Comparative Biochemistry and Physiology, Part C 145 (2007) 582 587 www.elsevier.

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Protective effect of modified glucomannans and organic selenium against antioxidant depletion in the chicken liver due to T-2 toxin-contaminated feed consumption
Julia E. Dvorska a , Athanasios C. Pappas b , Filiz Karadas c , Brian K. Speake b , Peter F. Surai b,d,
c

Sumy National University, Sumy, Ukraine Avian Science Research Centre, SAC, Scotland, UK Department of Animal Science, Faculty of Agriculture, University of Yuzuncu Yil, Van, Turkey d Department of Nutrition, Sant-Istvan University, Godollo, Hungary
b

Received 17 September 2006; received in revised form 4 February 2007; accepted 4 February 2007 Available online 12 February 2007

Abstract The aim of this work was to assess the effect of T-2 toxin on the antioxidant status of the chicken and to study possible protective effects of modified glucomannan (Mycosorb) and organic selenium (Sel-Plex). Inclusion of T-2 toxin in the chickens' diet (8.1 mg/kg for 21 days) was associated with significant decreases in the concentrations of selenium (Se)(by 32.2%), -tocopherol (by 41.4%), total carotenoids (by 56.5%), ascorbic acid (by 43.5%) and reduced glutathione (by 56.3%) in the liver, as well as a decrease in the hepatic activity of Se-dependent glutathione peroxidase (Se-GSH-Px) (by 36.8%). However, inclusion of modified glucomannans into the T-2 toxin-contaminated diet provided a partial protection against the detrimental effects of the mycotoxin on the antioxidant defences in the chicken liver. For example, the Se concentration in the liver was restored completely, although the Se-GSH-Px activity in the liver increased to only 81% of its control value. These protective effects of modified glucomannas were associated with a 45% reduction of lipid peroxidation in the liver in comparison to the effects of T-2 toxin alone. A combination of modified glucomannas with organic Se was shown to provide further protection against toxin-induced antioxidant depletion and lipid peroxidation in the chicken liver. Thus, the data clearly indicate a major protective effect of the mycotoxin-binder in combination with organic Se against the detrimental consequences of T-2 toxin-contaminated feed consumption by growing chickens. 2007 Elsevier Inc. All rights reserved.
Keywords: Antioxidants; Chicken; Glucomannan; Mycotoxin; Peroxidation; Selenium; T-2 toxin

1. Introduction Mycotoxin contamination of various feed and food commodities is a global problem (Schollenberger et al., 2006). More than 300 mycotoxins have been characterised (Fink-Gremmels, 1999) and this number is growing quickly. The trichothecene group of mycotoxins accounts for over one hundred fungal metabolites, of which T-2 toxin, produced by the Fusarium fungus, was the first to be studied (Leeson et al., 1995; Bondy and Pestka, 2000). The adverse effects of trichothecene toxins on animal health is expressed in a diverse range of symptoms
Corresponding author. Avian Science Research Centre, SAC, Scotland, UK. Tel.: +44 7808812073; fax: +44 1780 764505. E-mail address: psurai@alltech.com (P.F. Surai). 1532-0456/$ - see front matter 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpc.2007.02.005

including skin lesions, immunosuppression, hepatotoxicity, nephrotoxicity, neurotoxicity, genotoxicity and even death (Hollinger and Ekperigin, 1999). Recently four major molecular mechanisms of mycotoxin toxicity, including T-2 toxin, were suggested (Surai, 2006): 1) inhibition of DNA, RNA and protein synthesis simultaneously with direct damage to DNA; 2) promotion of lipid peroxidation; 3) promotion of apoptosis and 4) effect on gene expression. While a variety of different strategies to combat mycotoxicosis have been developed, the most promising are based on the addition of adsorbents to contaminated feed. The adsorbent material selectively binds mycotoxins during digestion, preventing their absorption from the gastrointestinal tract, thereby decreasing the toxic effects (Devegowda et al., 1998; Chowdhury and Smith, 2005; Karaman et al., 2005). Of several different

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adsorbent additives studied, an esterified glucan (Mycosorb, Alltech, Inc. USA) has been shown to be the most effective (Devegowda et al., 1998; Devegowda and Murthy, 2005). The aim of the present work was two-fold. The first was to study the dietary effect of T-2 toxin on the antioxidant systems of the liver in chickens. The second was to evaluate the protective properties of the mycotoxin-adsorbent additive, Mycosorb, and its combination with organic selenium (Se) (Sel-Plex, Alltech, Inc. USA) in preventing inhibition of the antioxidant system by T-2 toxin. 2. Materials and methods Eighty female chicks (Gallus gallus, 5-day old) were allocated among 20 pens, each holding 4 birds, with 5 replicate pens for each of the 4 dietary treatments and fed ad libitum. The control group was fed on a basal maize-based commercial diet formulated to meet the NRC (1994) requirements for all nutrients. The experimental groups were fed on the same basal diet with T-2 toxin added (final T-2 toxin concentration was 8.1 mg/kg feed); T-2 toxin (8.1 mg/kg) plus Mycosorb (Mycosorb is a trademark of Alltech. Inc. that has been registered with the U.S. Trademark Office, 1 g/kg feed); T-2 toxin (8.1 mg/kg) plus Mycosorb (1 g/kg) plus Sel-Plex (Sel-Plex is a trademark of Alltech. Inc. that has been registered with the U.S. Trademark Office, 0.3 ppm Se). Temperature and all other environmental conditions were maintained in accordance with existing norms for the facility. After 21 days of feeding all birds were sacrificed by cervical dislocation and samples for biochemical analyses were collected from five chicks (26 days old) having an average body mass for a group in each of the four groups. Samples were stored in liquid nitrogen before analysis. Se was determined by hydride generation atomic fluorescence spectroscopy of an acid digest of the samples. The method used a hydride generator, a fluorescent detector Model 10.033 (PS Analytical Ltd., Kent, UK) fitted with a boosted discharge hollow cathode lamp, and Avalon software (PS Analytical Ltd., Kent, UK) (Pappas et al., 2006). Vitamin E and carotenoid extraction from the liver was performed as previously described (Surai et al., 2001). In brief,
Fig. 2. Effect T-2 toxin, modified glucomannans and organic selenium on SeGSH-Px in the chicken liver, U/mg protein. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b) are significantly (P b 0.05) different.

liver samples (0.20.5 g) were homogenised in 2 ml of 1:1 (v/v) mixture of 5% NaCl solution and ethanol following by addition of 3 ml hexane and further homogenisation for 3 min. After centrifugation, the hexane layer was collected and the extraction was repeated twice. Hexane extracts were combined and evaporated under N2 and the residue was dissolved in 1 ml of methanol:dichloromethane (1:1, v/v), centrifuged and the supernatant was used for vitamins E and carotenoid determination. Vitamin E (-tocopherol) was determined as previously described (Surai and Speake, 1998) using an HPLC system (Shimadzu Liquid Chromatograph, LC-10AD, Japan Spectroscopic Co Ltd. with JASCO Intelligent Spectrofluorometer 821FP) fitted with a Spherisorb, type S30DS2, 3 m C18 reverse phase HPLC column, 15 cm 4.6 mm (Phase Separations Limited, UK). Chromatography was performed using a mobile phase of methanol/water (97:3, v/v) at a flow rate of 1.05 ml/min. Fluorescence detection of tocopherols involved excitation and emission wavelengths of 295 and 330 nm respectively. Standard solutions of -tocopherol in methanol were used for instrument calibration and tocol was used as an internal standard. Carotenoids were determined from the same extracts using the same HPLC system, but fitted with a Spherisorb, type S5NH2 5 m reverse phase HPLC column, 25 cm 4.6 mm (Phase Separations Limited, UK). Chromatography was performed using a mobile phase of methanol/water (97:3, v/v) at a flow rate of 1.5 mL/min. Total carotenoids were detected at 445 nm as a single peak using lutein as a standard (Horak et al., 2002).

Fig. 1. Effect T-2 toxin, modified glucomannans and organic selenium on Se level in chicken liver, ng/g; Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a,b,c) are significantly (P b 0.05) different.

Fig. 3. Effect of T-2 toxin, modified glucomannans and organic selenium in the diet on alpha-tocopherol (g/g) in the liver of chicks fed T-2 toxin. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b) are significantly (P b 0.05) different.

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Fig. 4. Effect of T-2 toxin, modified glucomannans and organic selenium in the diet on carotenoids (g/g) in the liver of chicks fed T-2 toxin. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b, c, d) are significantly (P b 0.05) different.

Fig. 6. Effect of T-2 toxin, modified glucomannans and organic selenium in the diet on GSH (g/g fresh tissue) in the liver of chicks fed T-2 toxin. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b, c) are significantly (P b 0.05) different.

Reduced glutathione was determined using the method of Griffith (1980) by means of the determination of total glutathione following enzymatic recycling with glutathione reductase; oxidized glutathione was determined in the presence of 2vinylpyridine and reduced glutathione was calculated as the difference between total and oxidized glutathione. For glutathione peroxidase (GSH-Px) activity assay, tissue samples were homogenised in 9 vol. of potassium phosphate buffer (0.01M, pH 7.4) at 4 C and the homogenate was centrifuged at 3500 g for 30 min at 4 C. Se-dependent GSHPx activity was measured in aliquots of the supernatant by a coupled reaction with excess glutathione reductase, monitoring the oxidation of NADPH at 340 nm, using H2O2 as substrate. Units of activity are expressed as mol NADPH oxidised/min/ mg supernatant protein. The protein in the supernatant was determined colourimetrically using a kit method (Bio-Rad, Hemel Hempstead, UK). Ascorbic acid was determined by HPLC-based method based on ascorbate oxidation by 2,6-dichlorophenolindophenol and derivatization of dehydroascorbic acid with 4,5-dimethyl-ophenylendiamine with fluorometric detection as previously described (Dvorsaka and Surai, 2001). Tissue susceptibility to lipid peroxidation was determined measuring malondialdehyde (MDA) accumulation as a result of Fe-stimulated lipid peroxidation, as previously described in Dvorska et al. (2002). Results were expressed as g MDA/g of

fresh tissue using 1,1,3,3-tetramethoxypropane as the standard for calibration. Results are presented as means SEM of measurements on tissue samples from five chickens per treatment. Statistical analysis was performed by one-way ANOVA and means were separated using Student's t-test. 3. Results The antioxidant profile for the chicken liver is shown in Figs. 16. Inclusion of T-2 toxin in the chickens' diet was associated with significant decreases of all studied antioxidants in the liver. In particular, the Se concentration decreased by 32.2% (P b 0.05, Fig. 1), Se-GSH-Px by 36.8% (P b 0.05; Fig. 2), tocopherol by 41.4% (P b 0.01, Fig. 3), total carotenoids by 56.5% (P b 0.01, Fig. 4), ascorbic acid by 43.5% (P b 0.05, Fig. 5) and reduced glutathione by 56.3% (P b 0.01; Fig. 6). These changes led to an increased susceptibility of the liver to lipid peroxidation, as indicated by a 3-fold increase in the concentration of MDA (P b 0.001; Fig. 7). Inclusion of modified glucomannans into the T-2 toxincontaminated diet provided a partial protection against the detrimental effects of the mycotoxin on the antioxidant defences in the chicken liver (Figs. 1, 2, 46). In fact, the Se concentration in the liver was restored completely. However, Se-GSH-Px activity in the liver returned to only 81% of its

Fig. 5. Effect of T-2 toxin, modified glucomannans and organic selenium in the diet on ascorbic acid (g/g fresh tissue) in the liver of chicks fed T-2 toxin. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b, c) are significantly (P b 0.05) different.

Fig. 7. Effect of T-2 toxin, modified glucomannans and organic selenium in the diet on lipid peroxidation (MDA, g/g fresh tissue) in the liver of chicks fed T-2 toxin. Means S.E.M. (n = 5) are shown. For comparisons among the groups, values that do not share a common superscript (a, b, c, d) are significantly (P b 0.05) different.

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control value. Furthermore, modified glucomannas were able to restore the concentration of -tocopherol, total carotenoids, ascorbic acid and reduced glutathione to 74.6, 62.6, 72.9 and 67.3% of their values in the control chicken fed on the commercial diet. These changes were associated with a 45% decrease (P b 0.05) of lipid peroxidation in the liver in comparison to the effect of T-2 toxin alone. However, lipid peroxidation was still 67% (P b 0.05) higher in comparison to the values found in the control group without T-2 toxin. A combination of the mycotoxin-binder with organic Se was shown to provide further protection against antioxidant depletion and lipid peroxidation in the liver (Figs. 1, 2, 46). In fact, all antioxidants studied, including Se, Se-GSH-Px, tocopherol, total carotenoids, ascorbic acid and reduced glutathione in the liver in this group were significantly (P b 0.05) higher than those in the group treated with T-2 toxin alone. Furthermore, the -tocopherol level recovered completely and was not different from the control group without T-2 toxin (Fig. 3). At the same time, the Se concentration in the liver of the chickens fed on T-2 toxin and modified glucomannas plus organic selenium was 2-fold higher than that in the control chickens (P b 0.01; Fig. 1). As a result of the antioxidant repletion in the liver its susceptibility to lipid peroxidation further decreased being less than half of that in the T-2 toxin treated chickens (P b 0.01). However, a combination of modified glucomannas and organic selenium was not able to completely prevent an increase in lipid peroxidation in the chicken liver due to T-2 toxin consumption, which remained 26% higher (P b 0.05, Fig. 7) than that in the control group without T-2 toxin. Thus, the data presented above clearly indicated protective effects of the mycotoxin-binder in combination with organic Se against the detrimental consequences of T-2 toxin-contaminated feed consumption by growing chickens. 4. Discussion The main finding of this study is a protective effect of the mycotoxin-binder in combination with organic Se against antioxidant depletion and lipid peroxidation in the chicken liver due to T-2 toxin consumption. It is interesting to mention that a comparatively high dose of T-2 toxin was used in this study and this caused dermatological oral lesions in the chickens within 5 days after the start of T-2 toxin feeding. The toxic effects of T-2 toxin were most likely mediated by oxidative stress resulting from an imbalance between free radical production and antioxidant defences. Indeed, stimulation of lipid peroxidation is considered to be a driving force of T-2 toxin toxicity (Surai, 2006; Surai and Mezes, 2005). Among avian species tested, the most sensitive to T-2 toxicosis were geese, followed by ducks and chickens (Mezes et al., 1999). Leal et al. (1999) found that after 7 days of toxin treatment (1.5 mg T-2 toxin/kg body weight/day) hepatic MDA concentration in male broiler chicks increased by 128%, while glutathione concentration decreased. T-2 toxin fed to chickens at 10 mg/kg feed for 17 days induced DNA fragmentation in chicken spleen leukocytes and decreased significantly the total antioxidant status of the plasma (Frankic et al., 2006). In an

investigation conducted in vitro with the Vero cell line, it was shown that T-2 toxin reduced cell viability correlated to an impairment of macromolecule levels. It also increased MDA formation and induced DNA fragmentation (Bouaziz et al., 2006). However, Hoehler and Marquardt (1996) found that T-2 toxin was not always effective in stimulating lipid peroxidation in chickens. Similarly, T-2 toxin at 2.35 mg/kg feed did not enhance lipid peroxidation in chickens (Weber et al., 2006). These findings could be attributed to differences in dietary composition, levels of antioxidants and mycotoxins in the diet, differences in analytical techniques used or other unidentified factors. At present, it is not clear whether T-2 toxin stimulates lipid peroxidation directly by enhancing free radical production, or the increased susceptibility of tissues to peroxidation is a reflection of a compromised antioxidant system. For the chickens in this experiment, the levels of the primary liver antioxidants (-tocopherol, carotenoids, ascorbic acid and reduced glutathione) were significantly decreased as a result T-2 toxin consumption. Other studies showed similar findings. For example, there was a significant decrease in vitamin E content of mice plasma after the administration of the T-2 toxin (up to 6.25 mg/kg body weight) with the concentrations remaining low for periods as long as 4872 h. The MDA content of liver increased significantly after 2448 h of toxin administration in contrast to the controls (Vila et al., 2002). Similarly, Hoehler and Marquardt (1996) found that the presence of T-2 toxin in the diet decreased the concentration of -tocopherol in chicken liver, while Coffin and Combs (1981) showed that T-2 toxin consistently depressed concentrations of vitamin E in chicken plasma. However, the addition of micelle-promoting compounds (taurocholic, monoolein, and oleic acids) alleviated the reduction of plasma vitamin E, indicating that T-2 toxin interferes with micelle formation during vitamin E absorption. Decreased antioxidant absorption from the diet is just one of the possible mechanisms of antioxidant depletion from the tissues. A prooxidant effect of mycotoxins in many cases could be mediated via changes in reduced glutathione (GSH) concentration. For example, Rizzo et al. (1994) demonstrated that T-2 toxin decreased GSH content in rat liver. Treatment of fasted mice with a single dose of T-2 toxin (1.8 or 2.8 mg/kg body weight) by oral gavage led to marked decrease in hepatic GSH levels (Atroshi et al., 1997). In male broiler chicks, the hepatic GSH concentration decreased after 7 days of treatment (1.5 mg T-2 toxin/kg body weight/day) (Leal et al., 1999). Acute exposure of mice to T-2 toxin (4 mg/kg, s.c.) resulted in a progressive decrease in hepatic GSH content, reaching a minimum 68 h after toxin administration (Fricke and Jorge, 1991). Considering that GSH is responsible for the maintenance of redox status of the cell (Sies, 1999) and therefore participates in regulation of gene expression (Arrigo, 1999), changes in GSH status could be detrimental. This is the first study to show a detrimental effect of T-2 toxin consumption on Se concentration in the chicken liver. This confirms the aforementioned possibility of T-2 toxin compromising nutrient absorption. This could be a result of disturbing antioxidantprooxidant balance in the digestive tract

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(Surai et al., 2004). In fact oxidative stress in the digestive tract can cause GSH depletion and apoptosis of enterocytes (for review see Surai and Dvorska, 2005) leading to malabsorption syndrome long known to be associated with mycotoxin action. It was postulated that the decreased level of vitamin A in the quail liver as a result of T-2 toxin consumption (Dvorska and Surai, 2001) was also a reflection of the decreased intestinal absorption of fat-soluble nutrients. One of the most important mycotoxin actions is their effect on antioxidant enzymes. In this experiment Se-GSH-Px activity in the chicken liver significantly (P b 0.05) decreased due to T-2 toxin consumption. Depending on experimental conditions (species, doses, route and duration of administration, concentrations of other antioxidants etc.), antioxidant enzyme activities can be increased in response to oxidative stress or decreased by direct or indirect action of mycotoxins. For example, oral administration of T-2 mycotoxin to rats (1.25 mg/kg) for 5 days caused a decrease in the activity of liver glutathione-Stransferase (Ahmed and Ram, 1986). In contrast, feeding a single dose of T-2 toxin (2 mg/kg body weight) to rats was associated with increased activities of GSH-shuttle enzymes including GSH-Px, glutathione reductase and glucose-6-phosphate dehydrogenase (Suneja et al., 1989), probably reflecting an adaptive response to oxidative stress. On the other hand, when male rats were given a diet deficient in vitamins C and E and Se and were administered orally a single dose of DON or T-2 toxin, there was a significant decrease in activities of GSH-Px, Catalase, SOD and glutathione reductase (Rizzo et al., 1994). Protective effects of the mycotoxin-binder modified glucomannas against antioxidant depletion due to T-2 toxin (Dvorska and Surai, 2001) or aurofusarin (Dvorska et al., 2003; Dvorska and Surai, 2004) consumption were shown in our previous studies with quail. The protective effect of modified glucomannas in this study was of similar magnitude. Indeed, clinical signs of T-2 toxicity in chickens fed on the diets containing modified glucomannas or its combination with organic selenium were practically absent. The principal finding in the experiment is a further protection provided by organic selenium. Indeed, a protective effect of Se against T-2 toxin was reported previously. For example, when male Wistar rats were fed diets supplemented with Se (0.5 and 2.5 mg/kg) for 6 weeks, signs of intoxication from T-2 toxin were less distinct and mortality caused by T-2 toxin was two times (Kravchenko et al., 1990) or 35 times (Tutelyan et al., 1990) lower compared to the unsupplemented group. The acute lethal toxicity of T-2 toxin was reduced by administration of sodium selenite (Yazdanpanah et al., 1997). Indeed, it is practically impossible to bind all mycotoxins in the feed, since there is a competition in the digestive tract between a mycotoxin absorption on the sorbent or into digestive tract. Therefore those mycotoxins, which are already absorbed, especially if they are in high doses similar to that used in this study, could cause oxidative stress and Se as an integral part of at least 25 selenoproteins (Surai, 2006) can help to deal with overproduction of free radicals. As can be seen from the data presented above, a combination of Mycosorb with organic selenium was associated with the highest Se concentration in the

liver which was responsible for increased expression of Se-GSHPx. It could well be that other selenoprotein expression was also increased, but this question need further investigation. Similar to previous observations (Raju and Devegowda, 2000; Freimund et al., 2003; Reddy et al., 2004; Devegowda and Murthy, 2005), these data clearly demonstrated an opportunity to decrease the detrimental effect of T-2 toxin by natural absorbent (modified glucomannans) in addition to other observations showing protective effect of this absorbent against aflatoxin (Karaman et al., 2005; Devegowda and Murthy, 2005), zearalenone (Yiannikouris et al., 2004,a,b,c), ochratoxin (Raju and Devegowda, 2000) and natural mycotoxin mixture (Chowdhury and Smith, 2005; Swamy et al., 2002; Aravind et al., 2003). However, despite positive effects on the birds, inclusion of Mycosorb or its combination with organic selenium in the chickens' diet was unable to completely prevent the adverse effects of high doses of T-2 toxin on the antioxidant systems of the liver; indicating that not all T-2 toxin was bound and released from the intestine. Therefore a higher level of Mycosorb inclusion or/with additional dietary supplementation of such antioxidants as vitamin E could be the next step in the research related to prevention of the damaging effects of mycotoxins on animals including poultry. References
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