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Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season

Year 2014, Volume: 40 Issue: 2, 202 - 210, 22.07.2014

Abstract

The plasma levels of copper (Cu), zinc (Zn), manganese (Mn) and selenium (Se) were measured in pregnant fat tailed ewes in relation to the activities of the relevant antioxidant enzymes as well as the oxidative status of the animals. Whole blood samples of 47 ewes were taken at the first day of a 51-day breeding period (before pregnancy) and 120 days later (70-120 days of pregnancy). Pregnancy was confirmed in 43 ewes by measuring plasma progesterone in the samples of day 120. For the whole period of the study, the ewes were grazing on medium-to-low quality pastures and cereal stubble and were offered about 1 kg/head/day of a mixture of alfalfa hay (40%) and wheat straw (60%) plus at least 100g barley grain/head/day. A trace mineralized supplement was available free choice. The level of malondialdehyde (MDA; an index of lipid peroxidation) and the activities of superoxide dismutase (SOD) and glutathione peroxidase (GPX) were measured in erythrocytes as well as the concentrations of Cu, Zn, Mn and Se in plasma. In the ewes with confirmed pregnancies the results were compared between days 1 and 120. MDA level increased (P≤0.05) at day 120, revealing the presence of oxidative stress. The activities of SOD and GPX and the concentrations of Cu and Zn decreased (P≤0.05), revealing antioxidant depletion in peripheral blood. Increased metabolic functions of reproductive tissues during pregnancy along with some nutritional insufficiencies could be the underlying reasons of these findings. Fat tailed ewes may experience oxidative stress during pregnancy when they are mainly fed medium to low quality forages. Further investigations are suggested to assess if the correction of such conditions is effective in reducing the proportion of barren ewes and improving the performance of the born lambs.

Key Words: Copper, zinc, selenium, antioxidant enzymes, sheep

References

  • Al-Gubory, K.H., Bolifraud, P., Germain, G., Nicole, A., Ceballos-Bicot, I. 200 Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction 128, 767-774. Al-Gubory, K.H., Fowler, P.A., Garrel, C. 2010. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. The International Journal of Biochemistry and Cell Biology 42, 1634-1650. Al-Gubory, K.H., Huet, J.C., Pernollet, J.C., Martal, J., Locatelli, A. 2003. Corpus luteum derived copper, zinc-superoxide dismutase serves as a luteinizing hormone-release inhibiting factor in sheep. Molecular and Cellular Endocrinology 199, 1-9.
  • Al-Gubory, K.H., Solari, A., Mirman, B. 1999. Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep. Reproduction, Fertility and Development 11, 317-322.
  • Bernabucci, U., Ronchi, B., Lacetera, N., Nardone, A. 2002. Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of Dairy Science 85, 217321
  • Bernabucci, U., Ronchi, B., Lacetera, N., Nardone, A. 2005. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science 88, 2017-2026.
  • Blomberg, L.A., Long, E.L., Sonstegard, T.S., Van Tassell, C.P., Dobrinsky, J.R., Zuelke, K.A. 200 Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiological Genomics 20, 188-194. Boscos, C.M., Samartzi, F.C., Dellis, S., Rogge, A., Stefanakis, A., Krambovitis, E. 2002. Use of progestagen-gonadotrophin treatments in estrus synchronization of sheep. Theriogenology 58, 1261-1272.
  • Castillo, C., Hernandez, J., Bravo, A., LopezAlonso, M., Pereira, V., Benedito, J.L. 2005. Oxidative status during late pregnancy and early lactation in dairy cows. The Veterinary Journal 169, 286-292.
  • Celi, P. 2008. Oxidative Stress in Ruminants. In: Mandelker L., Vajdovich P. (eds.) Studies on Veterinary Medicine. Humana Press pp.1912
  • Celi, P., Di Trana, A., Claps, S. 2010. Effect of plane of nutrition on oxidative stress in goats during the peripartum period. The Veterinary Journal 184, 95-99.
  • Di Trana, A., Celi, P., Claps, S., Fedele, V., Rubino, R. 200 The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation. Animal Science 82, 717-722. Droge, W. 2002. Free radicals in the physiological control of cell function. Physiology Reviews 82, 47–
  • El Mouatassim, S., Guerin, P., Menezo, Y. 1999. Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Molecular Human Reproduction 5, 720-725.
  • Gaál, T , M e , M , Mi k c a, O , Ri ic e - a , P. 19 Effect of fasting on blood lipid peroxidation parameters of sheep. Research in Veterinary Science 55, 104-107. Gaál, T , Ri ic e -S a , P , S adler, K , ak , , Reic i el, , K v r, P , M e , M , Süme h , L. 2006. 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 143, 3913
  • Garrel, C., Fowler, P.A., Al-Gubory, K.H. 2010. Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. Journal of Endocrinology 205, 107-116.
  • Glimp, H.A. 1991. Nutrition of the ewe. In: Church D.C. (ed.) Livestock Feeds and Feeding, (Prentice Hall, Englewood Cliffs), pp. 306-322.
  • Harvey, M.B., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A., Watson, A.J. 1995. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biology of Reproduction 53, 532-5
  • Jauniaux, E., Watson, A.L., Hempstock, J., Bao, Y.P., Skepper, J.N., Burton, G.J. 2000. Onset of maternal arterial blood flow and placental oxidative stress: a possible factor in human early pregnancy failure. The American Journal of Pathology 157, 2111-2122.
  • Kamiloglu, N.N., Beytut, E., Aksakal, M. 2006. Alteration in antioxidant status and lipid peroxidation of sheep previously treated with vitamin a and β-carotene during breeding and periparturient period. Bulletin of Veterinary Institute of Pulawy 50, 171-177.
  • Liu, A.X., Jin, F., Zhang, W.W., Zhou, T.H., Zhou, C.Y., Yao, W.M. 2006. Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biology of Reproduction 75, 414-420. Lykkesfeldt, J. 200 Determination of malondialdehyde as dithiobarbituric acid adduct in biological samples by HPLC with fluorescence detection: Comparison with ultraviolet-visible spectrophotometry. Clinica Chemica 47, 1725-1727.
  • Lykkesfeldt, J., Svendsen, O. 2007. Oxidants and antioxidants in disease: oxidative stress in farm animals. The Veterinary Journal 173, 502-511. Mohebbi-Fani, M., Mirzaei, A., Nazifi, S., Shabbooie, Z. 2012. Changes of vitamins A, E, and C and lipid peroxidation status of breeding and pregnant sheep during dry seasons on medium-to-low quality forages. Tropical Animal Health and Production 44, 259-265.
  • Mohebbi-Fani, M., Nazifi, S., Ansari-Lari, M., Namazi, F. 2010. Mixed mineral deficiencies in a dairy herd with subclinical production disorders. Comparative Clinical Pathology 19, 37Moore, K., Roberts, L.J. 1998. Measurement of Lipid Peroxidation. Free Radical Research 28, 6596
  • Myatt, L. 2006. Placental adaptive responses and fetal programming. Journal of Physiology 572, 25
  • Myatt, L., Cui, X. 2004. Oxidative stress in the placenta. Histochemistry and Cell Biology 122, 369-3
  • NRC, 1985. Nutrient Requirements of Sheep, Sixth Revised Edition (Washington, D.C., National Academy Press).
  • Orsi, N.M., Leese, H.J. 2001. Protection against reactive oxygen species during mouse preimplantation embryo development: Role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Molecular Reproduction and Development 59, 44-53
  • Paglia, D.E., Valentine, W.N. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158-169. Qanungo, S., Mukherjea, M. 2000. Ontogenic profile of some antioxidants and lipid peroxidation in human placental and fetal tissues. Molecular and Cellular Biochemistry 215, 11-19.
  • Qanungo, S., Sen, A., Mukherjea, M. 1999. Antioxidant status and lipid peroxidation in human feto-placental unit. Clinica Chimica Acta 285, 1-12.
  • Rueda, B.R., Tilly, K.I., Hansen, T.R., Hoyer, P.B., Tilly, J.L. 1995. Expression of superoxide dismutase, catalase and glutathione peroxidase in the bovine corpus luteum: evidence supporting a role for oxidative stress in luteolysis. Endocrinology 3, 227-232.
  • Shenkin, A., Baines, M., Fell, G.S., Lyon, T.D.G. 200 Vitamins and Trace Elements. In: C.A. Burtis, E.R. Ashwood and D.E. Bruns (eds.) Tietz Textbook of Clinical Chemistry and Molecular Dignostics, Elsevier Saunders, pp. 1075-1164.
  • Shimamura, K., Sugino, N., Yoshida, Y., Nakamura, Y., Ogino, K., Kato, H. 1995. Changes in lipid peroxide and antioxidant enzyme activities in corpora lutea during pseudopregnancy in rats.
  • Journal of Reproduction and Fertility 105, 2532
  • Sugino, N., Nakamura, Y., Takeda, O., Ishimatsu, M., Kato, H. 1993. Changes in activities of superoxide dismutase and lipid peroxide in corpus luteum during pregnancy in rats. Journal of Reproduction and Fertility 97, 347-351.
  • Sugino, N., Takiguchi, S., Kashida, S., Karube, A., Nakamura, Y., Kato, H. 2000. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Molecular Human Reproduction 6, 19Suttle, N.F. 1986. Problems in the diagnosis and anticipation of trace element deficiencies in grazing livestock. Veterinary Record 119, 1481
  • Uauy, R., Olivares, M., Gonzalez, M. 1998. Essentiality of copper in humans. American Journal of Clinical Nutrition 67, 952S-959S.
  • Venditti, P., Meo, S. 2006. Thyroid hormone-induced oxidative stress. Cellular and Molecular Life Sciences 63, 414-434.

KURU DÖNEMDE OTLATILAN GEBE KOYUNLARIN PLAZMALARINDA SELENYUM, BAKIR, ÇİNKO, MANGAN VE ONLARLA İLİŞKİLİ ANTİOKSİDAN ENZİMLER

Year 2014, Volume: 40 Issue: 2, 202 - 210, 22.07.2014

Abstract

Yağlı kuyruklu gebe koyunlarda, hayvanların oksidatif durumunun yanı sıra ilişkili antioksidan enzimlerin aktiviteleri hakkında Bakır (Cu), Çinko (Zn), Mangan (Mn) ve Selenyum’un (Se) plazma seviyeleri ölçüldü. 47 adet koyunun tüm kan örnekleri, 51 günlük üreme periyodlarının ilk gününde (gebelik öncesi) ve 120 gün sonra (gebeliğin 70-120 günleri) alındı. Gebelik, 120 günlük örneklerde plazma progesteronu ölçülerek 43 koyunda doğrulandı. Tüm çalışma periyodunda, koyunlar düşük-orta kaliteli otlaklarda ve ekin anızında otlatıldı ve hayvan başına günlük yaklaşık 1 kg, %40 kaba yonca samanı ve %60 buğday samanı karışımı ile ayrıca en az 100 g arpa tanesi önerildi. İz mineral ilavesi, seçmeksizin uygundu. Plazmada Cu, Zn, Mn ve Se konsantrasyonun yanı sıra eritrositlerde malondialdehit (MDA: lipid peroksidasyonu indeksi), superoksit dismutaz (SOD) ve glutatyon peroksidaz (GPX) düzeyi ölçüldü. MDA seviyesi, oksidatif stresin varlığıyla 120ci günde arttı (P≤0,05). SOD ve GPX aktiviteleri ve Cu ve Zn konsantrasyonları, periferal kanda antioksidan azalmasıyla ilişkili olarak azaldı (P≤0,05). Gebelik süresince üremeyi sağlayan dokuların artan metabolik fonksiyonları bazı besin yetersizlikleri ile birlikte bulguların altında yatan nedenler olabilir. Yağlı kuyruklu koyunlar, düşük-orta kaliteli baklagil yemleriyle beslenildiği zaman gebelik süresince oksidatif strese maruz kalabilir. Gelecek çalışmalarda verimsiz dişi koyunların oranının azaltması ve yeni doğan kuzuların performansının geliştirilmesinde bu koşulların ilişkisinin araştırılması önerilir.

Anahtar Kelimeler: Bakır, çinko, selenyum, antioksidan enzimler, koyun

References

  • Al-Gubory, K.H., Bolifraud, P., Germain, G., Nicole, A., Ceballos-Bicot, I. 200 Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction 128, 767-774. Al-Gubory, K.H., Fowler, P.A., Garrel, C. 2010. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. The International Journal of Biochemistry and Cell Biology 42, 1634-1650. Al-Gubory, K.H., Huet, J.C., Pernollet, J.C., Martal, J., Locatelli, A. 2003. Corpus luteum derived copper, zinc-superoxide dismutase serves as a luteinizing hormone-release inhibiting factor in sheep. Molecular and Cellular Endocrinology 199, 1-9.
  • Al-Gubory, K.H., Solari, A., Mirman, B. 1999. Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep. Reproduction, Fertility and Development 11, 317-322.
  • Bernabucci, U., Ronchi, B., Lacetera, N., Nardone, A. 2002. Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of Dairy Science 85, 217321
  • Bernabucci, U., Ronchi, B., Lacetera, N., Nardone, A. 2005. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science 88, 2017-2026.
  • Blomberg, L.A., Long, E.L., Sonstegard, T.S., Van Tassell, C.P., Dobrinsky, J.R., Zuelke, K.A. 200 Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiological Genomics 20, 188-194. Boscos, C.M., Samartzi, F.C., Dellis, S., Rogge, A., Stefanakis, A., Krambovitis, E. 2002. Use of progestagen-gonadotrophin treatments in estrus synchronization of sheep. Theriogenology 58, 1261-1272.
  • Castillo, C., Hernandez, J., Bravo, A., LopezAlonso, M., Pereira, V., Benedito, J.L. 2005. Oxidative status during late pregnancy and early lactation in dairy cows. The Veterinary Journal 169, 286-292.
  • Celi, P. 2008. Oxidative Stress in Ruminants. In: Mandelker L., Vajdovich P. (eds.) Studies on Veterinary Medicine. Humana Press pp.1912
  • Celi, P., Di Trana, A., Claps, S. 2010. Effect of plane of nutrition on oxidative stress in goats during the peripartum period. The Veterinary Journal 184, 95-99.
  • Di Trana, A., Celi, P., Claps, S., Fedele, V., Rubino, R. 200 The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation. Animal Science 82, 717-722. Droge, W. 2002. Free radicals in the physiological control of cell function. Physiology Reviews 82, 47–
  • El Mouatassim, S., Guerin, P., Menezo, Y. 1999. Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Molecular Human Reproduction 5, 720-725.
  • Gaál, T , M e , M , Mi k c a, O , Ri ic e - a , P. 19 Effect of fasting on blood lipid peroxidation parameters of sheep. Research in Veterinary Science 55, 104-107. Gaál, T , Ri ic e -S a , P , S adler, K , ak , , Reic i el, , K v r, P , M e , M , Süme h , L. 2006. 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 143, 3913
  • Garrel, C., Fowler, P.A., Al-Gubory, K.H. 2010. Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. Journal of Endocrinology 205, 107-116.
  • Glimp, H.A. 1991. Nutrition of the ewe. In: Church D.C. (ed.) Livestock Feeds and Feeding, (Prentice Hall, Englewood Cliffs), pp. 306-322.
  • Harvey, M.B., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A., Watson, A.J. 1995. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biology of Reproduction 53, 532-5
  • Jauniaux, E., Watson, A.L., Hempstock, J., Bao, Y.P., Skepper, J.N., Burton, G.J. 2000. Onset of maternal arterial blood flow and placental oxidative stress: a possible factor in human early pregnancy failure. The American Journal of Pathology 157, 2111-2122.
  • Kamiloglu, N.N., Beytut, E., Aksakal, M. 2006. Alteration in antioxidant status and lipid peroxidation of sheep previously treated with vitamin a and β-carotene during breeding and periparturient period. Bulletin of Veterinary Institute of Pulawy 50, 171-177.
  • Liu, A.X., Jin, F., Zhang, W.W., Zhou, T.H., Zhou, C.Y., Yao, W.M. 2006. Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biology of Reproduction 75, 414-420. Lykkesfeldt, J. 200 Determination of malondialdehyde as dithiobarbituric acid adduct in biological samples by HPLC with fluorescence detection: Comparison with ultraviolet-visible spectrophotometry. Clinica Chemica 47, 1725-1727.
  • Lykkesfeldt, J., Svendsen, O. 2007. Oxidants and antioxidants in disease: oxidative stress in farm animals. The Veterinary Journal 173, 502-511. Mohebbi-Fani, M., Mirzaei, A., Nazifi, S., Shabbooie, Z. 2012. Changes of vitamins A, E, and C and lipid peroxidation status of breeding and pregnant sheep during dry seasons on medium-to-low quality forages. Tropical Animal Health and Production 44, 259-265.
  • Mohebbi-Fani, M., Nazifi, S., Ansari-Lari, M., Namazi, F. 2010. Mixed mineral deficiencies in a dairy herd with subclinical production disorders. Comparative Clinical Pathology 19, 37Moore, K., Roberts, L.J. 1998. Measurement of Lipid Peroxidation. Free Radical Research 28, 6596
  • Myatt, L. 2006. Placental adaptive responses and fetal programming. Journal of Physiology 572, 25
  • Myatt, L., Cui, X. 2004. Oxidative stress in the placenta. Histochemistry and Cell Biology 122, 369-3
  • NRC, 1985. Nutrient Requirements of Sheep, Sixth Revised Edition (Washington, D.C., National Academy Press).
  • Orsi, N.M., Leese, H.J. 2001. Protection against reactive oxygen species during mouse preimplantation embryo development: Role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Molecular Reproduction and Development 59, 44-53
  • Paglia, D.E., Valentine, W.N. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158-169. Qanungo, S., Mukherjea, M. 2000. Ontogenic profile of some antioxidants and lipid peroxidation in human placental and fetal tissues. Molecular and Cellular Biochemistry 215, 11-19.
  • Qanungo, S., Sen, A., Mukherjea, M. 1999. Antioxidant status and lipid peroxidation in human feto-placental unit. Clinica Chimica Acta 285, 1-12.
  • Rueda, B.R., Tilly, K.I., Hansen, T.R., Hoyer, P.B., Tilly, J.L. 1995. Expression of superoxide dismutase, catalase and glutathione peroxidase in the bovine corpus luteum: evidence supporting a role for oxidative stress in luteolysis. Endocrinology 3, 227-232.
  • Shenkin, A., Baines, M., Fell, G.S., Lyon, T.D.G. 200 Vitamins and Trace Elements. In: C.A. Burtis, E.R. Ashwood and D.E. Bruns (eds.) Tietz Textbook of Clinical Chemistry and Molecular Dignostics, Elsevier Saunders, pp. 1075-1164.
  • Shimamura, K., Sugino, N., Yoshida, Y., Nakamura, Y., Ogino, K., Kato, H. 1995. Changes in lipid peroxide and antioxidant enzyme activities in corpora lutea during pseudopregnancy in rats.
  • Journal of Reproduction and Fertility 105, 2532
  • Sugino, N., Nakamura, Y., Takeda, O., Ishimatsu, M., Kato, H. 1993. Changes in activities of superoxide dismutase and lipid peroxide in corpus luteum during pregnancy in rats. Journal of Reproduction and Fertility 97, 347-351.
  • Sugino, N., Takiguchi, S., Kashida, S., Karube, A., Nakamura, Y., Kato, H. 2000. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Molecular Human Reproduction 6, 19Suttle, N.F. 1986. Problems in the diagnosis and anticipation of trace element deficiencies in grazing livestock. Veterinary Record 119, 1481
  • Uauy, R., Olivares, M., Gonzalez, M. 1998. Essentiality of copper in humans. American Journal of Clinical Nutrition 67, 952S-959S.
  • Venditti, P., Meo, S. 2006. Thyroid hormone-induced oxidative stress. Cellular and Molecular Life Sciences 63, 414-434.
There are 33 citations in total.

Details

Primary Language English
Journal Section Research Article
Authors

Mehdi Mohebbı-fanı This is me

Abdollah Mırzaeı This is me

Saeed Nazıfı

Mohammad Tabandeh This is me

Zahra Shabbooeı This is me

Publication Date July 22, 2014
Published in Issue Year 2014 Volume: 40 Issue: 2

Cite

APA Mohebbı-fanı, M., Mırzaeı, A., Nazıfı, S., Tabandeh, M., et al. (2014). Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season. İstanbul Üniversitesi Veteriner Fakültesi Dergisi, 40(2), 202-210. https://doi.org/10.16988/iuvfd.32621
AMA Mohebbı-fanı M, Mırzaeı A, Nazıfı S, Tabandeh M, Shabbooeı Z. Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season. iuvfd. July 2014;40(2):202-210. doi:10.16988/iuvfd.32621
Chicago Mohebbı-fanı, Mehdi, Abdollah Mırzaeı, Saeed Nazıfı, Mohammad Tabandeh, and Zahra Shabbooeı. “Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes During Dry Season”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 40, no. 2 (July 2014): 202-10. https://doi.org/10.16988/iuvfd.32621.
EndNote Mohebbı-fanı M, Mırzaeı A, Nazıfı S, Tabandeh M, Shabbooeı Z (July 1, 2014) Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 40 2 202–210.
IEEE M. Mohebbı-fanı, A. Mırzaeı, S. Nazıfı, M. Tabandeh, and Z. Shabbooeı, “Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season”, iuvfd, vol. 40, no. 2, pp. 202–210, 2014, doi: 10.16988/iuvfd.32621.
ISNAD Mohebbı-fanı, Mehdi et al. “Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes During Dry Season”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 40/2 (July 2014), 202-210. https://doi.org/10.16988/iuvfd.32621.
JAMA Mohebbı-fanı M, Mırzaeı A, Nazıfı S, Tabandeh M, Shabbooeı Z. Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season. iuvfd. 2014;40:202–210.
MLA Mohebbı-fanı, Mehdi et al. “Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes During Dry Season”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi, vol. 40, no. 2, 2014, pp. 202-10, doi:10.16988/iuvfd.32621.
Vancouver Mohebbı-fanı M, Mırzaeı A, Nazıfı S, Tabandeh M, Shabbooeı Z. Selenium, Copper, Zinc, Manganese and Their Relevant Antioxidant Enzymes in Plasma of Grazing Pregnant Ewes during Dry Season. iuvfd. 2014;40(2):202-10.