Changes in Malondialdehyde, Reduced Glutathione, and Thiol–Disulfide Homeostasis in Cattle with Traumatic Pericarditis

Öz

Traumatic pericarditis most commonly develops during the course of traumatic reticuloperitonitis and is associated with an increased oxidative burden; however, the diagnostic contribution of oxidative biomarkers remains unclear. In this study, the oxidative stress profile and dynamic thiol–disulfide homeostasis were evaluated in cattle with traumatic pericarditis. Comparisons between the pericarditis and control groups were performed within the same sex, and sex-related differences were additionally investigated within the pericarditis subgroup. A total of 100 cattle were included in the pericarditis and control group comparisons. Serum malondialdehyde (MDA), reduced glutathione (GSH), total and native thiol (TT, NT), and disulfide (Ds) levels were measured spectrophotometrically, and Ds/TT, Ds/NT, and NT/TT ratios were calculated. Within the same sex, MDA levels were higher in the pericarditis group than in controls in both females (P<0.01) and males (P<0.05). GSH levels were lower in males with pericarditis (P<0.001), whereas no significant difference was detected in females (P>0.05). TT and NT decreased in the pericarditis group in both sexes (females: TT P<0.01, NT P<0.05; males: both P<0.0001). No significant change in Ds was observed in within-sex comparisons between pericarditis and control groups; however, in the sex comparison within the pericarditis subgroup, Ds levels were higher in females (P<0.01). In the traumatic pericarditis group, ratio biomarkers differed significantly between sexes: Ds/TT and Ds/NT were higher in females than in males, whereas the NT/TT ratio was higher in males (P<0.01). These findings suggest that pericarditis is accompanied by increased lipid peroxidation and a reduction in the antioxidant/thiol pool, and that impairment in thiol–disulfide balance exhibits a sex-specific pattern. The evaluated panels may provide complementary value to clinical assessment; however, prospective, multicenter validation and determination of threshold values are required for clinical implementation.

Anahtar Kelimeler

• Cattle
• malondialdehyde
• ; oxidative stress
• reduced glutathione
• thiol–disulfide homeostasis
• traumatic pericarditis

Travmatik Perikarditisli Sığırlarda Malondialdehit, Redükte Glutatyon ve Tiyol-Disülfid Homeostazının Değişimleri

Öz

Travmatik perikarditis, çoğunlukla retikuloperitonitis travmatikayı izleyen süreçte gelişir ve artmış oksidatif yükle ilişkilidir; ancak tanıda oksidatif biyobelirteçlerin katkısı net değildir. Bu çalışmada, travmatik perikarditisli sığırlarda oksidatif stres profili ile dinamik tiyol–disülfid dengesi değerlendirilmiştir. Aynı cinsiyet içinde perikarditis ve kontrol grubu karşılaştırmaları yapılmış ve perikarditis alt grubunda dişi-erkek farkları ayrıca incelenmiştir. Perikarditis ve kontrol grupları karşılaştırmalarında toplam 100 sığır incelenmiştir. Serum malondialdehit (MDA), redükte glutatyon (GSH), toplam ve natif tiyol (TT, NT) ile disülfid (Ds) spektrofotometrik olarak ölçülmüş; Ds/TT, Ds/NT ve NT/TT oranları hesaplanmıştır. Aynı cinsiyet içinde, perikarditis varlığında MDA düzeyleri kontrol grubuna kıyasla her iki cinsiyette yüksek bulunmuştur (dişi P<0,01; erkek P<0,05). GSH düzeyleri perikarditisli erkeklerde düşük bulunmuştur (P<0,001), dişilerde ise anlamlı farklılık saptanmamıştır (P>0,05). TT ve NT her iki cinsiyette de perikarditisli grupta azalmıştır (dişide TT için P<0,01, NT için P<0,05; erkekte her ikisi için P<0,0001). Cinsiyet içi perikarditis ve kontrol grubu karşılaştırmalarında Ds’de anlamlı değişim saptanmamış; buna karşılık perikarditis alt grubunda dişi–erkek karşılaştırmasında Ds düzeyi dişilerde daha yüksek bulunmuştur (P<0,01). Perikarditis (TP) grubunda, cinsiyetler arası karşılaştırmada oran belirteçleri istatistiksel olarak anlamlı farklılık göstermiştir: Ds/TT ve Ds/NT değerleri dişilerde erkeklere kıyasla daha yüksek, NT/TT oranı ise erkeklerde daha yüksek bulunmuştur (P<0,01). Bulgular, perikarditisin artmış lipid peroksidasyonu ve antioksidan/tiyol havuzunda daralma ile seyrettiğini ve tiyol-disülfid dengesindeki bozulmanın cinsiyete özgü bir patern sergilediğini düşündürmektedir. Değerlendirilen paneller klinik değerlendirmeye tamamlayıcı katkı sağlayabilir; ancak klinik kullanım için prospektif, çok merkezli doğrulama ve eşik değerlerinin belirlenmesi gereklidir.

Anahtar Kelimeler

• Sığır
• malondialdehit
• oksidatif stres
• redükte glutatyon
• tiyol–disülfid homeostazı
• travmatik perikarditis

Kaynakça

1. Abu-Seida, A. M., & Al-Abbadi, O. S. (2016). Recent advances in the management of foreign body syndrome in cattle and buffaloes: A review. Pakistan Veterinary Journal, 36(4), 385–393.
2. Akyüz, E., & Aydın, U. (2022). Prognostic value of haptoglobin and ceruloplasmin levels determined in cows with adhesive and nonadhesive traumatic reticuloperitonitis. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 28(3), 337–344. https://doi.org/10.9775/kvfd.2021.27040
3. Aref, N.-E. M., & Abdel-Hakiem, M. A. H. (2013). Clinical and diagnostic methods for evaluation of sharp foreign body syndrome in buffaloes. Veterinary World, 6(9), 586–591. https://doi.org/10.5455/vetworld.2013.586-591
4. Balkan, B. M., Meral, O., Cetintav, B., Ozkurt, G., Balkan, A. B., & Sel, T. (2024). Evaluation of thiol/disulphide and oxidant–antioxidant status of dairy cows in periparturient and post-partum period. Veterinary Medicine and Science, 10(6), e70023. https://doi.org/10.1002/vms3.70023
5. Beutler, E., Duron, O., & Kelly, B. M. (1963). Improved method for the determination of blood glutathione. The Journal of Laboratory and Clinical Medicine, 61, 882–888.
6. Bishnoi, A. K., & Gahlot, T. K. (2011). Diagnostic studies on traumatic pericarditis in cattle. Veterinary Practitioner, 12(2), 184–186.
7. Bölükbaşı, L., & Merhan, O. (2024). Lipid peroxidation and thiol/disulfide homeostasis in cattle with trichophytosis. Dicle University Journal of Faculty of Veterinary Medicine, 17(2), 161–164. https://doi.org/10.47027/duvetfd.1534484
8. Bozukluhan, K., Merhan, O., Kiziltepe, S., Egritag, H. E., Akyuz, E., & Gokce, H. I. (2021). Determination of haptoglobin, some biochemical and oxidative stress parameters in calves with pneumonia. Fresenius Environmental Bulletin, 30(7), 9492–9496.

9. Braun, U. (2009). Traumatic pericarditis in cattle: Clinical, radiographic and ultrasonographic findings. The Veterinary Journal, 182(2), 176–186. https://doi.org/10.1016/j.tvjl.2008.06.021
10. Brunelli, E., Domanico, F., La Russa, D., & Pellegrino, D. (2014). Sex differences in oxidative stress biomarkers.
11. Current Drug Targets, 15(8), 811–815. https://doi.org/10.2174/1389450115666140624112317
12. Celi, P. (2011). Biomarkers of oxidative stress in ruminant medicine. Immunopharmacology and Immunotoxicology, 33(2), 233–240. https://doi.org/10.3109/08923973.2010.514917
13. Cremers, C. M., & Jakob, U. (2013). Oxidant sensing by reversible disulfide bond formation. The Journal of Biological Chemistry, 288(37), 26489–26496. https://doi.org/10.1074/jbc.R113.462929
14. Deveci, M. Z. Y., & Erdal, H. (2022). Determination of dynamic thiol-disulfide levels in dairy cattle with foot disease. Veterinarski Arhiv, 92(6), 657–666. https://doi.org/10.24099/vet.arhiv.1785
15. Doğan, M., & Bozukluhan, K. (2024). Determination of oxidative stress and sialic acid levels in cattle infected with hydatid cyst. Dicle University Journal of Faculty of Veterinary Medicine, 17(2), 173–177. https://doi.org/10.47027/duvetfd.1537837
16. Ercan, N., & Fidancı, U. R. (2012). Oksidatif DNA hasar ürünleri ve hastalıklar. Dicle University Journal of Faculty of Veterinary Medicine, 2(2), 40–57.
17. Erel, O., & Erdogan, S. (2020). Thiol-disulfide homeostasis: An integrated approach with biochemical and clinical aspects. Turkish Journal of Medical Sciences, 50(SI-2), 1728–1738. https://doi.org/10.3906/sag-2003-64
18. Erel, O., & Neselioglu, S. (2014). A novel and automated assay for thiol/disulphide homeostasis. Clinical Biochemistry, 47(18), 326–332. https://doi.org/10.1016/j.clinbiochem.2014.09.026
19. Ertaş, F., Kızıltepe, Ş., & Merhan, O. (2023). Investigation of dynamic thiol disulfide homeostasis in young cattle with pneumonia. MAS Journal of Applied Sciences, 8(Özel Sayı), 949–954. https://doi.org/10.5281/zenodo.10003819
20. Gomaa, N., Nassif, N. M., Havez, M. A., & Fawzy, S. (2023). A comparative study on oxidative stress indices among cattle and buffalo with foreign body syndrome. Journal of the Hellenic Veterinary Medical Society, 74(3), 5903–5910. https://doi.org/10.12681/jhvms.28170
21. Gül, Y. (2017). Retikuloperitonitis travmatikanın tanı-ayırıcı tanı ve tedavisindeki son gelişmeler. Fırat University Veterinary Journal of Health Sciences, 31(1), 59–66.
22. Gutteridge, J. M. (1995). Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clinical Chemistry, 41(12), 1819–1828. https://doi.org/10.1093/clinchem/41.12.1819
23. Jafarzadeh, S. R., Nowrouzian, I., Khaki, Z., Ghamsari, S. M., & Adibhashemi, F. (2004). The sensitivities and specificities of total plasma protein and plasma fibrinogen for the diagnosis of traumatic reticuloperitonitis in cattle. Preventive Veterinary Medicine, 65(1–2), 1–7. https://doi.org/10.1016/j.prevetmed.2004.07.004
24. Jones, D. P. (2006). Redefining oxidative stress. Antioxidants & Redox Signaling, 8(9–10), 1865–1879. https://doi.org/10.1089/ars.2006.8.1865
25. Kırbaş, A., Kaman, R., Merhan, O., Bozukluhan, K., Değirmençay, Ş., & Eroğlu, M. S. (2021). Evaluation of acute phase response and oxidative damage in sheep naturally infected with Streptococcus pluranimalium using haptoglobin, nitric oxide, and malondialdehyde levels. Fırat University Veterinary Journal of Health Sciences, 35(3), 145–150.
26. Merhan, O., Başer, L., Bozukluhan, K., Kükürt, A., Lehimcioğlu, N. C., Atakişi, E., & Çelik, Ö. (2025). Determination of dynamic thiol disulfide homeostasis in cows with dystocia. Animal Health Production and Hygiene, 14(2), 40–45. https://doi.org/10.53913/aduveterinary.1790327
27. Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P., & Malik, A. B. (2014). Reactive oxygen species in inflammation and tissue injury. Antioxidants & Redox Signaling, 20(7), 1126–1167. https://doi.org/10.1089/ars.2012.5149
28. Radostits, O. M., Gay, C. C., Hinchcliff, K. W., & Constable, P. D. (Eds.). (2007). Veterinary medicine: A textbook of the diseases of cattle, horses, sheep, pigs and goats (10th ed.). Elsevier Saunders.
29. Rubio, C. P., Escribano, D., Mainau, E., Cerón, J. J., Navarro, E., & Manteca, X. (2021). Changes in salivary biomarkers of oxidative status in calves at weaning and grouping. BMC Veterinary Research, 17, 373. https://doi.org/10.1186/s12917-021-03087-2
30. Sezer, M., Akyüz, E., Aydın, U., Merhan, O., Batı, Y. U., Gezer, T., Gökçe, G., & Bozukluhan, K. (2024a). Evaluation of serum iron, total iron binding capacity, transferrin saturation, haptoglobin and ceruloplasmin levels in cows with reticuloperitonitis traumatica (RPT) and pericarditis traumatica (PT). Dicle University Journal of Faculty of Veterinary Medicine, 17(2), 124–129. https://doi.org/10.47027/duvetfd.1381264
31. Sezer, M., Gezer, T., Merhan, O., Akyüz, E., Bozukluhan, K., & Gökce, G. (2024b). Evaluation of iron, iron binding capacity, transferrin, some oxidative stress markers and hematological parameters in foot and mouth disease in cattle. Mediterranean Veterinary Journal, 9(1), 224–229. https://doi.org/10.24880/meditvetj.1517834
32. Sies, H. (2020). Oxidative stress: Concept and some practical aspects. Antioxidants, 9(9), 852. https://doi.org/10.3390/antiox9090852
33. Taverna, M., Marie, A.-L., Mira, J.-P., & Guidet, B. (2013). Specific antioxidant properties of human serum albumin. Annals of Intensive Care, 3(1), 4. https://doi.org/10.1186/2110-5820-3-4
34. Tesena, P., Vinijkumthorn, R., Preuksathaporn, T., Piyakul, P., Chotikaprakal, T., Sirireugwipas, R., Wong-Aree, K., & Prapaiwan, N. (2024). Evaluation of gastrointestinal tract lesions and serum malondialdehyde levels after repeated oral administration of phenylbutazone in horses. Veterinary Research Communications, 48(4), 2343–2355. https://doi.org/10.1007/s11259-024-10415-y
35. Tiberi, J., Cesarini, V., Stefanelli, R., Canterini, S., Fiorenza, M. T., & La Rosa, P. (2023). Sex differences in antioxidant defence and the regulation of redox homeostasis in physiology and pathology. Mechanisms of Ageing and Development, 211, 111802. https://doi.org/10.1016/j.mad.2023.111802
36. Turgut, K. (2000). Dysproteinemias and tests. In K. Turgut (Ed.), Veterinary clinical laboratory diagnosis (2nd ed., pp. 505–506). Bahçıvanlar Press Industry.
37. Uzun, N. (2019). The analysis of glutathione level and superoxide dismutase activity in normal and preeclampsia pregnant. Eastern Anatolian Journal of Science, 5(1), 23–29.
38. Yıldırım, M. (2006). İskenderun mezbahanesine getirilen sığırlarda rumen ve retikulum lezyonlarının araştırılması [Master’s thesis, Mustafa Kemal Üniversitesi Sağlık Bilimleri Enstitüsü].
39. Yoshioka, T., Kawada, K., Shimada, T., & Mori, M. (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(3), 372–376. https://doi.org/10.1016/0002-9378(79)90708-7