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Role of glutathione redox system on the susceptibility to deoxynivalenol of pheasant (Phasianus colchicus)

  • Fernye, Csaba (Department of Nutrition, Faculty of Agricultural Environmental Sciences, Szent Istvan University) ;
  • Ancsin, Zsolt (Department of Nutrition, Faculty of Agricultural Environmental Sciences, Szent Istvan University) ;
  • Erdelyi, Marta (Department of Nutrition, Faculty of Agricultural Environmental Sciences, Szent Istvan University) ;
  • Mezes, Miklos (Department of Nutrition, Faculty of Agricultural Environmental Sciences, Szent Istvan University) ;
  • Balogh, Krisztian (Department of Nutrition, Faculty of Agricultural Environmental Sciences, Szent Istvan University)
  • Received : 2018.10.12
  • Accepted : 2019.05.30
  • Published : 2020.04.15

Abstract

There are only a few reports on the effects of mycotoxins on pheasant (Phasianus colchicus) and the susceptibility to deoxynivalenol of these birds have never been reported before. The present experiment focuses to investigate the effects of different dietary concentrations of deoxynivalenol on blood plasma protein content, some parameters of lipid peroxidation and glutathione redox system and on the performance of pheasant chicks. A total of 320 1-day-old female pheasants were randomly assigned to four treatment groups fed with a diet contaminated with deoxynivalenol (control, 5.11 mg/kg, 11.68 mg/kg and 16.89 mg/kg). Birds were sacrificed at early (12, 24 and 72 h) and late (1, 2 and 3 weeks) stages of the experiment to demonstrate the oxidative stress-inducing effect of deoxynivalenol. Feed refusal was dose dependent, especially in the last third of the trial, but only minor body weight gain decrease was found. Lipid-peroxidation parameters did not show dose-dependent effect, except in blood plasma during the early stage of the trial. The glutathione redox system, reduced glutathione content and glutathione peroxidase activity, was activated in the liver, but primarily in the blood plasma. Glutathione peroxidase activity has changed parallel with reduced glutathione concentration in all tissues. Comparing our results with literature data, pheasants seem to have the same or higher tolerance to deoxynivalenol than other avian species, and glutathione redox system might contribute in some extent to this tolerance, as effective antioxidant defence against oxidative stress.

Keywords

Acknowledgement

Open access funding provided by Szent Istvan University (SZIE). The research was supported by the EFOP-3.6.3-VEKOP-16-2017-00008 project, co-financed by the European Union and the European Social Fund to CF, KB, MM and ME.

References

  1. Grove JF (1988) Non-macrocyclic trichothecenes. Nat Prod Rep 5:187-209 https://doi.org/10.1039/NP9880500187
  2. Grove JF (2000) Non-macrocyclic trichothecenes (Part 2). Prog Chem Org Nat Prod 69:1-70
  3. IPCS (1990) Environmental health criteria 105. Selected mycotoxins WHO, Vammala. II: Trichothecenes. pp 71-164
  4. CAST (2003) Mycotoxins: risks in plant, animal and human systems. Task force report no. 139. Council for Agriculture, Science and Technology, Ames, IA, pp 64-65
  5. Carter CJ, Cannon M (1977) Structural requirements for the inhibitory action of 12, 13-epoxytrichothecenes on protein synthesis in eukaryotes. Biochem J 166:399-409 https://doi.org/10.1042/bj1660399
  6. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497-516 https://doi.org/10.1128/CMR.16.3.497-516.2003
  7. Payros D, Alassane-Kpembi I, Pierron A, Loiseau N, Pinton P, Oswald IP (2016) Toxicology of deoxynivalenol and its acetylated and modified forms. Arch Toxicol 90:2931-2957 https://doi.org/10.1007/s00204-016-1826-4
  8. Friend DW, Trenholm HL, Elliot JI, Thompson BK, Hartin KE (1982) Effects of feeding vomitoxin-contaminated wheat to pigs. Can J Anim Sci 65:1211-1222
  9. Kubena LF, Swanson SP, Harvey RB, Fletcher OJ, Rowe LD, Phillips TD (1985) Effects of deoxynivalenol (vomitoxin)-contaminated wheat to growing chicks. Poult Sci 64:1649-1655 https://doi.org/10.3382/ps.0641649
  10. Kubena LF, Harvey RB, Corrier DE, Phillips TD, Huff WE (1987) Effects of feeding deoxynivalenol (DON, vomitoxin)- contaminated wheat to female white leghorn chickens from day old through egg production. Poult Sci 66:1612-1618 https://doi.org/10.3382/ps.0661612
  11. Cote LM, Dahlem AM, Yoshizawa T, Swanson SP, Buck WB (1986) Excretion of deoxynivalenol and its metabolite in milk, urine and feces of lactating dairy cow. J Dairy Sci 69:2416-2423 https://doi.org/10.3168/jds.s0022-0302(86)80681-6
  12. Huff WE, Kubena LF, Harvey RB, Hagler WM Jr, Swanson SP, Phillips TD, Creger CR (1986) Individual and combined effects of aflatoxin and deoxynivalenol (DON, vomitoxin) in broiler chickens. Poult Sci 65:1291-1298 https://doi.org/10.3382/ps.0651291
  13. Kubena LF, Harvey RB (1988) Response of growing leghorn chicks to deoxynivalenol-contaminated wheat. Poult Sci 67:1778-1780 https://doi.org/10.3382/ps.0671778
  14. Moran ET Jr, Hunter B, Ferket P, Young LG, McGirr LG (1982) High tolerance of broilers to vomitoxin from corn infected with Fusarium graminearum. Poult Sci 61:1828-1831 https://doi.org/10.3382/ps.0611828
  15. Harvey RB, Kubena LF, Huff WE, Elissalde MH, Phillips TD (1991) Hematologic and immunologic toxicity of deoxynivalenol (DON)-contaminated diets to growing chickens. Bull Environ Contam Toxicol 46:410-416 https://doi.org/10.1007/BF01688940
  16. Pestka JJ (2007) Deoxynivalenol: toxicity mechanisms and animal health risk. Anim Feed Sci Technol 137:283-298 https://doi.org/10.1016/j.anifeedsci.2007.06.006
  17. Dvorska JE, Pappas AC, Karadas F, Speake BK, Surai PF (2007) Protective effect of modified glucomannans and organic selenium against antioxidant depletion in the chicken liver due to T-2 toxincontaminated feed consumption. Comp Biochem Physiol C Toxicol Pharmacol 145:582-587 https://doi.org/10.1016/j.cbpc.2007.02.005
  18. Ruff MD, Huff WE, Wilkins GC (1990) Characterization of the toxicity of the mycotoxins, aflatoxin, ochratoxin, and T-2 toxin in game birds. I: chukar partridge. Avian Dis 34:717-720 https://doi.org/10.2307/1591269
  19. Huff WE, Ruff MD, Chute MB (1992) Characterization of the toxicity of the mycotoxins, aflatoxin, ochratoxin, and T-2 toxin in game birds. II: ringneck pheasant. Avian Dis 36:30-33 https://doi.org/10.2307/1591710
  20. Fernye C, Ancsin Z, Bocsai A, Balogh K, Mezes M, Erdelyi M (2018) Role of glutathione redox system on the T-2 toxin tolerance of pheasant (Phasianus colchicus). Toxicol Res 34:249-257 https://doi.org/10.5487/TR.2018.34.3.249
  21. Ruff MD, Huff WE, Wilkins GC (1992) Characterization of the toxicity of the mycotoxins, aflatoxin, ochratoxin, and T-2 toxin in game birds. III: bobwhite and Japanese quail. Avian Dis 36:34-39 https://doi.org/10.2307/1591711
  22. Neiger RD, Johnson TJ, Hurley DJ, Higgins KF, Rottinghaus GE, Stahr H (1994) The short-term effect of low concentrations of dietary aflatoxin and T-2 toxin on Mallard ducklings. Avian Dis 38:738-743 https://doi.org/10.2307/1592109
  23. Boston S, Wobeser G, Gillespie M (1996) Consumption of deoxynivalenol-contaminated wheat by mallard ducks under experimental conditions. J Wildl Dis 32:17-22 https://doi.org/10.7589/0090-3558-32.1.17
  24. Fodor J, Nemeth M, Kametler L, Posa R, Kovacs M, Horn P (2006) Novel methods of Fusarium toxins' production for toxicological experiments. Acta Agrar Kvar 10:277-285
  25. Pussemier L, Pierard JY, Anselme M, Tangni EK, Motte JC, Larondelle Y (2006) Development and application of analytical methods for the determination of mycotoxins in organic and conventional wheat. Food Addit Contam 23:1208-1218 https://doi.org/10.1080/02652030600699312
  26. Prelusky DB, Trenholm HL, Hamilton RMG, Miller JD (1987) Transmission of (14C) deoxynivalenol to eggs following oral administration to laying hens. J Agric Food Chem 35:182-186 https://doi.org/10.1021/jf00074a004
  27. Xu L, Eicher SD, Apllegate TJ (2011) Effects of increasing dietary concentration of corn naturally contaminated with deoxynivalenol on broiler and turkey poult performance and response to lipopolysaccharide. Poult Sci 90:2766-2774 https://doi.org/10.3382/ps.2011-01654
  28. AOAC (1984) Official methods of analysis 28054 B, 14th edn. Arlington, USA
  29. Placer ZA, Cushman LL, Johnson BC (1966) Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical systems. Anal Biochem 16:31
  30. Mihara M, Uchiyama M, Fukuzawa K (1980) Thiobarbituric acid value of fresh homogenate of rat as parameter of lipid peroxidation in ageing, CCl4 intoxication and vitamin E deficiency. Biochem Med 23:302-311 https://doi.org/10.1016/0006-2944(80)90040-X
  31. Sedlak I, Lindsay RH (1968) Estimation of total, protein-bound and non-protein sulfhydryl groups in tissues with Ellmann's reagent. Anal Biochem 25:192-205 https://doi.org/10.1016/0003-2697(68)90092-4
  32. Lawrence R, Burk R (1978) Species, tissue and subcellular distribution of non Se-dependent glutathione peroxidase activity. J Nutr 108:211-215 https://doi.org/10.1093/jn/108.2.211
  33. Weichselbaum TE (1948) An accurate and rapid method for the determination of protein in small amounts of serum and plasma. Am J Clin Pathol 16:40-43 https://doi.org/10.1093/ajcp/16.3_ts.40
  34. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275 https://doi.org/10.1016/S0021-9258(19)52451-6
  35. Harvey RB, Kubena LF, Rottinghaus GE, Turk JR, Caper HH, Buckley SA (1997) Moniliformin from Fusarium fujikuroi culture material and deoxynivalenol from naturally contaminated wheat incorporated into diets of broiler chicks. Avian Dis 41:957-963 https://doi.org/10.2307/1592352
  36. Kubena LF, Huff WE, Harvey RB, Corrier DE, Phillips TD, Creger CR (1988) Influence of ochratoxin A and deoxynivalenol on growing broiler chicks. Poult Sci 67:253-260 https://doi.org/10.3382/ps.0670253
  37. Keshavarz K (1993) Corn contaminated with deoxynivalenol: effects on performance of poultry. J Appl Poult Res 2:43-50 https://doi.org/10.1093/japr/2.1.43
  38. Hulan HW, Proudfoot FG (1982) Effects of feeding vomitoxin contaminated wheat on the performance of broiler chickens. Poult Sci 61:1653-1659 https://doi.org/10.3382/ps.0611653
  39. Danicke S, Matthes S, Halle I, Ueberschar KH, Doll S, Valenta H (2003) Effects of graded levels of Fusarium toxin-contaminated wheat and of a detoxifying agent in broiler diets on performance, nutrient digestibility and blood chemical parameters. Br Poult Sci 44:113-126 https://doi.org/10.1080/0007166031000085300
  40. Kiessling KH (1986) Biochemical mechanism of action of mycotoxins. Pure Appl Chem 58:327-338 https://doi.org/10.1351/pac198658020327
  41. Faixova Z, Faix S, Borutova R, Leng L (2007) Efficacy of dietary selenium to counteract toxicity of deoxynivalenol in growing chicken. Acta Vet Brno 76:349-356 https://doi.org/10.2754/avb200776030349
  42. Smith TK (1992) Recent advances in the understanding of Fusarium trichothecene mycotoxicoses. J Anim Sci 70:3989-3993 https://doi.org/10.2527/1992.70123989x