The Protective Effects of an Adsorbent against Oxidative Stress in Quails Fed Aflatoxin-Contaminated Diet
Keywords:mycotoxins, lipid peroxidation, free radicals, antioxidants, adsorbent.
Background: Contamination of crops with aflatoxin is considered a serious global threat to food safety, since potent carcinogenic, teratogenic, mutagenic and immunosuppressive effects of aflatoxins are well recognized. Recently, the use of adsorbents has been linked with protective effects against oxidative stress in several diseases. Thus, the aim of this study was to assess the occurrence of oxidative stress in quails (Coturnix coturnix) fed with aflatoxin-contaminated diet, as well as the protective effect of an adsorbent.
Materials, Methods & Results: Twenty-eight quails were divided into four groups (n = 7): diet without additives (control; the group A), diet and adsorbent containing aluminosilicates (the group B), aflatoxin-contaminated diet (200 ppb) (the group C), and aflatoxin-contaminated diet (200 ppb) and adsorbent containing aluminosilicates (the group D). The composition of the adsorbent containing aluminosilicates was 0.3% based on yeast cell wall, silymarin, and bentonite. The animals received feed and water ad libitum during 20 days. At the end of the experimental period, total blood was collected by cardiac puncture in tubes without anticoagulant to obtain serum (centrifuged at 3500 g during 10 min) for later determination of biochemical parameters. The liver was placed in a solution of Tris–HCl 10 mM, pH 7.4 for TBARS (Thiobarbituric acid reactive substances), ROS (Reactive oxygen species), SOD (Superoxide dismutase) and CAT (Catalase) analysis. The hepatic tissue was gently homogenized in a glass potter in specific buffer, homogenated, and centrifuged at 10.000 g at 4ºC for 10 min to yield a supernatant (S1) used for analyses. Homogenate aliquots were stored at -80°C until utilization. Fragments of liver and intestine (5 cm) were collected for histopathological analyses. Between days 15 to 20 of the experiment, group C quails showed clinical signs, such as apathy, creepy feathers and reduced feed intake. At day 20 of experiment, macroscopically, the liver of quails belonging to the group C showed greenish yellow color differently from the other groups. Microscopically, no alterations were observed in the liver of animals in groups A and B. Severe diffuse microvacuolar degeneration (hydropic) of hepatocytes and small foci of necrosis in the liver were observed in the group C, as observed in the group D, but in a more moderate degree to microvacuolar degeneration. Seric total protein, albumin, globulin and uric acid levels decreased in the group C and D. The levels of alanine aminotransferase (ALT) increased in the group C, and the treatment with adsorbent was able to avoid this increment. Seric and hepatic reactive oxygen species and TBARS increased in the group C, and the treatment with adsorbent reduced theses parameters in the group D. Catalase (CAT) activity decreased, while ALA-D increased in the group C. The treatment with adsorbent was able to prevent CAT activity decrease, but it did not prevent the increase in ALA-D activity.
Discussion: Aflatoxins are considered one of the most important problems in poultry production causing high economic losses to producers. In this study, the use of adsorbent showed a protective effect to hepatic tissue, minimizing histopathological lesions, as well as by preventing lipid peroxidation and exacerbated production of free radicals. Based on this data, aflatoxin intoxication causes hepatic oxidative stress that contributes directly to disease pathogenesis, and the addition of an adsorbent containing 0.3% based on bentonite, yeast cell wall and silymarin may be considered a new approach to prevent cellular and hepatic damage caused by aflatoxins.
Abel S. & Gelderblom W.C.A. 1998. Oxidative damage and fumonisin B1-induced toxicity in primary rat hepatocytes and rat liver in vivo. Toxicology. 131(2): 121-131.
Aebi H. 1984. Catalase in vitro. Method Enzymology. 105(1): 121-126.
Althnaian T. 2016. Gene expression and activities of antioxidant enzymes in kidneys of rats intoxicated with aflatoxin B1. Journal of Biological Sciences. 16(1): 65-71.
Batina P.N., Lopes S.T.A. & Santurio J.M. 2005. Efeitos da adição de montmorilonita sódica na dieta sobre o perfil bioquímico de frangos de corte intoxicados com aflatoxina. Ciência Rural. 35(6): 826-883.
Bradford M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 72(2): 248-254.
Brito V.B., Folmer V., Soares J.C., Silveira I.D. & Rocha J.B. 2007. Long-term sucrose and glucose consumption decreases the delta-aminolevulinate dehydratase activity in mice. Nutrition. 23(6): 818-826.
Cardozo S.V., Cardozo T.S.F., Teixeira Filho W.L., Ferreira A.M.R. & Lopes C.W.G. 2011. Alterações histopatológicas cardíacas em codornas japonesas (Coturnix japonica) intoxicadas experimentalmente com dose sub-letal de aflatoxina. Revista Brasileira de Medicina Veterinaria. 33(2): 210-214.
Chen J., Chen K., Yuan S., Peng X., Fang J., Wang F., Cui H., Chen Z., Yuan J. & Geng Y. 2013. Effects of aflatoxin B1 on oxidative stress markers and apoptosis of spleens in broilers. Toxicology and Industrial Health. 2013(1): 1-7.
Eraslan G., Liman B.C., Guclu B.K., Atasever A., Koc A.N. & Beyaz L. 2004. Evaluation of aflatoxin toxicity in japanese quails given various doses of hydrated sodium calcium aluminosilicate. Bulletin of the Veterinary Institute in Pulawy. 48(5): 511-517.
El-Bahr S.M. 2015. Effect of curcumin on hepatic antioxidant enzymes activities and gene expressions in rats intoxicated with aflatoxin B1. Phytotherapy Research. 29(1): 134-140.
Franciscato C., Lopes S.T.A., Santurio J.M., Wolkmer P., Maciel R.M., Paula M.T., Garmatz B.C. & Costa M.M. 2006. Concentrações séricas de minerais e funções hepática e renal de frangos intoxicados com aflatoxina e tratados com montmorilonita sódica. Pesquisa Agropecuária Brasileira. 41(8): 1573-1577.
Halliwell B. & Gutteridge J.M.C. 2007. Free radicals in biology and medicine. 4th edn. New York: Oxford University Press, 851p.
Herzallah S.M. 2013. Aflatoxin b1 residues in eggs and flesh of laying hens fed aflatoxin b1 contaminated diet. American Journal of Agricultural and Biological Sciences. 8(1): 156-161.
Ibrahim Q.Q. 2013. Histopathological study of quails liver experimentally induced by aflatoxin. Brazilian Journal of Veterinary Research and Animal Science. 12(1): 116-127.
Jentzsch A.M., Bachmann H., Fürst P. & Biesalski H.K. 1996. Improved analysis of malondialdehyde in human body fluids. Free Radical Biology & Medicine. 20(2): 251- 256.
Kasmani F.B., Torshizi M.A.K. Allameh A. & Shariatmadari F. 2012. A novel aflatoxin-binding Bacillus probiotic: Performance, serum biochemistry, and immunological parameters in Japanese quail. Poultry Science. 91(12): 18461853.
Ledoux D.R., Rottinghaus G.E., Bermudez A.J. & Alonso-Debolt M. 1998. Efficacy of a hydrated sodium calcium aluminosilicate to ameliorate the toxic effects of aflatoxin in broiler chicks. Poultry Science. 77(2): 204-210.
Madheswaran R., Balachandran C. & Manohar B.M. 2004. Influence of dietary culture material containing aflatoxin and T2 toxin on certain serum biochemical constituents in Japanese quail. Mycopathologia. 158(3): 337-341.
Mary V.S., Theumer M.G., Arias S.L. & Rubinstein H.R. 2012. Reactive oxygen species sources and biomolecular oxidative damage induced by aflatoxin B1 and fumonisin B1 in rat spleen mononuclear cells. Toxicology. 302(2): 299307.
Misra H.P. & Fridovich I. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry. 247(12): 3170-3175.
1Muller F.L., Lustgarten M.S., Jang Y., Richardson A. & Remmen H.V. 2007. Trends in oxidative aging theories. Free Radical Biology & Medicine. 43(5): 477-503.
Nazar F.N., Magnoli A.P., Dalcero A.M. & Marin R.H. 2012. Effect of feed contamination with aflatoxin B1 and administration of exogenous corticosterone on Japanese quail biochemical and immunological parameters. Poultry Science. 91(1): 47-54.
Nelson D.P. & Kiesow L.A. 1972. Entalpy of the composition of hydrogen peroxide by catalase at 25 ºC. Analytical Biochemistry. 49(4): 474-479.
Ogido R., Oliveira C.A.F., Ledoux D.R., Rottinghaus G.E., Corrêa B., Butkeraitis P., Reis T.A., Gonçales E. & Albuquerque R. 2004. Effects of prolonged administration of aflatoxin B1 and fumonisin B1 in laying Japanese quail. Poultry Science. 83(10): 1953-1958.
Ohkawa H., Ohishi N. & Yagi K. 1978. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry. 95(3): 351-358.
Oliveira C.A.F., Butkeraitis P., Rosmaninho J.F., Guerra J.L., Corrêa B. & Reis T.A. 2004. Alterações hepáticas em codornas japonesas submetidas à intoxicação prolongada por aflatoxina B1. Ciência Rural. 34(2): 213-217.
Ramos A.J. & Hernandez E. 1996. In situ absorption of aflatoxins in rat small intestine. Mycopathologia. 134(1): 27-30.
Rodrigues J.V. & Gomes C.M. 2012. Mechanism of superoxide and hydrogen peroxide generation by human electrontransfer flavoprotein and pathological variants. Free Radical Biology and Medicine. 53(1): 12-19.
Rostagno H.S., Albino L.F.T., Donzele J.L., Gomes P.C., Oliveira R.F., Lopes D.C., Ferreira A.S., Barreto S.L.T. & Euclides R.F. 2011. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. Departamento de Zootecnia. Viçosa: UFV, 252 p.
Santurio J.M., Mallmann C.A., Rosa A.P., Appel G., Heer A., Dageförde S. & Böttcher M. 1999. Effect of sodium bentonite on the performance and blood variables of broiler chickens intoxicated with aflatoxins. Bristh Poultry Science. 40(1): 115-119.
Sassa S. 1998. ALA-D porphyria. Seminars in Liver Disease. 18(1): 95-101.
Souza J.B., Rocha J.B., Nogueira C.W., Borges V.C., Kaizer R.R., Morsch V.M., Dressler V.L., Martins A.F., Flores E.M. & Schetinger M.R. 2007. Delta-aminolevulinate dehydratase (delta ALA-D) activity in diabetes and hypothyroidism. Clinical Biochemistry. 40(2): 321-325.
Tessari E.N.C., Oliveira C.A.F., Cardoso A L.S.P., Ledoux D.R. & Rottinghaus G.E. 2005. Efeitos da aflatoxina B1 e fumonisina B1 sobre os níveis séricos de aspartato amino-transferase e proteína total de frangos de corte. Arquivos do Instituto Biológico. 72(1): 185-189.
Thorpe C.W., Ware G.M. & Pohland A.E. 1982. Determination of aflatoxins by HPLC with a fluorescence detector and using postcolumn derivatization. In: Proceedings of the Fifth International IUPAC Symposium on Mycotoxins and Phycotoxins (Vienna, Austria). pp.52-55.
West S., Wyatt R. D. & Hamilton P.B. 1973. Improved Yield of Aflatoxin by Incremental Increases of Temperature. Applied and Environmental Microbiology. 25(10): 1018-1019.
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