Impact of Antioxidant–Oxidant Status at Mating on Reproductive Performance of Gray Shirazi Ewes

Document Type : Original Article

Authors

1 Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

3 Animal Science Research Department, Fars Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization (AREEO), Shiraz, Iran

Abstract

This study aimed to evaluate changes in oxidant–antioxidant status at mating, mid-pregnancy, and early lactation in Gray Shirazi ewes and to investigate their associations with pregnancy outcome categories, lamb birth weight, parity, and body condition score (BCS). Sixty healthy primiparous and multiparous Gray Shirazi ewes were randomly selected and monitored from mating to early lactation (September 2021–April 2022). Blood samples were collected at mating, mid-pregnancy, and early lactation. Serum concentrations of superoxide dismutase (SOD), glutathione peroxidase (GPX), nitric oxide (NO), total antioxidant capacity (TAC), and malondialdehyde (MDA) were measured using commercial kits. Data were analyzed using repeated-measures and one-way ANOVA followed by LSD post-hoc tests, as well as Pearson correlation analysis (P < 0.05). SOD activity was significantly higher during early lactation than at the other stages (P < 0.05), whereas GPX activity was lowest during pregnancy. TAC levels were significantly lower in early lactation than at the other sampling stages. MDA concentrations were highest at mating (P < 0.05), while NO levels did not differ among stages. At mating, non-pregnant ewes showed significantly higher MDA and NO levels than ewes that later produced single or twin lambs. No significant correlations were observed between oxidative markers and lamb birth weight. However, MDA levels were negatively correlated with BCS during pregnancy (r = −0.301, P < 0.05). Oxidant–antioxidant status in Gray Shirazi ewes varies across reproductive stages, reflecting physiological and metabolic adaptations. Certain oxidative markers, particularly MDA, TAC, and NO, showed associations with pregnancy outcomes. Monitoring oxidative status at different reproductive stages may contribute to improved management of oxidative stress and reproductive performance in ewes.

Keywords

Main Subjects


  1. Lykkesfeldt J, Svendsen O. Oxidants and antioxidants in disease: oxidative stress in farm animals. The veterinary journal. 2007;173(3):502-11. https://doi.org/10.1016/j.tvjl.2006.06.005
  2. Bernabucci U, Ronchi B, Lacetera N, Nardone A. Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of dairy science. 2002;85(9):2173-9. https://doi.org/10.3168/jds.s0022-0302(02)74296-3 
  3. Kamiloğlu NN, Beytut E, Güven A, Altinsaat Ç. Changes in the erythrocyte anti-oxidant system of offspring of dams treated with Vitamin A and β-carotene during gestation. Small Ruminant Research. 2006;65(1-2):142-8. https://doi.org/10.1016/j.smallrumres.2005.06.001 
  4. Mohebbi-Fani M, Mirzaei A, Nazifi S, Tabandeh M. Oxidative status and antioxidant enzyme activities in erythrocytes from breeding and pregnant ewes grazing natural pastures in dry season. Revue de Médecine Vétérinaire. 2012;163(10):454-60.
  5. Seguí J, Gironella M, Sans M, Granell S, Gil F, Gimeno M, et al. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. Journal of leukocyte biology. 2004;76(3):537-44. https://doi.org/10.1189/jlb.0304196 
  6. Celi P. The role of oxidative stress in small ruminants' health and production. Revista Brasileira de Zootecnia. 2010;39:348-63.
  7. Vipond J, Morgan C, McEvoy T, editors. Year round feeding the ewe for lifetime production2010: SAC.
  8. Akhtar M, Javed K, Abdullah M, Ahmad N, Elzo M. Environmental factors affecting preweaning growth traits of Buchi sheep in Pakistan. J Anim Plant Sci. 2012;22(3):529-36.
  9. Gaskins C, Snowder G, Westman M, Evans M. Influence of body weight, age, and weight gain on fertility and prolificacy in four breeds of ewe lambs. Journal of animal science. 2005;83(7):1680-9. https://doi.org/10.2527/2005.8371680x 
  10. Brookes PS. 32 Mitochondrial proton leak and superoxide generation: an hypothesis. Portland Press Ltd.; 1998. https://doi.org/10.1042/bst026s331 
  11. Grisham MB. Reactive metabolites of oxygen and nitrogen in biology and medicine. 1992.
  12. Russel A, Doney J, Gunn R. Subjective assessment of body fat in live sheep. The Journal of Agricultural Science. 1969;72(3):451-4. https://doi.org/10.1017/S0021859600024874 
  13. Chavatte-Palmer P, Al Gubory K, Picone O, Heyman Y. Nutrition maternelle: incidence sur la fertilité de la descendance et importance de la période périconceptionelle pour le long terme. Gynécologie obstétrique & fertilité. 2008;36(9):920-9. https://doi.org/10.1016/j.gyobfe.2008.06.020 
  14. Gür S, Türk G, Demirci E, Yüce A, Sönmez M, Özer Ş, et al. Effect of pregnancy and foetal number on diameter of corpus luteum, maternal progesterone concentration and oxidant/antioxidant balance in ewes. Reproduction in domestic animals. 2011;46(2):289-95. https://doi.org/10.1111/j.1439-0531.2010.01660.x
  15. Toescu V, Nuttall S, Martin U, Kendall M, Dunne F. Oxidative stress and normal pregnancy. Clinical endocrinology. 2002;57(5):609-13. https://doi.org/10.1046/j.1365-2265.2002.01638.x
  16. Santarosa B, Dantas G, Ferreira D, Hooper HB, Sinzato Y, Damasceno D, et al. Comparison of oxidative stress markers between single and twin gestations in Dorper ewes during pregnancy, delivery and postpartum. Small Ruminant Research. 2021;197:106333. https://doi.org/10.1046/j.1365-2265.2002.01638.x
  17. Gaál T, Ribiczeyné-Szabó P, Stadler K, Jakus J, Reiczigel J, Kövér P, et al. Free radicals, lipid peroxidation and the antioxidant system in the blood of cows and newborn calves around calving. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 2006;143(4):391-6. https://doi.org/10.1016/j.cbpb.2005.12.014
  18. Mutinati M, Piccinno M, Roncetti M, Campanile D, Rizzo A, Sciorsci RL. Oxidative stress during pregnancy in the sheep. Reproduction in Domestic Animals. 2013;48(3):353-7. https://doi.org/10.1111/rda.12141
  19. Rios TS, Esqueda MTS-T, Cruz AD, Mora JLC, Perrusquía RG, Morales JLR, et al. Oxidative state of ewes with different number of parity during gestation and lactation. Pesquisa Veterinária Brasileira. 2017;37(12):1405-10.
  20. Erişir M, Benzer F, Kandemir FM. Changes in the rate of lipid peroxidation in plasma and selected blood antioxidants before and during pregnancy in ewes. Acta Veterinaria Brno. 2009;78(2):237-42. https://doi.org/10.2754/avb200978020237
  21. Soriano VS, e Sá J, Junior HPR, Torbitz VD, Moresco RN, Stefani LM, et al. Postpartum nitric oxide, oxidants and antioxidants levels in ewes and their lambs. Small Ruminant Research. 2015;123(1):13-6. https://doi.org/10.1016/j.smallrumres.2014.09.010
  22. Nawito M, Abd El Hameed AR, Sosa A, Mahmoud KGM. Impact of pregnancy and nutrition on oxidant/antioxidant balance in sheep and goats reared in South Sinai, Egypt. Veterinary World. 2016;9(8):801. https://doi.org/10.14202/vetworld.2016.801-805
  23. Begum S, Yamasaki M, Mochizuki M. Urinary levels of nitric oxide metabolites in normal pregnancy and preeclampsia. Journal of Obstetrics and Gynaecology Research. 1996;22(6):551-9. https://doi.org/10.1111/j.1447-0756.1996.tb01070.x
  24. King R, Gude N, Di IJ, Brennecke S. Regulation of human placental fetal vessel tone: role of nitric oxide. Reproduction, fertility and development. 1995;7(6):1407-11. https://doi.org/10.1071/rd9951407
  25. Feldman PL, Stuehr DJ, Griffith OW, Fukuto JM. Mechanisms of mammalian nitric oxide biosynthesis. Biochemical, Pharmacological, and Clinical Aspects of Nitric Oxide: Springer; 1995. p. 13-20. https://doi.org/10.1007/978-1-4615-1903-4_2
  26. Hata T, Hashimoto M, Kanenishi K, Akiyama M, Yanagihara T, Masumura S. Maternal circulating nitrite levels are decreased in both normal normotensive pregnancies and pregnancies with preeclampsia. Gynecologic and obstetric investigation. 1999;48(2):93-7. https://doi.org/10.1159/000010147
  27. Brown MA, Tibben E, Zammit VC, Cario GM, Carlton MA. Nitric oxide excretion in normal and hypertensive pregnancies. Hypertension in pregnancy. 1995;14(3):319-26. https://doi.org/10.3109/10641959509015678
  28. Smárason Jr A, Allman KG, Young D, Redman CW. Elevated levels of serum nitrate, a stable end product of nitric oxide, in women with pre‐eclampsia. BJOG: An International Journal of Obstetrics & Gynaecology. 1997;104(5):538-43. https://doi.org/10.1111/j.1471-0528.1997.tb11528.x
  29. Yüksel S, Yiğit AA. Malondialdehyde and nitric oxide levels and catalase, superoxide dismutase, and glutathione peroxidase levels in maternal blood during different trimesters ofpregnancy and in the cord blood of newborns. Turkish journal of medical sciences. 2015;45(2):454-9. https://doi.org/10.3906/SAG-1311-72