The association of some blood metabolites and NF-κB gene expression with subclinical ketosis in Holstein dairy cows during the transition period
Subject Areas :
Veterinary Clinical Pathology
Saeideh Moradi
1
(Ph.D. Student of Animal Physiology, Department of Animal Science, Faculty of Agriculture,
University of Tabriz, Tabriz, Iran.)
Gholamali moghaddam
2
(Professor, Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Tabriz, Iran.)
Samad lotfollahzade
3
(Associate Professor, Department of Clinical Science, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran.)
Raziallah Jafari
4
(Associate Professor, Department of Clinical Science, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.)
Abbas Rafat
5
(Professor, Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Tabriz, Iran.)
Received: 2022-04-20
Accepted : 2022-08-13
Published : 2022-08-23
Keywords:
Oxidative stress,
subclinical ketosis,
B,
BHBA,
NF-&kappa,
Abstract :
Subclinical ketosis is one of the most important metabolic diseases which irreversible economic effects on the dairy industry. Subclinical ketosis has been associated with increases reactive oxygen species and oxidative stress in cells. Since the nuclear factor kappa-B is known as a fast cellular response factor to endogenous stress; this study was conducted to evaluate relative gene expression and some blood metabolites in dairy cattle during the transition period were performed. Blood samples (5 mL) were obtained from the tail vein of 100 cows with fourth and fifth lactation one week pre-parturition and one week post-parturition. In the present study, It was found positive correlations between plasma NEFA concentrations in the pre-parturition period and BHBA, GGT, MDA, and NF-κB and negative correlations between plasma NEFA concentration and HDL. As well as, the positive correlations between BHBA plasma concentration and NEFA , ALP, GGT, MDA and NF-κB and negative correlations between plasma BHBA concentration and HDL in the post-parturition period. Also while the cut-off point BHBA≤1.2(Health) and BHBA≥ 1.2(mmol/l)(subclinical ketosis or disease) in the post-parturition period was designated, it was observed that NEFA(p<.0001), BHBA(p<.0001), MDA(p<.0001), GGT(p<.0001) and ALP(p=0.03) were gradually increased, and HDL(p= <.0001) gradually decreased in disease group. The results showed that the activity of NF-κB (p<.0001) was gradually increased in the disease group. Also results showed that increased NEFAs and BHBA increased inflammation response through activating the NF-κB pathway and oxidative stress.
References:
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Amouoghli Tabrizi, B., Safi, S., Asri Rezaee, S. and Abdie Nojamehr. (2007). Study of the levels of betahydroxy butyrate, glucose, protein and albumin in Holstein cows with subclinical ketosis. Journal of Veterinary Clinical Pathology, 2(2): 125-132. [In Persian]
Asri Rezaee, S., Amouoghli Tabrizi, B. and Saber Marouf, B. (2012). Evaluation of the levels of Leptin, Beta hydroxyl butyrate, Glucose, Cholesterol and Triglyceride in serum of Holstein cows with sub clinical ketosis. Journal of Veterinary Clinical pathology, 6(3): 1647-1656. [In Persian]
Baker, R.G., Hayden, M.S. and Ghosh, S. (2011). NF-κB, inflammation, and metabolic disease. Cell Metabolism, 13(1): 11-22.
Bernabucci, U., Ronchi, B., Lacetera, N. and 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(6): 2017-2026.
Chapinal, N., Carson, M., Duffield, T.F., Capel, M., Godden, S., Overton, M., et al. (2011). The association of serum metabolites with clinical disease during the transition period. Journal of Dairy Science, 94(10): 897-903.
Contreras, G.A., Raphael, W., Mattmiller, S.A., Gandy, J. and Sordilo, L.M. (2012). Nonesterified fatty acids modify inflammatory response and eicosanoid biosynthesis in bovine endothelial cells. Journal of Dairy Science, 95(9): 5011-5023.
Czaja, M.J. (2007). Cell signaling in oxidative stress-induced liver injury. In Seminars in Liver Disease, 27(4) : 378-389.
Dann, H.M. and Drackley, J.K. (2005). Carnitine palmitoyltransferaseI in liver of periparturient dairy cows: effects of prepartum intake, postpartum induction of ketosis, and periparturient disorders. Journal of Dairy Science, 88(11): 3851-3859.
Denk, A., Wirth, T. and Baumann, B. (2000). NF-κB transcription factors: critical regulators of hematopoiesis and neuronal survival. Cytokine and Growth Factor Reviews, 11(4): 303-320.
Dorrington, M.G. and Fraser, I.D. (2019). NF-κB signaling in macrophages: dynamics, crosstalk, and signal integration. Frontiers in Immunology, 10(1): 705-708.
Drackley, J. K. (1999). Biology of dairy cows during the transition period: The final frontier?. Journal of Dairy Science, 82(11): 2259-2273.
Du, X., Chen, L., Huang, D., Peng, Z., Zhao, C., Zhang, Y., et al. (2017). Elevated apoptosis in the liver of dairy cows with ketosis. Cellular Physiology and Biochemistry, 43(2): 568-578.
El-Bahr, S.M. and El-Deeb, W.M. (2017). Oxidative stress and cardiac biomarkers in lambs affected with enzootic ataxia: the diagnostic and prognostic significance. Veterinarski Arhiv, 87(3): 259-271.
El-Deeb, W.M. and Younis, E.E. (2009). Clinical and biochemical studies on Theileria annulata in Egyptian buffaloes (Bubalus bubalis) with particular orientation to oxidative stress and ketosis relationship. Veterinary Parasitology, 164(2-4): 301-305.
Feldstein, A.E., Werneburg, N.W., Canbay, A., Guicciardi, M.E., Bronk, S.F., Rydzewski, R., et al. (2004). Free fatty acids promote hepatic lipotoxicity by stimulating TNFα expression via a lysosomal pathway. Hepatology, 40(1): 185-194.
Fiore, F., Spissu, N., Sechi, S. and Coccom, R. (2019). Evaluation of oxidative stress in dairy cows with left displacement of abomasum. Animal, 9(11): 966.
Galvão, K.N., Flaminio, M.J.B.F., Brittin, S.B., Sper, R., Fraga, M., Caixeta, L., et al. (2010). Association between uterine disease and indicators of neutrophil and systemic energy status in lactating Holstein cows. Journal of Dairy Science, 93(7): 2926-2937.
González, F.D., Muiño, R., Pereira, V., Campos, R. and Benedito, J.L. (2011). Relationship among blood indicators of lipomobilization and hepatic function during early lactation in high-yielding dairy cows. Journal of Veterinary Science, 12(3): 251-255.
Grummer, R.R. (1995). Impact of changes in organic nutrient metabolism on feeding the transition dairy cow. Journal of Animal Science, 73(9): 2820-2833.
Hammon, D., Evjen, I.M., Dhiman, T.R., Goff, J.P. and Walters, L.J. (2006). Neutrophil function and energy status in Holstein cows with uterine health disorders. Veterinary Immunology and Immunopathology, 113(1-2): 21-29.
Hayden, M.S. and Ghosh, S. (2008). Shared principles in NF-κB signaling. Cell, 132(3): 344-362.
Hayden, M.S., West, A.P. and Ghosh, S. (2006). NF-κB and the immune response. Oncogene, 25(51): 6758-6780.
Herdt, T.H. (2000). Ruminant adaptation to negative energy balance: Influences on the etiology of ketosis and fatty liver. Veterinary Clinics of North America: Food Animal Practice, 16(2): 215-230.
Hybertson, B.M., Gao, B., Bose, S.K. and McCord, J.M. (2011). Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Molecular Aspects of Medicine, 32(4-6): 234-246.
Ji, L.L., Gomez-Cabera, M.C. and Vina, J. (2006). Exercise and hormesis. Annals of the New York Academy of Sciences, 1067(1): 425-435.
LeBlanc, S.J., Osawa, T. and Dubuc, J. (2011). Reproductive tract defense and disease in postpartum dairy cows. Theriogenology, 76(9): 1610-1618.
Leopold, J. A. and Loscalzo, J. (2009). Oxidative risk for atherothrombotic cardiovascular disease. Free Radical Biology and Medicine, 47(12): 1673-1706.
Li, X., Chen, H., Lei, L., Liu, J., Guan, Y., Liu, Z., et al. (2013). Non-esterified fatty acids activate the AMP-activated protein kinase signaling pathway to regulate lipid metabolism in bovine hepatocytes. Cell Biochemistry and Biophysics, 67(3): 1157-1169.
Li, Y., Ding, H.Y., Wang, X.C., Feng, S.B., Li, X.B., Wang, Z., et al. (2016). An association between the level of oxidative stress and the concentrations of NEFA and BHBA in the plasma of ketotic dairy cows. Journal of Animal Physiology and Animal Nutrition, 100(5): 844-851.
Liguori, I., Russo, G., Curcio, F., Bulli, G., Aran, L., Della-Morte, D., et al. (2018). Oxidative stress, aging, and diseases. Clinical Interventions in Aging, 13: 757-772.
Liu, T., Zhang, L., Joo, D. and Sun, S.C. (2017). NF-κB signaling in inflammation. Signal Transduction and Targeted Therapy, 2: 17023.
Mezzetti, M., Cattaneo, L., Maria Passamonti, M., Lopreiato, V., Minuti, A. and Trevisi, E. (2021). The Transition Period Updated: A Review of the New Insights into the Adaptation of Dairy Cows to the New Lactation. Dairy, 2(4): 617-636.
Morgan, M.J. and Liu, Z.G. (2011). Crosstalk of reactive oxygen species and NF-κB signaling. Cell Research, 21(1): 103-115.
Nelson, D.L., Cox, M.M. and Lehninger, A.L. (2005). Principles of biochemistry. 4th ed., USA: New York, Freeman, pp: 600-622.
Niu, Q., Cao, M., Chen, S., Zhao,Y., Li, C. and Zhou, X. (2019). Effective and economical column- based method for RNA isolation from animal cells. Biotechnology Letters, 41(8-9): 915-920.
Ospina, P.A., Nydam, D.V., Stokol, T. and Overton, T.R. (2010). Evaluation of nonesterified fatty acids and beta-hydroxybutyrate in transition dairy cattle in the northeastern United States: critical thresholds for prediction of clinical diseases. Journal of Dairy Science, 93(4): 546-554.
Pedernera, M., Celi, P., García, S.C., Salvin, E.H., Barchia, I. and Fulkerson, W.J. (2010). Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. The Veterinary Journal, 186(3): 352-357.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic acids Research, 29(9): 45-49.
Puchalska, P. and Crawford, P.A. (2017). Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metabolism, 25(2): 262-284.
Puppel, K., Gołębiewski, M., Solarczyk, P., Grodkowski, G., Slósarz, J., Kunowska-Slósarz, M., et al. (2019). The relationship between plasma β-hydroxybutyric acid and conjugated linoleic acid in milk as a biomarker for early diagnosis of ketosis in postpartum Polish Holstein-Friesian cows. BMC Veterinary Research, 15(1): 367.
Romagnoli, M., Gomez-Cabrera, M.C., Perrelli, M.G., Biasi, F., Pallardo, V.F., Sastre, J., et al. (2010). Xanthine oxidase-induced oxidative stress causes activation of NF-κB and inflammation in the liver of type I diabetic rats. Free Radical Biology and Medicine, 49(2): 171-177.
Sadeghi-nasab, A., Hassanpour, A., Sabaghsaray, H. and Amiri-Sadeghan, S. (2011). Assessment of thyroid hormones, insulin and magnesium in dairy cattle with subclinical ketosis. Journal of Veterinary Clinical Pathology, 5(2): 1149-1159. [In Persian]
Senoh, T., Oikawa, S., Nakada, K., Tagami, T. and Iwasaki, T. (2019). Increased serum malondialdehyde concentration in cows with subclinical ketosis. Journal of Veterinary Medical Science. 81: 817-820.
Shi, X., Li, D., Deng, Q., Li, Y., Sun, G., Yuan, X., et al. (2015). NEFAs activate the oxidative stress-mediated NF-κB signaling pathway to induce inflammatory response in calf hepatocytes. The Journal of Steroid Biochemistry and Molecular Biology, 145(8): 103-112.
Sordillo, L.M. and Aitken, S.L. (2009). Impact of oxidative stress on the health and immune function of dairy cattle. Veterinary Immunology and Immunopathology, 128(1-3): 104-109.
Sordillo, L.M. and Raphael, W. (2013). Significance of metabolic stress, lipid mobilization,and inflammation on transition cow disorders. Veterinary Clinics of North America: Food Animal Practice, 29(2): 267-278.
Stokol, T. and Nydam, D.V. (2006). Effect of hemolysis on nonesterified fatty acid and beta-hydroxybutyrate concentrations in bovine blood. Journal of Veterinary Diagnostic Investigation, 18(5): 466-469.
Suriyasathaporn, W.S., Heuer, C.H., Noordhuizen-Stassen, E.N. and Schukken, Y.H.S. (2000). Hyperketonemia and the impairment of udder defense: a review. Veterinary Research, 31(4): 397-412.
Turk, R., Juretić, D., Gereš, D., Svetina, A., Turk, N. and Flegar-Mestric, Z. (2008). Influence of oxidative stress and metabolic adaptation on PON1 activity and MDA level in transition dairy cows. Animal Reproduction Science, 108(1-2): 98-106.
Turk, R., Juretić, D., Gereš, D., Turk, N., Simeon-Rudolf, V., Rekić, B., et al. (2005). Oxidative stress in dairy cows–serum paraoxonase activity related to hepatomegaly. Croatica Chemica Acta, 78(3): 375-378.
Wang, D., Yu, D., Zhao, C., Xia, C., Xu, C. and Wu, L. (2021). Subclinical ketosis risk prediction in dairy cows based on prepartum metabolic indices. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 73(1): 11-17.
Wankhade, P.R., Manimaran, A., Kumaresan, A., Jeyakumar, S., Ramesha, K.P., Sejian, V., et al. (2017). Metabolic and immunological changes in transition dairy cows: A review. Veterinary World, 10(11): 1367-1377.
Weisberg, S.P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., et al. (2006). CCR2 modulates inflammatory and metabolic effects of high-fat feeding. Journal of Clinical Investigation, 116(1): 115-124.
Wree, A., Schlattjan, M., Bechmann, L.P., Claudel, T., Sowa, J.P., Stojakovic, T., et al. (2014). Adipocyte cell size, free fatty acids and apolipoproteins are associated with non-alcoholic liver injury progression in severely obese patients. Metabolism: Clinical and Experimental, 63(12): 1542-1552.
_||_
Adias, T.C., Egerton, E. and Erhabor, O. (2013). Evaluation of coagulation parameters and liver enzymes among alcohol drinkers in Port Harcourt, Nigeria. International Journal of General Medicine, 6(1): 489-94.
Amouoghli Tabrizi, B., Safi, S., Asri Rezaee, S. and Abdie Nojamehr. (2007). Study of the levels of betahydroxy butyrate, glucose, protein and albumin in Holstein cows with subclinical ketosis. Journal of Veterinary Clinical Pathology, 2(2): 125-132. [In Persian]
Asri Rezaee, S., Amouoghli Tabrizi, B. and Saber Marouf, B. (2012). Evaluation of the levels of Leptin, Beta hydroxyl butyrate, Glucose, Cholesterol and Triglyceride in serum of Holstein cows with sub clinical ketosis. Journal of Veterinary Clinical pathology, 6(3): 1647-1656. [In Persian]
Baker, R.G., Hayden, M.S. and Ghosh, S. (2011). NF-κB, inflammation, and metabolic disease. Cell Metabolism, 13(1): 11-22.
Bernabucci, U., Ronchi, B., Lacetera, N. and 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(6): 2017-2026.
Chapinal, N., Carson, M., Duffield, T.F., Capel, M., Godden, S., Overton, M., et al. (2011). The association of serum metabolites with clinical disease during the transition period. Journal of Dairy Science, 94(10): 897-903.
Contreras, G.A., Raphael, W., Mattmiller, S.A., Gandy, J. and Sordilo, L.M. (2012). Nonesterified fatty acids modify inflammatory response and eicosanoid biosynthesis in bovine endothelial cells. Journal of Dairy Science, 95(9): 5011-5023.
Czaja, M.J. (2007). Cell signaling in oxidative stress-induced liver injury. In Seminars in Liver Disease, 27(4) : 378-389.
Dann, H.M. and Drackley, J.K. (2005). Carnitine palmitoyltransferaseI in liver of periparturient dairy cows: effects of prepartum intake, postpartum induction of ketosis, and periparturient disorders. Journal of Dairy Science, 88(11): 3851-3859.
Denk, A., Wirth, T. and Baumann, B. (2000). NF-κB transcription factors: critical regulators of hematopoiesis and neuronal survival. Cytokine and Growth Factor Reviews, 11(4): 303-320.
Dorrington, M.G. and Fraser, I.D. (2019). NF-κB signaling in macrophages: dynamics, crosstalk, and signal integration. Frontiers in Immunology, 10(1): 705-708.
Drackley, J. K. (1999). Biology of dairy cows during the transition period: The final frontier?. Journal of Dairy Science, 82(11): 2259-2273.
Du, X., Chen, L., Huang, D., Peng, Z., Zhao, C., Zhang, Y., et al. (2017). Elevated apoptosis in the liver of dairy cows with ketosis. Cellular Physiology and Biochemistry, 43(2): 568-578.
El-Bahr, S.M. and El-Deeb, W.M. (2017). Oxidative stress and cardiac biomarkers in lambs affected with enzootic ataxia: the diagnostic and prognostic significance. Veterinarski Arhiv, 87(3): 259-271.
El-Deeb, W.M. and Younis, E.E. (2009). Clinical and biochemical studies on Theileria annulata in Egyptian buffaloes (Bubalus bubalis) with particular orientation to oxidative stress and ketosis relationship. Veterinary Parasitology, 164(2-4): 301-305.
Feldstein, A.E., Werneburg, N.W., Canbay, A., Guicciardi, M.E., Bronk, S.F., Rydzewski, R., et al. (2004). Free fatty acids promote hepatic lipotoxicity by stimulating TNFα expression via a lysosomal pathway. Hepatology, 40(1): 185-194.
Fiore, F., Spissu, N., Sechi, S. and Coccom, R. (2019). Evaluation of oxidative stress in dairy cows with left displacement of abomasum. Animal, 9(11): 966.
Galvão, K.N., Flaminio, M.J.B.F., Brittin, S.B., Sper, R., Fraga, M., Caixeta, L., et al. (2010). Association between uterine disease and indicators of neutrophil and systemic energy status in lactating Holstein cows. Journal of Dairy Science, 93(7): 2926-2937.
González, F.D., Muiño, R., Pereira, V., Campos, R. and Benedito, J.L. (2011). Relationship among blood indicators of lipomobilization and hepatic function during early lactation in high-yielding dairy cows. Journal of Veterinary Science, 12(3): 251-255.
Grummer, R.R. (1995). Impact of changes in organic nutrient metabolism on feeding the transition dairy cow. Journal of Animal Science, 73(9): 2820-2833.
Hammon, D., Evjen, I.M., Dhiman, T.R., Goff, J.P. and Walters, L.J. (2006). Neutrophil function and energy status in Holstein cows with uterine health disorders. Veterinary Immunology and Immunopathology, 113(1-2): 21-29.
Hayden, M.S. and Ghosh, S. (2008). Shared principles in NF-κB signaling. Cell, 132(3): 344-362.
Hayden, M.S., West, A.P. and Ghosh, S. (2006). NF-κB and the immune response. Oncogene, 25(51): 6758-6780.
Herdt, T.H. (2000). Ruminant adaptation to negative energy balance: Influences on the etiology of ketosis and fatty liver. Veterinary Clinics of North America: Food Animal Practice, 16(2): 215-230.
Hybertson, B.M., Gao, B., Bose, S.K. and McCord, J.M. (2011). Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Molecular Aspects of Medicine, 32(4-6): 234-246.
Ji, L.L., Gomez-Cabera, M.C. and Vina, J. (2006). Exercise and hormesis. Annals of the New York Academy of Sciences, 1067(1): 425-435.
LeBlanc, S.J., Osawa, T. and Dubuc, J. (2011). Reproductive tract defense and disease in postpartum dairy cows. Theriogenology, 76(9): 1610-1618.
Leopold, J. A. and Loscalzo, J. (2009). Oxidative risk for atherothrombotic cardiovascular disease. Free Radical Biology and Medicine, 47(12): 1673-1706.
Li, X., Chen, H., Lei, L., Liu, J., Guan, Y., Liu, Z., et al. (2013). Non-esterified fatty acids activate the AMP-activated protein kinase signaling pathway to regulate lipid metabolism in bovine hepatocytes. Cell Biochemistry and Biophysics, 67(3): 1157-1169.
Li, Y., Ding, H.Y., Wang, X.C., Feng, S.B., Li, X.B., Wang, Z., et al. (2016). An association between the level of oxidative stress and the concentrations of NEFA and BHBA in the plasma of ketotic dairy cows. Journal of Animal Physiology and Animal Nutrition, 100(5): 844-851.
Liguori, I., Russo, G., Curcio, F., Bulli, G., Aran, L., Della-Morte, D., et al. (2018). Oxidative stress, aging, and diseases. Clinical Interventions in Aging, 13: 757-772.
Liu, T., Zhang, L., Joo, D. and Sun, S.C. (2017). NF-κB signaling in inflammation. Signal Transduction and Targeted Therapy, 2: 17023.
Mezzetti, M., Cattaneo, L., Maria Passamonti, M., Lopreiato, V., Minuti, A. and Trevisi, E. (2021). The Transition Period Updated: A Review of the New Insights into the Adaptation of Dairy Cows to the New Lactation. Dairy, 2(4): 617-636.
Morgan, M.J. and Liu, Z.G. (2011). Crosstalk of reactive oxygen species and NF-κB signaling. Cell Research, 21(1): 103-115.
Nelson, D.L., Cox, M.M. and Lehninger, A.L. (2005). Principles of biochemistry. 4th ed., USA: New York, Freeman, pp: 600-622.
Niu, Q., Cao, M., Chen, S., Zhao,Y., Li, C. and Zhou, X. (2019). Effective and economical column- based method for RNA isolation from animal cells. Biotechnology Letters, 41(8-9): 915-920.
Ospina, P.A., Nydam, D.V., Stokol, T. and Overton, T.R. (2010). Evaluation of nonesterified fatty acids and beta-hydroxybutyrate in transition dairy cattle in the northeastern United States: critical thresholds for prediction of clinical diseases. Journal of Dairy Science, 93(4): 546-554.
Pedernera, M., Celi, P., García, S.C., Salvin, E.H., Barchia, I. and Fulkerson, W.J. (2010). Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. The Veterinary Journal, 186(3): 352-357.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic acids Research, 29(9): 45-49.
Puchalska, P. and Crawford, P.A. (2017). Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metabolism, 25(2): 262-284.
Puppel, K., Gołębiewski, M., Solarczyk, P., Grodkowski, G., Slósarz, J., Kunowska-Slósarz, M., et al. (2019). The relationship between plasma β-hydroxybutyric acid and conjugated linoleic acid in milk as a biomarker for early diagnosis of ketosis in postpartum Polish Holstein-Friesian cows. BMC Veterinary Research, 15(1): 367.
Romagnoli, M., Gomez-Cabrera, M.C., Perrelli, M.G., Biasi, F., Pallardo, V.F., Sastre, J., et al. (2010). Xanthine oxidase-induced oxidative stress causes activation of NF-κB and inflammation in the liver of type I diabetic rats. Free Radical Biology and Medicine, 49(2): 171-177.
Sadeghi-nasab, A., Hassanpour, A., Sabaghsaray, H. and Amiri-Sadeghan, S. (2011). Assessment of thyroid hormones, insulin and magnesium in dairy cattle with subclinical ketosis. Journal of Veterinary Clinical Pathology, 5(2): 1149-1159. [In Persian]
Senoh, T., Oikawa, S., Nakada, K., Tagami, T. and Iwasaki, T. (2019). Increased serum malondialdehyde concentration in cows with subclinical ketosis. Journal of Veterinary Medical Science. 81: 817-820.
Shi, X., Li, D., Deng, Q., Li, Y., Sun, G., Yuan, X., et al. (2015). NEFAs activate the oxidative stress-mediated NF-κB signaling pathway to induce inflammatory response in calf hepatocytes. The Journal of Steroid Biochemistry and Molecular Biology, 145(8): 103-112.
Sordillo, L.M. and Aitken, S.L. (2009). Impact of oxidative stress on the health and immune function of dairy cattle. Veterinary Immunology and Immunopathology, 128(1-3): 104-109.
Sordillo, L.M. and Raphael, W. (2013). Significance of metabolic stress, lipid mobilization,and inflammation on transition cow disorders. Veterinary Clinics of North America: Food Animal Practice, 29(2): 267-278.
Stokol, T. and Nydam, D.V. (2006). Effect of hemolysis on nonesterified fatty acid and beta-hydroxybutyrate concentrations in bovine blood. Journal of Veterinary Diagnostic Investigation, 18(5): 466-469.
Suriyasathaporn, W.S., Heuer, C.H., Noordhuizen-Stassen, E.N. and Schukken, Y.H.S. (2000). Hyperketonemia and the impairment of udder defense: a review. Veterinary Research, 31(4): 397-412.
Turk, R., Juretić, D., Gereš, D., Svetina, A., Turk, N. and Flegar-Mestric, Z. (2008). Influence of oxidative stress and metabolic adaptation on PON1 activity and MDA level in transition dairy cows. Animal Reproduction Science, 108(1-2): 98-106.
Turk, R., Juretić, D., Gereš, D., Turk, N., Simeon-Rudolf, V., Rekić, B., et al. (2005). Oxidative stress in dairy cows–serum paraoxonase activity related to hepatomegaly. Croatica Chemica Acta, 78(3): 375-378.
Wang, D., Yu, D., Zhao, C., Xia, C., Xu, C. and Wu, L. (2021). Subclinical ketosis risk prediction in dairy cows based on prepartum metabolic indices. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 73(1): 11-17.
Wankhade, P.R., Manimaran, A., Kumaresan, A., Jeyakumar, S., Ramesha, K.P., Sejian, V., et al. (2017). Metabolic and immunological changes in transition dairy cows: A review. Veterinary World, 10(11): 1367-1377.
Weisberg, S.P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., et al. (2006). CCR2 modulates inflammatory and metabolic effects of high-fat feeding. Journal of Clinical Investigation, 116(1): 115-124.
Wree, A., Schlattjan, M., Bechmann, L.P., Claudel, T., Sowa, J.P., Stojakovic, T., et al. (2014). Adipocyte cell size, free fatty acids and apolipoproteins are associated with non-alcoholic liver injury progression in severely obese patients. Metabolism: Clinical and Experimental, 63(12): 1542-1552.
