Academic Journal
Comparative Effects of Laparotomy and Laparoscopy-Assisted Embryo Transfer on Oxidative Stress and Thiol-Disulphide Homeostasis in Tuj Ewes.
| Title: | Comparative Effects of Laparotomy and Laparoscopy-Assisted Embryo Transfer on Oxidative Stress and Thiol-Disulphide Homeostasis in Tuj Ewes. |
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| Authors: | Demir MC; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Demir MS; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Makav M; Department of Physiology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Kaya S; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Gökdemir T; Department of Reproduction and Artificial Insemination, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Önder NT; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Kuru M; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye., Kaçar C; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, Kars, Türkiye. |
| Source: | Veterinary medicine and science [Vet Med Sci] 2026 Jul; Vol. 12 (4), pp. e71023. |
| Publication Type: | Journal Article; Comparative Study |
| Language: | English |
| Journal Info: | Publisher: John Wiley & Sons Ltd Country of Publication: England NLM ID: 101678837 Publication Model: Print Cited Medium: Internet ISSN: 2053-1095 (Electronic) Linking ISSN: 20531095 NLM ISO Abbreviation: Vet Med Sci Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: [Oxford] : John Wiley & Sons Ltd., [2015]- |
| MeSH Terms: | Laparoscopy*/veterinary , Disulfides*/blood , Disulfides*/metabolism , Sulfhydryl Compounds*/blood , Sulfhydryl Compounds*/metabolism , Embryo Transfer*/veterinary , Embryo Transfer*/methods , Laparotomy*/veterinary , Oxidative Stress*, Sheep/physiology ; Glutathione/blood ; Animals ; Female ; Homeostasis |
| Abstract: | Objectives: In this study, it was aimed to compare the effects of embryo transfer performed via laparotomy and laparoscopy on thiol-disulphide homeostasis and some oxidative stress markers in Tuj ewes. Methods: In the study, 10 Tuj ewes were randomly divided into two groups (laparotomy, n = 5; laparoscopy, n = 5). A progesterone-based synchronization protocol was applied to all animals. Blood samples were collected immediately before surgery, immediately after surgery, and at 24 and 48 h postoperatively. Serum levels of glutathione (GSH), malondialdehyde (MDA), total thiol (TT), native thiol (NT), disulphide (Ds) and thiol-disulphide ratios were determined. Results: Group, time, and group × time interactions were found to be statistically significant for GSH, MDA, TT, and NT parameters (p < 0.05). In the laparotomy group, GSH, TT, and NT levels markedly decreased during the postoperative period (p < 0.05), whereas MDA levels showed a significant increase, particularly at 48 h (p < 0.05). In the laparoscopy group, changes in oxidative stress markers were found to be more limited. Although no significant differences were observed between the groups in terms of disulphide levels and thiol-disulphide ratios (p > 0.05), time-dependent changes in these parameters were statistically significant (p < 0.05). In the laparotomy group, significant negative correlations were detected between MDA and antioxidant parameters (p < 0.05), while strong positive correlations were observed among thiol parameters (p < 0.01). Conclusions: As a result, it was concluded that the surgical approach used in embryo transfer affects the systemic oxidative stress response and that thiol-disulphide homeostasis can be considered a sensitive biomarker for revealing these differences. It was determined that the laparoscopic embryo transfer method disrupts redox balance to a lesser extent and better preserves the antioxidant defence system compared with laparotomy. (© 2026 The Author(s). Veterinary Medicine and Science published by John Wiley & Sons Ltd.) |
| References: | Agarwal, A., S. Gupta, and R. K. Sharma. 2005. “Role of Oxidative Stress in Female Reproduction.” Reproductive Biology and Endocrinology 3, no. 1: 28. https://doi.org/10.1186/1477‐7827‐3‐28. Amiridis, G. S., and S. Cseh. 2012. “Assisted Reproductive Technologies in the Reproductive Management of Small Ruminants.” Animal Reproduction Science 130, no. 3–4: 152–161. https://doi.org/10.1016/j.anireprosci.2012.01.009. Biswas, S., A. S. Chida, and I. Rahman. 2006. “Redox Modifications of Protein–thiols: Emerging Roles in Cell Signaling.” Biochemical Pharmacology 71, no. 5: 551–564. https://doi.org/10.1016/j.bcp.2005.10.044. Boğa Kuru, B., and M. Makav. 2024. “Impact of Continuous Light Stress on Growth Performance, Organ Weight, Serum Melatonin Concentration, and Thiol‐disulfide Homeostasis in Rats.” ScienceAsia 50, no. 6: 1. https://doi.org/10.2306/scienceasia1513‐1874.2024.113. Calvin, H. I., K. Grosshans, and E. J. Blake. 1986. “Estimation and Manipulation of Glutathione Levels in Prepuberal Mouse Ovaries and Ova:Relevance to Sperm Nucleus Transformation in the Fertilized Egg.” Gamete Research 14, no. 3: 265–275. https://doi.org/10.1002/mrd.1120140310. Circu, M. L., and T. Y. Aw. 2010. “Reactive Oxygen Species, Cellular Redox Systems, and Apoptosis.” Free Radical Biology and Medicine 48, no. 6: 749–762. https://doi.org/10.1016/j.freeradbiomed.2009.12.022. Cordeiro, M. F., J. B. Lima‐Verde, E. S. Lopes‐Júnior, et al. 2003. “Embryo Recovery Rate in Santa Inês Ewes Subjected to Successive Superovulatory Treatments With pFSH.” Small Ruminant Research 49, no. 1: 19–23. https://doi.org/10.1016/S0921‐4488(03)00059‐2. Csapo, A. I., M. O. Pulkkinen, B. Ruttner, J. P. Sauvage, and W. G. Wiest. 1972. “The Significance of the human Corpus Luteum in Pregnancy Maintenance.” American Journal of Obstetrics and Gynecology 112, no. 8: 1061–1067. https://doi.org/10.1016/0002‐9378(72)90181‐0. de Matos, D. G., and C. C. Furnus. 2000. “The Importance of Having High Glutathione (GSH) Level After Bovine in Vitro Maturation on Embryo Development: Effect of β‐mercaptoethanol, Cysteine and Cystine.” Theriogenology 53, no. 3: 761–771. https://doi.org/10.1016/S0093‐691X(99)00278‐2. Demir, M. C., C. Kaçar, Y. Öztürkler, et al. 2025. “Comparison of Laparoscopic and Laparotomic Methods in Embryo Transfer in Tuj ewes.” Journal of Advances in VetBio Science and Techniques 10, no. 2: 115–121. https://doi.org/10.31797/vetbio.1686254. Demir, M. C., M. Kuru, M. Makav, M. S. Demir, and S. Kaya. 2026. “Alterations in Thiol–Disulfide Homeostasis and Oxidative Stress Markers in Cows With Clinical and Subclinical Mastitis.” Turkish Journal of Veterinary Research 10, no. 1: 93–100. https://doi.org/10.47748/tjvr.1866616. El Mouatassim, S. 1999. “Expression of Genes Encoding Antioxidant Enzymes in human and Mouse Oocytes During the Final Stages of Maturation.” Molecular Human Reproduction 5, no. 8: 720–725. https://doi.org/10.1093/molehr/5.8.720. Erel, O., and S. Neselioglu. 2014. “A Novel and Automated Assay for Thiol/Disulphide Homeostasis.” Clinical Biochemistry 47, no. 18: 326–332. https://doi.org/10.1016/j.clinbiochem.2014.09.026. Ernest, B., O. Duron, and B. M. Kelly. 1963. “Improved Method for Determination of Blood Glutathione.” Journal Of Laboratory and Clinical Medicine 61, no. 1: 882–888. https://sid.ir/paper/547908/en. Falchi, L., S. Ledda, and M. T. Zedda. 2022. “Embryo Biotechnologies in Sheep: Achievements and New Improvements.” Reproduction in Domestic Animals 57, no. S5: 22–33. https://doi.org/10.1111/rda.14127. Garrel, C., P. A. Fowler, and K. H. Al‐Gubory. 2010. “Developmental Changes in Antioxidant Enzymatic Defences Against Oxidative Stress in Sheep Placentomes.” Journal of Endocrinology 205, no. 1: 107–116. https://doi.org/10.1677/JOE‐09‐0362. Guerin, P., S. E. Mouatassim, and Y. Menezo. 2001. “Oxidative Stress and Protection Against Reactive Oxygen Species in the Pre‐implantation Embryo and Its Surroundings.” Human Reproduction Update 7, no. 2: 175–189. Halliwell, B. 1994. “Free Radicals, Antioxidants, and human Disease: Curiosity, Cause, or Consequence?,” Lancet 344, no. 8924: 721–724. https://elibrary.ru/item.asp?id=2116055. Jozwik, M. 1999. “Oxidative Stress Markers in Preovulatory Follicular Fluid in Humans.” Molecular Human Reproduction 5, no. 5: 409–413. https://doi.org/10.1093/molehr/5.5.409. Kershaw, C. M., M. Khalid, M. R. McGowan, et al. 2005. “The Anatomy of the Sheep Cervix and Its Influence on the Transcervical Passage of an Inseminating Pipette Into the Uterine Lumen.” Theriogenology 64, no. 5: 1225–1235. https://doi.org/10.1016/j.theriogenology.2005.02.017. Kohen, R., and A. Nyska. 2002. “Invited Review: Oxidation of Biological Systems: Oxidative Stress Phenomena, Antioxidants, Redox Reactions, and Methods for Their Quantification.” Toxicologic Pathology 30, no. 6: 620–650. https://doi.org/10.1080/01926230290166724. Kundi, H., I. Ates, E. Kiziltunc, et al. 2015. “A Novel Oxidative Stress Marker in Acute Myocardial Infarction; Thiol/Disulphide Homeostasis.” The American Journal of Emergency Medicine 33, no. 11: 1567–1571. https://doi.org/10.1016/j.ajem.2015.06.016. Miyamura, M. 1995. “Glutathione Concentration During Maturation and Fertilization in Bovine Oocytes.” Theriogenology 43: 282–286. https://cir.nii.ac.jp/crid/1570291226299354880. Myatt, L. 2006. “Placental Adaptive Responses and Fetal Programming.” Journal of Physiology 572, no. 1: 25–30. https://doi.org/10.1113/jphysiol.2006.104968. Myatt, L., and X. Cui. 2004. “Oxidative Stress in the Placenta.” Histochemistry and Cell Biology 122, no. 4: 369–382. https://doi.org/10.1007/s00418‐004‐0677‐x. Nielsen, F., B. B. Mikkelsen, J. B. Nielsen, H. R. Andersen, and P. Grandjean. 1997. “Plasma Malondialdehyde as Biomarker for Oxidative Stress: Reference Interval and Effects of Life‐style Factors.” Clinical Chemistry 43, no. 7: 1209–1214. https://doi.org/10.1093/clinchem/43.7.1209. Ni̇sbet, C., S. Çenesi̇z, M. Açici, and Ş. Umur. 2008. “Kistik Ekinokokkozisli Sığırlarda Serum Malondialdehit, Seruloplazmin ve Adenozin Deaminaz Düzeylerinin Belirlenmesi.” Journal of the Faculty of Veterinary Medicine Erciyes University 5, no. 1: 1–5. https://dergipark.org.tr/en/pub/ercivet/article/77410. Perreault, S. D., R. R. Barbee, and V. L. Slott. 1988. “Importance of Glutathione in the Acquisition and Maintenance of Sperm Nuclear Decondensing Activity in Maturing Hamster Oocytes.” Developmental Biology 125, no. 1: 181–186. https://doi.org/10.1016/0012‐1606(88)90070‐X. Rizzo, A., M. Mutinati, M. Spedicato, et al. 2008. “First Demonstration of an Increased Serum Level of Reactive Oxygen Species during the Peripartal Period in the Ewes.” Immunopharmacology and Immunotoxicology 30, no. 4: 741–746. https://doi.org/10.1080/08923970802279050. Suzuki, T., N. Sugino, T. Fukaya, et al. 1999. “Superoxide Dismutase in Normal Cycling human Ovaries: Immunohistochemical Localization and Characterization.” Fertility and Sterility 72, no. 4: 720–726. https://doi.org/10.1016/S0015‐0282(99)00332‐5. Uttara, B., A. Singh, P. Zamboni, and R. Mahajan. 2009. “Oxidative Stress and Neurodegenerative Diseases: a Review of Upstream and Downstream Antioxidant Therapeutic Options.” Current Neuropharmacology 7, no. 1: 65–74. https://doi.org/10.2174/157015909787602823. Winterbourn, C. C., and M. B. Hampton. 2008. “Thiol Chemistry and Specificity in Redox Signaling.” Free Radical Biology & Medicine 45, no. 5: 549–561. https://doi.org/10.1016/j.freeradbiomed.2008.05.004. Yoshida, M., K. Ishigaki, and V. G. Pursel. 1992. “Effect of Maturation media on Male Pronucleus Formation in Pig Oocytes Matured in Vitro.” Molecular Reproduction and Development 31, no. 1: 68–71. https://doi.org/10.1002/mrd.1080310112. Yoshioka, T., K. Kawada, T. Shimada, and M. Mori. 1979. “Lipid Peroxidation in Maternal and Cord Blood and Protective Mechanism Against Activated‐oxygen Toxicity in the Blood.” American Journal of Obstetrics and Gynecology 135, no. 3: 372–376. https://doi.org/10.1016/0002‐9378(79)90708‐7. |
| Contributed Indexing: | Keywords: embryo transfer; laparoscopy; laparotomy; oxidative stress; sheep; thiol–disulphide homeostasis |
| Substance Nomenclature: | 0 (Disulfides) 0 (Sulfhydryl Compounds) GAN16C9B8O (Glutathione) |
| Entry Date(s): | Date Created: 20260612 Date Completed: 20260612 Latest Revision: 20260726 |
| Update Code: | 20260726 |
| PubMed Central ID: | PMC13261301 |
| DOI: | 10.1002/vms3.71023 |
| PMID: | 42281509 |
| Database: | MEDLINE |
| ISSN: | 2053-1095 |
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| DOI: | 10.1002/vms3.71023 |