132–1140. https://doi.org/10.1111/jog.13028

    Article  CAS  PubMed  Google Scholar 

  17. Akdemir A, Sahin C, Erbas O, Yeniel AO, Sendag F (2015) Is ursodeoxycholic acid crucial for ischemia/reperfusion-induced ovarian injury in rat ovary? Arch Gynecol Obstet 292(2):445–450. https://doi.org/10.1007/s00404-015-3646-9

    Article  CAS  PubMed  Google Scholar 

  18. Tokgoz VY, Sipahi M, Keskin O, Guvendi GF, Takir S (2018) Protective effects of vitamin D on ischemia-reperfusion injury of the ovary in a rat model. Iran J Basic Med Sci 21(6):593–599. https://doi.org/10.22038/ijbms.2018.26914.6581

    Article  PubMed  PubMed Central  Google Scholar 

  19. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136

    Article  CAS  Google Scholar 

  20. Zhai Y, Busuttil RW, Kupiec-Weglinski JW (2011) Liver ischemia and reperfusion injury: new insights into mechanisms of innate-adaptive immune-mediated tissue inflammation. Am J Transplant 11(8):1563–1569. https://doi.org/10.1111/j.1600-6143.2011.03579.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Petrowsky H, McCormack L, Trujillo M, Selzner M, Jochum W, Clavien PA (2006) A prospective, randomized, controlled trial comparing intermittent portal triad clamping versus ischemic preconditioning with continuous clamping for major liver resection. Ann Surg 244(6):921–928. https://doi.org/10.1097/01.sla.0000246834.07130.5d (Discussion 928–930)

    Article  PubMed  PubMed Central  Google Scholar 

  22. Gill R, Kuriakose R, Gertz ZM, Salloum FN, Xi L, Kukreja RC (2015) Remote ischemic preconditioning for myocardial protection: update on mechanisms and clinical relevance. Mol Cell Biochem 402(1–2):41–49. https://doi.org/10.1007/s11010-014-2312-z

    Article  CAS  PubMed  Google Scholar 

  23. Gassanov N, Nia AM, Caglayan E, Er F (2014) Remote ischemic preconditioning and renoprotection: from myth to a novel therapeutic option? J Am Soc Nephrol 25(2):216–224. https://doi.org/10.1681/asn.2013070708

    Article  CAS  PubMed  Google Scholar 

  24. Hausenloy DJ, Yellon DM (2008) Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res 79(3):377–386. https://doi.org/10.1093/cvr/cvn114

    Article  CAS  PubMed  Google Scholar 

  25. Maulik N, Yoshida T, Das DK (1998) Oxidative stress developed during the reperfusion of ischemic myocardium induces apoptosis. Free Radical Biol Med 24(5):869–875

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Vehbi Yavuz Tokgoz for coordination at the beginning of the study.

Funding

The study was supported by the Giresun University BAP Committee (SAG-BAP-A-160317-87).

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Giresun University, Ataturk Bulvari, Teyyareduzu Mahallesi, Giresun, 28200, Turkey

    Mehmet Sipahi

  2. Department of Emergency Medicine, Giresun University, Giresun, Turkey

    Mucahit Gunaydin

  3. Department of General Surgery, Giresun University, Giresun, Turkey

    Tugrul Kesicioglu

  4. Department of Medical Biochemistry, Giresun University, Giresun, Turkey

    Murat Usta

  5. Biology Department of Council of Forensic Medicine, Izmir, Turkey

    Berna Tezcan Yavuz

  6. Department of Histology and Embryology, Ege University, Izmir, Turkey

    Canberk Tomruk

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  1. Mehmet Sipahi
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  4. Murat Usta
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Contributions

MS: 65%: Hypothesis, development of project, surgery, and statistical analyses. MG: 10%: Surgery. TK: 10%: Surgery. Murat Usta: 5%: Biochemistry. BT: 5%: Histology. CT: 5%: Histology

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Correspondence to Mehmet Sipahi.

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Sipahi, M., Gunaydin, M., Kesicioglu, T. et al. A new approach to prevent ischemia/reperfusion injury in a rat model: remote ischemic conditioning. Arch Gynecol Obstet 299, 1691–1699 (2019). https://doi.org/10.1007/s00404-019-05149-1

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  • DOI: https://doi.org/10.1007/s00404-019-05149-1

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