Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T03:25:17.801Z Has data issue: false hasContentIssue false

Effect of dioxin exposure on several indices of blood redox status in lactating buffalo cows

Published online by Cambridge University Press:  04 March 2011

Maria Stefania Spagnuolo*
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
Fiorella Sarubbi
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
Cristina Rossetti
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
Giuseppe Grazioli
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
Giulia Pia Di Meo
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
Leopoldo Iannuzzi
Affiliation:
National Research Council (CNR), Institute of Animal Production Systems in Mediterranean Environments (ISPAAM), Naples, Italy
*
*For correspondence; e-mail: [email protected]

Abstract

Dioxins are lipophilic compounds with a small molecular weight and are highly persistent, bioaccumulative and toxic. Dioxin detoxification is associated with an increased production of reactive oxygen species (ROS). In physiological conditions the body is protected against ROS and their toxic products by a wide range of antioxidant systems. We hypothesize that the imbalance between ROS production, associated with dioxin exposure, and the antioxidant defence capacity, may lead to oxidative stress, with consequent increased consumption of antioxidants and accumulation of toxic compounds in blood and tissues. The objective of this study was to evaluate the effect of exposure to dioxins on the plasma redox status of lactating buffalo cows. To this aim, the major liposoluble (retinol and α-tocopherol) and water-soluble (ascorbate) antioxidants, the superoxide dismutase (SOD) and glutathione peroxidase (GPx) activity, the total antioxidant capacity (TAC), as well as specific protein oxidation markers (protein bound carbonyls and nitro-tyrosine) and lipid oxidation markers (hydroperoxides), were chosen as indices of blood redox status. The concentration of antioxidants, protein-bound carbonyls (PC), nitro-tyrosine (N-Tyr), and hydroperoxides (LPO), the SOD and GPx activity, and the TAC were measured in plasma samples obtained from buffalo cows exposed to environmental levels of dioxins higher (n=21, group A) or lower (n=29; group B) than those permitted. Plasma titres of antioxidants, as measured by HPLC, and the total antioxidant capacity, as measured by trolox equivalents capacity, were higher in group B than in A. Similarly, SOD and GPx activities were higher in group B than in A. Conversely, plasma levels of PC, N-Tyr and LPO, as measured by ELISA, were higher in group A than in B. Our results suggest that exposure to dioxins impairs the plasma antioxidant defence system of lactating buffalo cows, and that metabolic processes associated with dioxin detoxification might induce or enhance oxidation of protein and lipids. This adverse effect on blood redox status might have negative implications for animal health and reproduction, and might compromise animal welfare.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Azzi, A & Stocker, A 2000 Vitamin E: non-antioxidant roles. Progress in Lipid Research 39 231255CrossRefGoogle ScholarPubMed
Beckman, JS & Koppenol, WH 1996 Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and the ugly. American Journal of Physiology 271 C1424C1437CrossRefGoogle Scholar
Berlett, BS & Stadtman, ER 1997 Protein oxidation in aging, disease, and oxidative stress. Journal of Biological Chemistry 272 2031320316CrossRefGoogle ScholarPubMed
Buss, H, Chan, TP, Sluis, KB, Domigan, NM & Winterbourn, CC 1997 Protein carbonyl measurement by a sensitive ELISA method. Free Radical Biology and Medicine 23 361366CrossRefGoogle ScholarPubMed
Faustman, C, Chan, WKM, Schaefer, DM & Havens, A 1998 Beef color update: the role for Vitamin E. Journal of Animal Science 76 10191026CrossRefGoogle ScholarPubMed
Frei, B, England, L & Ames, BN 1989 Ascorbate is an outstanding antioxidant in human blood plasma. Proceedings of the National Academy of Sciences USA 86 63776381CrossRefGoogle ScholarPubMed
Galli, F & Azzi, A 2010 Present trends in vitamin E research. Biofactors 36 3342CrossRefGoogle ScholarPubMed
Grimble, RF 1990 Nutrition and cytokine action. Nutrition Research Reviews 3 193210CrossRefGoogle ScholarPubMed
Halliwell, B 1994 Free radicals and antioxidants: a personal view. Nutrition Reviews 52 253265CrossRefGoogle ScholarPubMed
Halliwell, B 1997 What nitrates tyrosine? Is nitrotyrosine specific as a biomarker of peroxynitrite formation in vivo? FEBS Letters 411 157160CrossRefGoogle ScholarPubMed
Halliwell, B & Gutteridge, JMC 2000 Free radicals, other reactive species and disease. In Free Radicals in Biology and Medicine (Eds Halliwell, B & Gutteridge, JMC) pp 617783. Oxford, UK: Oxford University PressGoogle Scholar
Herdt, TH & Stowe, HD 1991 Fat-soluble vitamin nutrition for dairy cattle. Veterinary Clinics of North America. Food Animal Practice 7 391415CrossRefGoogle ScholarPubMed
INRA 1988 Alimentation and Nutrition of Bovines and Caprines (Ed. Jarrige, R). Institute Nacionale de la Recherche Agronomique, Paris, FranceGoogle Scholar
Jialal, I, Devaraj, S & Kaul, N 2001 The effect of alpha-tocopherol on monocyte proatherogenic activity. Journal of Nutrition 131 389394CrossRefGoogle ScholarPubMed
Kristal, BS & Yu, BP 1992 An emerging hypothesis: synergistic induction of aging by free radicals and Maillard reactions. Journal of Gerontology 47B 107114CrossRefGoogle Scholar
Mallard, BA, Dekkers, JC, Ireland, MJ, Leslie, KE, Sharif, S, Vankampen, CL, Wagter, L & Wilkie, BN 1998 Alteration in immune responsiveness during the peripartum period and its ramification on dairy cow and calf health. Journal of Dairy Science 81 585–95CrossRefGoogle ScholarPubMed
Mandal, PK 2005 Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. Journal of Comparative Physiology B 175 221230CrossRefGoogle ScholarPubMed
Matsumura, F 2003 On the significance of the role of cellular stress response reactions in the toxic actions of dioxin. Biochemical Pharmacology 66 527540CrossRefGoogle ScholarPubMed
Miller, JK, Brzezinska-Slebodzinska, E & Madsen, FC 1993 Oxidative stress, antioxidants, and animal function. Journal of Dairy Science 76 28122823CrossRefGoogle ScholarPubMed
Miller, JK, Mueller, FJ, Thomas, DG & Madsen, FC 1991 Vitamin E and reproduction in dairy cows. In Vitamin E in Animal Nutrition and Management (Ed. Coelho, MB) p 159. Parsippany NJ, USA: BASFGoogle Scholar
Miller, NJ, Rice-Evans, CA, Davies, MJ, Gopinathan, V & Milner, A 1993 A novel method for measuring antioxidant capacity and its application to monitoring antioxidant status in premature neonates. Clinical Sciences 84 407412Google ScholarPubMed
Parke, A & Parke, DV 1995 The pathogenesis of inflammatory disease: surgical shock and multiple system organ failure. Immunopharmacology 3 149168Google Scholar
Shertzer, HG, Vasiliou, V, Liu, RM, Tabor, MW & Nebert, DW 1995 Enzyme induction by l-buthionine (S,R)-sulfoximine in cultured mouse hepatoma cells. Chemical Research in Toxicology 8 431436CrossRefGoogle ScholarPubMed
Slezak, BP, Hatch, GE, DeVito, MJ, Diliberto, JJ, Slade, R, Crissman, K, Hassoun, E & Birnbaum, LS 2000 Oxidative stress in female B6C3F1 mice following acute and subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicological Sciences 54 390398CrossRefGoogle ScholarPubMed
Smith, KL, Harrison, JH, Hancock, DD, Todhunter, DA & Conrad, HR 1984 Effect of vitamin E and selenium supplementation on incidence of clinical mastitis and duration of clinical symptoms. Journal of Dairy Science 67 12931300CrossRefGoogle ScholarPubMed
Spagnuolo, MS, Cigliano, L, Balestrieri, M, Porta, A & Abrescia, P 2001 Synthesis of ascorbate and urate in the ovary of water buffalo. Free Radicals Research 35 233243CrossRefGoogle ScholarPubMed
Spagnuolo, MS, Cigliano, L, Sarubbi, F, Polimeno, F, Ferrara, L, Bertoni, G & Abrescia, P 2003 The accumulation of alpha-tocopherol and retinol in the milk of water buffalo is correlated with the plasma levels of triiodothyronine. Biofactors 19 197209CrossRefGoogle ScholarPubMed
Uchida, K & Stadtman, ER 1993 Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. Journal of Biological Chemistry 268 63886393CrossRefGoogle ScholarPubMed
Van Soest, PJ, Robertson, JB & Lewis, BA 1991 Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74 35833597CrossRefGoogle ScholarPubMed
Zhao, W & Ramos, KS 1998 Modulation of hepatocyte gene expression by the carcinogen benzo[a]pyrene. Toxicology In Vitro 12 175182CrossRefGoogle Scholar