Evaluation of experimental models in rats for induction of ovarian ischemia
DOI:
https://doi.org/10.33448/rsd-v11i14.36012Keywords:
Ovarian torsion; Reperfusion injury; Rats.Abstract
Gynecological emergencies are common, and ovarian torsion is the main situation encountered. Its consequences can range from acute unilateral pelvic pain to female infertility, and in order to avoid this, the most reliable studies possible are needed. Thus, the aim was to evaluate the techniques used in ovarian ischemia in rats. From this, an analysis of the most used methods, biochemical and histopathological analyzes was made, so that a comparison could be established with those that may be more efficient in carrying out studies to alleviate the problems caused by ovarian torsion. A search was carried out on the Pubmed, Scielo and Lilacs platforms, from 2017 to 2022, with the descriptors “ovarian torsion”, “Reperfusion injury” and “rats”, and 50 articles were selected. The results were that 62% of the articles used a vascular clamp, the main biochemical marker was malondialdehyde in 70%, and the histopathological markers were related to tissue integrity, such as follicular degeneration, edema, leukocyte infiltration and vascular congestion. Thus, it can be inferred that they are the most effective methods to simulate ovarian ischemia.
References
Abdel-Gaber, S. A., Atta, M., Abdel-Hafez, S., & Abdelzaher, W. Y. (2020). Ameliorative effect of nicorandil in ovarian ischemia-reperfusion-induced injury in rats: role of potassium channel. Naunyn-Schmiedeberg's archives of pharmacology, 393(9), 1599–1610. https://doi.org/10.1007/s00210-020-01854-w
Agartan, E. S., Mogulkoc, R., Baltaci, A. K., Menevse, E., Dasdelen, D., & Avunduk, M. C. (2022). 3',4'-Dihydroxyflavonol (DiOHF) prevents DNA damage, lipid peroxidation and inflammation in ovarian ischaemia-reperfusion injury of rats. Journal of obstetrics and gynaecology: the journal of the Institute of Obstetrics and Gynaecology, 42(2), 338–345. https://doi.org/10.1080/01443615.2021.1916813
Ali, F. F., Ahmed, A. F., & Elroby Ali, D. M. (2019). Underlying mechanisms behind the protective effect of angiotensin (1-7) in experimental rat model of ovarian ischemia reperfusion injury. Life sciences, 235, 116840. https://doi.org/10.1016/j.lfs.2019.116840
Allam, E. A., Abdel Moniem, R. A., & Soliman, G. Y. (2022). Functional and structural assessment of the possible protective effect of platelet-rich plasma against ischemia/reperfusion-induced ovarian injury in adult rats. The Chinese journal of physiology, 65(2), 64–71. https://doi.org/10.4103/cjp.cjp_3_22
Atasever, M., & Bakacak, Z. (2017). Nigella Sativa Oil Protects the Rat Ovary from Oxidative Injury Due to Ischemia-Reperfusion. Medical science monitor: international medical journal of experimental and clinical research, 23, 5027–5033. https://doi.org/10.12659/msm.905356
Barbosa, K. B. F., Costa, N. M. B., Alfenas, R. de C. G., De Paula, S. O., Minim, V. P. R., & Bressan, J. (2010). Estresse oxidativo: conceito, implicações e fatores modulatórios. Revista de Nutrição, 23(4), 629–643. https://doi.org/10.1590/s1415-52732010000400013
Barghi, B., Shokoohi, M., Khaki, A. A., Khaki, A., Moghimian, M., & Soltani, M. (2021). Eugenol improves tissue damage and oxidative stress in adult female rats after ovarian torsion/detorsion. Journal of obstetrics and gynaecology : the journal of the Institute of Obstetrics and Gynaecology, 41(6), 933–938. https://doi.org/10.1080/01443615.2020.1816938
Behroozi-Lak, T., Ebrahimpour, M., Zarei, L., Pourjabali, M., Farhad, N., & Mohaddesi, H. (2018). Systemic administration of curcumin nanoparticles protects ischemia-reperfusion injury in ovaries: An animal model study. Revista da Associação Médica Brasileira (1992), 64(1), 22–31. https://doi.org/10.1590/1806-9282.64.01.22
Beyazit, F., Büyük, B., Turkon, H., Elmas, S., & Uzun, M. (2019). Adalimumab mitigates ovarian ischemia-reperfusion injury in rats by regulating oxidative stress, apoptosis and resolution of inflammation. The journal of obstetrics and gynaecology research, 45(2), 358–367. https://doi.org/10.1111/jog.13846
Campana, G. (n.d.). Exame anti-mulleriano: Conheça a relação desse hormônio com a fertilidade feminina. Alta. https://altadiagnosticos.com.br/saude/hormonio-antimuleriano-e-o-exame
Çandar, T., Uzunlar, Ö., Kiseli, M., & Özcan, S. (2021). The effect of folate on ischemia/reperfusion injury in a rat adnexal torsion model. Archives of gynecology and obstetrics, 303(6), 1495–1500. https://doi.org/10.1007/s00404-020-05934-3
Castro e Silva Jr., O., Centurion, S., Pacheco, E. G., Brisotti, J. L., Oliveira, A. F., & Sasso, K. D. (2002). Aspectos básicos da lesão de isquemia e reperfusão e do pré-condicionamento isquêmico. Acta Cirúrgica Brasileira, 17, 96–100. https://doi.org/10.1590/S0102-86502002000900020
Celik Kavak, E., Gulcu Bulmus, F., Bulmus, O., Kavak, S. B., & Kocaman, N. (2018). Magnesium: does it reduce ischemia/reperfusion injury in an adnexal torsion rat model?. Drug design, development and therapy, 12, 409–415. https://doi.org/10.2147/DDDT.S157115
Colak, S., Gurlek, B., Topcu, A., Tumkaya, L., Mercantepe, T., & Yilmaz, A. (2020). Protective effects of nebivolol on ovarian ischemia-reperfusion injury in rat. The journal of obstetrics and gynaecology research, 46(11), 2407–2416. https://doi.org/10.1111/jog.14503
Coskun, A., Coban, Y. K., & Ciralik, H. (2009). Critical ischemic time for the rat ovary: Experimental study evaluating early histopathologic changes. Journal of Obstetrics and Gynaecology Research, 35(2), 330–334. https://doi.org/10.1111/j.1447-0756.2008.00874.x
Dayangan Sayan, C., Karaca, G., Sema Ozkan, Z., Tulmac, O. B., Ceylan Isik, A., Devrim, T., Aydin, G., & Yeral, I. (2018). What is the protective effect of metformin on rat ovary against ischemia-reperfusion injury?. The journal of obstetrics and gynaecology research, 44(2), 278–285. https://doi.org/10.1111/jog.13524
Demir Çaltekin, M., Özkut, M. M., Çaltekin, İ., Kaymak, E., Çakır, M., Kara, M., & Yalvaç, E. S. (2021). The protective effect of JZL184 on ovarian ischemia reperfusion injury and ovarian reserve in rats. The journal of obstetrics and gynaecology research, 47(8), 2692–2704. https://doi.org/10.1111/jog.14859
Demir, M., Yilmaz, B., Kalyoncu, S., Tuncer, M., Bozdag, Z., Ince, O., Bozdayi, M. A., Ulusal, H., & Taysi, S. (2021). Metformin reduces ovarian ischemia reperfusion injury in rats by improving oxidative/nitrosative stress. Taiwanese journal of obstetrics & gynecology, 60(1), 45–50. https://doi.org/10.1016/j.tjog.2020.10.004
Değer, U., & Çavuş, Y. (2020). Investigation of the role of rosmarinic acid treatment in regulating inflammation, cell damage, and angiogenesis in rat ovarian torsion and detorsion models. Acta cirurgica brasileira, 35(3), e202000304. https://doi.org/10.1590/s0102-865020200030000004
Eken, M. K., Ersoy, G. S., Kaygusuz, E. I., Devranoğlu, B., Takır, M., Çilingir, Ö. T., & Çevik, Ö. (2019). Etanercept protects ovarian reserve against ischemia/reperfusion injury in a rat model. Archives of medical science : AMS, 15(4), 1104–1112. https://doi.org/10.5114/aoms.2017.72406
Erdem, A. O., Ozkisacik, S., Coskun, O. D., Dogan, S., Culhaci, N., & Yazici, M. (2020). The long-term protective effect of hypothermia and gradual detorsion on ovarian tissue in adnexal torsion/detorsion model in rats. Journal of Pediatric Surgery, 55(8), 1639–1644. https://doi.org/10.1016/j.jpedsurg.2019.10.022
Ersoy Canillioglu, Y., & Erkanli Senturk, G. (2020). Alterations of IL-1 and VEGF After Ischemia-Reperfusion Injured Uterus and Ovary in Rats. Medeniyet medical journal, 35(2), 106–115. https://doi.org/10.5222/MMJ.2020.67026
Evora, P. R., Pearson, P. J., Seccombe, J. F., & Schaff, H. V. (1996). Lesão de isquemia-reperfusão. Aspectos fisiopatológicos e a importância da função endotelial. Arq. Bras. Cardiol, 239–245. https://pesquisa.bvsalud.org/portal/resource/pt/lil-319285
Galvão, T. (2015). Principais itens para relatar Revisões sistemáticas e Meta-análises: A recomendação PRISMA. Epidemiologia E Serviços de Saúde, 24(2), 335–342. https://doi.org/10.5123/s1679-49742015000200017
Geyikoglu, F., Koc, K., Erol, H. S., Colak, S., Ayer, H., Jama, S., Eser, G., Dortbudak, M. B., & Saglam, Y. S. (2019). The propolis and boric acid can be highly suitable, alone/or as a combinatory approach on ovary ischemia-reperfusion injury. Archives of gynecology and obstetrics, 300(5), 1405–1412. https://doi.org/10.1007/s00404-019-05303-9
Görkem, Ü., Togrul, C., Sahin, I., Coskun, B., Ozat, M., Güngör, T., & Deveci, E. (2017). Protective Effect of Caffeic Acid Phenethyl Ester (CAPE) on Ischemia-Reperfusion Injury in Rat Ovary. International Journal of Morphology, 35(1), 141–147. https://doi.org/10.4067/s0717-95022017000100023
Grotto, D., Valentini, J., Boeira, S., Paniz, C., Maria, L. S., Vicentini, J., Moro, A., Charão, M., Garcia, S. C., & Cardoso, S. G. (2008). Avaliação da estabilidade do marcador plasmático do estresse oxidativo: malondialdeído. Química Nova, 31(2), 275–279. https://doi.org/10.1590/s0100-40422008000200016
Güleç Başer, B., İslimye Taşkın, M., Adalı, E., Öztürk, E., Hısmıoğulları, A. A., & Yay, A. (2018). Does progesterone have protective effects on ovarian ischemia-reperfusion injury?. Journal of the Turkish German Gynecological Association, 19(2), 87–93. https://doi.org/10.4274/jtgga.2017.0047
Honardoust, P., Najafpour, A., & Mohammadi, R. (2021). Influence of Systemic Administration of Coq10 Nanoparticles on Ischemia-Reperfusion Injury on Ovaries in Rat. Evidence-based complementary and alternative medicine : eCAM, 2021, 2303417. https://doi.org/10.1155/2021/2303417
Hortu, I., Ilgen, O., Sahin, C., Akdemir, A., Yigitturk, G., & Erbas, O. (2020). Losartan ameliorates ovarian ischaemia/reperfusion injury in rats: an experimental study. Journal of Obstetrics and Gynaecology: The Journal of the Institute of Obstetrics and Gynaecology, 40(8), 1148–1154. https://doi.org/10.1080/01443615.2019.1701639
Hortu, I., Ozceltik, G., Sahin, C., Akman, L., Yildirim, N., & Erbas, O. (2019). Granulocyte Colony-Stimulating Factor Prevents Ischemia/Reperfusion-Induced Ovarian Injury in Rats: Evaluation of Histological and Biochemical Parameters. Reproductive sciences (Thousand Oaks, Calif.), 26(10), 1389–1394. https://doi.org/10.1177/1933719118816839
Ilgen, O., Hortu, I., Ozceltik, G., Yigitturk, G., Erbas, O., & Karadadas, N. (2020). Effects of Methylene Blue on Ovarian Torsion−Detorsion Injury in a Rat Model. Journal of Pediatric and Adolescent Gynecology, 33(5), 506–510. https://doi.org/10.1016/j.jpag.2020.06.010
Kalyoncu, S., Yilmaz, B., Demir, M., Tuncer, M., Bozdag, Z., Ince, O., Akif Bozdayi, M., Ulusal, H., & Taysi, S. (2020). Octreotide and lanreotide decrease ovarian ischemia-reperfusion injury in rats by improving oxidative and nitrosative stress. The journal of obstetrics and gynaecology research, 46(10), 2050–2058. https://doi.org/10.1111/jog.14379
Kalyoncu, Ş., Yilmaz, B., Demir, M., Tuncer, M., Bozdağ, Z., Ince, O., Bozdayi, M. A., Ulusal, H., & Taysi, S. (2020). Melatonin attenuates ovarian ischemia reperfusion injury in rats by decreasing oxidative stress index and peroxynitrite. Turkish journal of medical sciences, 50(6), 1513–1522. https://doi.org/10.3906/sag-2004-135
Kaplan, S., & Türk, A. (2021). Effects of vitamin B12 on rat ovary with ischemia-reperfusion injury. Biotechnic & Histochemistry, 97(4), 284–289. https://doi.org/10.1080/10520295.2021.1961863
Kaplan, S., & Türk, A. (2022). Effects of vitamin B12 on rat ovary with ischemia-reperfusion injury. Biotechnic & histochemistry : official publication of the Biological Stain Commission, 97(4), 284–289. https://doi.org/10.1080/10520295.2021.1961863
Karaçor, T., Dogan, Z., Elibol, E., Bulbul, M., & Nacar, M. C. (2020). Effects of iloprost on experimental ischemia and reperfusion injury in rat ovary. Biotechnic & histochemistry : official publication of the Biological Stain Commission, 95(5), 373–380. https://doi.org/10.1080/10520295.2019.1703219
Kirmizi, D. A., Baser, E., Okan, A., Kara, M., Yalvac, E. S., & Doganyigit, Z. (2021). The effect of a natural molecule in ovary ischemia reperfusion damage: does lycopene protect ovary?. Experimental animals, 70(1), 37–44. https://doi.org/10.1538/expanim.20-0080
Medeiros, F. da C., Silveira, M. H., & Gomes, M. S. (2018). Lesão por isquemia e reperfusão hepática: reação em cadeia causada pela ação de radicais livres durante procedimentos cirúrgicos. Anais Colóquio Estadual de Pesquisa Multidisciplinar & Congresso Nacional de Pesquisa Multidisciplinar. https://publicacoes.unifimes.edu.br/index.php/coloquio/article/view/489
Melekoglu, R., Ciftci, O., Eraslan, S., Alan, S., & Basak, N. (2018). The Protective Effects of Glycyrrhetinic Acid and Chrysin against Ischemia-Reperfusion Injury in Rat Ovaries. BioMed research international, 2018, 5421308. https://doi.org/10.1155/2018/5421308
Menezes Neto, B. F. D., Secanho, M. S., Fernandes, M. S., Carvalho, L. B., & Viterbo, F. (2022). Clamp vascular de fio de mononylon em microcirurgia experimental. Revista Brasileira de Cirurgia Plástica, 37, 60–65. https://doi.org/10.5935/2177-1235.2022RBCP0010
Najafpour, A., & Azizizadeh, H. (2018). Interaperitoneal Administration of Αlpha-Tocopherol Loaded Nanoparticles Improves Ischemia-Reperfusion Injury in Rat Ovaries Torsion and Detorsion Model. Bulletin of emergency and trauma, 6(3), 207–216. https://doi.org/10.29252/beat-060304
Nayki, C., Nayki, U., Keskin Cimen, F., Kulhan, M., Yapca, O. E., Kurt, N., & Bilgin Ozbek, A. (2018). The effect of rutin on ovarian ischemia-reperfusion injury in a rat model. Gynecological endocrinology: the official journal of the International Society of Gynecological Endocrinology, 34(9), 809–814. https://doi.org/10.1080/09513590.2018.1450378
Oktem, O., & Oktay, K. (2007). Quantitative assessment of the impact of chemotherapy on ovarian follicle reserve and stromal function. Cancer, 110(10), 2222–2229. https://doi.org/10.1002/cncr.23071
Onat, T., Demir Caltekin, M., Doğanyigit, Z., Turkler, C., Kaymak, E., Kara, M., & Serdar Yalvac, E. (2021). Activation of cannabinoid 2 receptors by JWH-133 protects against ovarian ischemia-reperfusion injury in rats. Biotechnic & histochemistry : official publication of the Biological Stain Commission, 96(5), 394–400. https://doi.org/10.1080/10520295.2021.1905183
Oyama, K., Nakamoto, K., Omori, M., Fukasawa, H., & Hirata, S. (2022). Prognostication of Ovarian Function after Ovarian Torsion Using Intraoperative Indocyanine Green Angiography. Journal of minimally invasive gynecology, 29(2), 237–242. https://doi.org/10.1016/j.jmig.2021.08.003
Ozekinci, M., Kucuksayan, E., Erdogan, G., Aslan, M., Pestereli, E., Canpolat, M., & Sircan-Kucuksayan, A. (2020). Histopathological and biochemical assessment of a novel diagnostic method for ovarian torsion. Biotechnic & histochemistry : official publication of the Biological Stain Commission, 95(3), 203–209. https://doi.org/10.1080/10520295.2019.1663558
Ozlem, K., Birkan, Y., Mustafa, K., & Emin, K. (2018). Protective effect of Vaccinium myrtillus on ischemia- reperfusion injury in rat ovary. Taiwanese journal of obstetrics & gynecology, 57(6), 836–841. https://doi.org/10.1016/j.tjog.2018.10.012
Pacheco, M., Borges De Menezes, L., & Gonçalves De Araújo, E. (2012). Fisiopatologia do estresse oxidativo após isquemia e reperfusão cerebral e potencial neuroproteção do pequi (caryocar brasiliense). http://www.conhecer.org.br/enciclop/2012b/ciencias%20da%20saude/Fisiopatologia.pdf
Parhizkar, P., Mohammadi, R., Shahrooz, R., & Mohammadi, V. (2019). Effects of Pyrroloquinoline Quinone (PQQ) on Ischemia-Reperfusion Injury in Rat Ovaries: Histological and Biochemical Assessments. Bulletin of emergency and trauma, 7(1), 35–40. https://doi.org/10.29252/beat-070105.
Pinheiro, B. do V., Holanda, M. A., Araújo, F. G., & Romaldini, H. (1999). Lesão pulmonar de reperfusão. Jornal de Pneumologia, 25, 124–136. https://doi.org/10.1590/S0102-35861999000200010
Pınar, N., Soylu Karapınar, O., Özcan, O., Atik Doğan, E., & Bayraktar, S. (2017). Protective effects of tempol in an experimental ovarian ischemia–reperfusion injury model in female Wistar albino rats. Canadian Journal of Physiology and Pharmacology, 95(7), 861–865. https://doi.org/10.1139/cjpp-2016-0309
Refaie, M., & El-Hussieny, M. (2018). Protective effect of pioglitazone on ovarian ischemia reperfusion injury of female rats via modulation of peroxisome proliferator activated receptor gamma and heme-oxygenase 1. International immunopharmacology, 62, 7–14. https://doi.org/10.1016/j.intimp.2018.06.037
Rodrigues, A. F., Oliveira, B. E. C., Santos, D. R., Júnior, E. F. da S., Guimaraes, F. F., Muniz, H. G., Andrade, L. V. de, & Geber, S. (2010). Torção ovariana. Www.rmmg.org, 20(2), 78–81. http://www.rmmg.org/artigo/detalhes/1058
Sipahi, M., Gunaydin, M., Kesicioglu, T., Usta, M., Yavuz, B. T., & Tomruk, C. (2019). A new approach to prevent ischemia/reperfusion injury in a rat model: remote ischemic conditioning. Archives of gynecology and obstetrics, 299(6), 1691–1699. https://doi.org/10.1007/s00404-019-05149-1
Soyman, Z., Kelekçi, S., Sal, V., Şevket, O., Bayındır, N., & Uzun, H. (2017). Effects of Apigenin on Experimental Ischemia/Reperfusion Injury in the Rat Ovary. Balkan medical journal, 34(5), 444–449. https://doi.org/10.4274/balkanmedj.2016.1386
Topcu, A., Balik, G., Atak, M., Mercantepe, T., Uydu, H. A., & Tumkaya, L. (2019). An investigation of the effects of metformin on ovarian ischemia-reperfusion injury in rats. European journal of pharmacology, 865, 172790. https://doi.org/10.1016/j.ejphar.2019.172790
Turkler, C., Kulhan, N. G., Ata, N., Kiremitli, T., Cimen, F. K., & Suleyman, H. (2018). The ameliorative effect of lutein on ovarian ischemia-reperfusion injury in rats. Bratislavske lekarske listy, 119(11), 713–717. https://doi.org/10.4149/BLL_2018_127
Yayla, M., Cetin, D., Adali, Y., Kilicle, P. A., & Toktay, E. (2018). Potential therapeutic effect of pomegranate seed oil on ovarian ischemia/reperfusion injury in rats. Iranian journal of basic medical sciences, 21(12), 1262–1268. https://doi.org/10.22038/ijbms.2018.30149.7268
Yildirim, N., Simsek, D., Kose, S., Yildirim, A., Guven, C., Yigitturk, G., & Erbas, O. (2018). The protective effect of Gingko biloba in a rat model of ovarian ischemia/reperfusion injury: Improvement in histological and biochemical parameters. Advances in clinical and experimental medicine : official organ Wroclaw Medical University, 27(5), 591–597. https://doi.org/10.17219/acem/68896
Yilmaz, E., Un, H., Gundogdu, B., Polat, E., Askin, S., Topdagi, Y. E., & Halici, Z. (2020). Protective Effect of Lycopene against Reperfusion Injury in Rats with Ovarian Torsion: A Biochemical and Histopathological Evaluation. Journal of laboratory physicians, 12(1), 32–37. https://doi.org/10.1055/s-0040-1715553
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Valentina Silva Rodrigues; Rebeca de Souza da Nóbrega; Lucas Dias Silva; Gabriel Rezende Neves; Francinei Gomes Pinto; Tiago Monteiro Batista; Isabela Ferreira de Freitas; Luiz Felipe Leão Lima
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
