ENVIRONMENT, WELL-BEING, AND BEHAVIOR

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1 ENVIRONMENT, WELL-BEING, AND BEHAVIOR Effect of Addition of a Probiotic Microorganism to Broiler Diets Contaminated with Deoxynivalenol on Performance and Histological Alterations of Intestinal Villi of Broiler Chickens W. A. Awad,* J. Böhm,* E. Razzazi-Fazeli,* K. Ghareeb, and J. Zentek* 1 *Institute of Nutrition, and Institute of Animal Husbandry and Animal Welfare, Department of Veterinary Public Health and Food Science, University of Veterinary Medicine, Veterinärplatz 1, A-1210 Vienna, Austria ABSTRACT An experiment was conducted to study the and relative weights of the gizzard, duodenum, pancreas, effects of deoxynivalenol (DON) on the performance of broilers, organ weights, and intestinal histology and to evaluate the efficacy of a probiotic feed additive (PB, Eubacterium sp.) with the ability to deepoxidize DON. Two hundred seventy-seven 1-d-old broiler chicks were randomly assigned to 1 of the 3 dietary treatments for 6 wk. The dietary treatments were 1) control; 2) artificially contaminated diets with 10 mg of DON/kg of diet; 3) DON-contaminated diets plus probiotic feed additive (DON-PB). The BW and the efficiency of feed utilization were not adversely affected (P > 0.05) by the inclusion of DON in the diets. A slight improvement in feed intake and BW gain over the course of the experiment was observed in broilers fed DON-PB with no change in feed efficiency. The absolute or relative organ weights were not altered (P > 0.05) in broilers fed the diet containing DON compared with controls and the DON-PB group. The absolute liver weights were numerically increased (P < 0.1) for broilers receiving the diet containing DON- PB. There were no significant differences in the absolute heart, and spleen. However, the absolute and relative weights of the jejunum and cecum were increased for DON-PB-fed broilers compared with the controls and DON group. No pathological lesions were found in the gut of birds fed DON-contaminated diets during the feeding trial, but mild intestinal changes were observed. The DON altered small intestinal morphology, especially in the duodenum and jejunum, where villi were shorter and thinner (P < 0.05). The addition of the eubacteria to the DON-contaminated feed of the broilers effectively alleviated the histological alterations caused by DON and led to comparable villus length as in the control group. In conclusion, diets with DON contamination below levels that induce a negative impact on health and performance could affect small intestinal morphology in broilers. The histological alterations caused by DON were reduced by supplementing the DON-containing diets with PB. This indicates that in case of DON contamination of feedstuffs, the addition of PB would be a proper way to counteract the possible effects caused by this mycotoxin. Key words: chicken, deoxynivalenol, microbial feed additive, organ weight, villus histology 2006 Poultry Science 85: INTRODUCTION The presence of mycotoxins in poultry feeds is a significant factor for financial losses to animal industries. Deoxynivalenol (DON) is the most common trichothecene mycotoxin detected globally in contaminated feedstuffs. As a mycotoxin, DON causes losses in livestock production and poses a health problem to livestock and humans consuming contaminated cereal products. The mode of toxic action of DON is the inhibition of protein synthesis and thus affects rapidly dividing cells, such as those of the gastrointestinal tract and immune system (Leeson et al., 1995). This induces susceptibility to dis Poultry Science Association Inc. Received July 19, Accepted December 19, Corresponding author: juergen.zentek@vu-wien.ac.at eases (Bondy and Pestka, 2000). Several researchers reported that broiler chicks could tolerate up to 15 mg of dietary deoxynivalenol/kg from naturally contaminated diets without any adverse effects on BW gain, feed consumption, or feed efficiency (Kubena et al., 1997; Harvey et al., 1997; Leitgeb, et al., 1999, 2000; Awad et al., 2004a,b). Small erosions of the gizzard and proventriculus mucosa, and increased absolute and relative gizzard weights were observed in birds fed a diet containing 82.8 mg of DON/kg for 27 d (Lun et al., 1986). Harvey et al. (1997) and Bergsjo and Kaldhusdal (1994) found no effect on histopathological lesions of organs of broiler chicks fed DON-contaminated diets. Swamy et al. (2004) found that the relative weights of the liver, kidney, spleen, and bursa of Fabricius of broilers were not altered by dietary inclusion of Fusarium-contaminated grains. Hoerr et al. (1981) reported that acute administration of large dosages of diacetoxyscirpenol (2.7 mg/kg of 974

2 MICROBIAL DEGRADATION OF DEOXYNIVALENOL 975 BW) to d 7 broilers, via gavage, resulted in villus atrophy and decreased epithelial mitosis within 24 h. Prelusky et al. (1994a) reported other changes in pigs fed a diet containing low levels of DON, including alterations in stomach and serum proteins, and suggesting specific effects of Fusarium toxins and particular DON. The injury of the gastrointestinal tract, involving thickening of the mucosa of the stomach and a higher degree of folding, is one important characteristic of DON toxicity (Rotter et al., 1994). Awad et al. (2004a) observed that the feeding of broilers with naturally DON-contaminated wheat (5 mg of DON/kg) for 21 d decreased the absolute and relative small intestine weights as well as histological alterations of intestinal villi, especially in the duodenum, as evidenced by shorter and thinner villi. Deoxynivalenol is the major trichothecene in feedstuffs in central Europe and worldwide. In addition to the general necessity for minimizing all risk factors influencing the contamination of cereals with DON as the so-called field toxins before harvest (Oldenburg et al., 2000), several postharvest strategies can be applied to counteract possible deleterious effects of this mycotoxin in farm animals (Dänicke et al., 2000). Neither breeding of resistant cultivars nor the use of chemical plant protection eliminated the contamination of crops by DON so far; organic products appear particularly prone to pollution with DON (Malmauret et al., 2002). The detoxification of DON is of major practical interest; the use of feed additives with the Fusarium toxin s degrading properties might be one method for accomplishing this (Binder et al., 1998) with regard to costs and practicability of a potential detoxification procedure. Rumen and intestinal microflora detoxify DON by the removal of the epoxide oxygen. This de-epoxidation is the most important step in the detoxification of trichothecenes. Deoxynivalenol has been completely transformed to de-epoxy DON after incubating DON with the contents from large intestine of hens (He et al., 1992). Recently a pure culture of an anaerobic Eubacterium sp. capable of DON degradation was characterized (Fuchs et al., 2002). This microbial feed additive has been tested for in vivo efficacy in broilers (Awad et al., 2004b) and was shown to be effective in counteracting the toxic effects of DON on intestinal glucose transport. Therefore, the objectives of the present study were to investigate the effect of 10 mg of DON/kg in the presence or absence of a microbial feed additive on performance, organ weights, and intestinal histology and to evaluate the efficacy of a microbial feed additive (Eubacterium sp.) to counteract the toxic effects of DON on intestinal histology of broiler chickens. MATERIALS AND METHODS Birds, Housing, and Diets Two hundred seventy-seven 1-d-old (males and females) broiler chicks of a commercial strain (Ross E032, Geflügelhof Schulz, Lassnitzhöhe, Austria) were indi- Table 1. Composition of the experimental diet (%) Ingredient Starter Grower Wheat Soybean meal Maize Rape seed oil Dicalcium-phosphate Lysine Methionine Premix Deoxynivalenol 2 (mg/kg) Eubacterium sp. 3 (cfu/kg) Calculated composition 4 Crude protein ME (MJ/kg) Lysine Methionine Calcium Phosphorus Sodium Analyzed composition 5 Crude protein Starch Sugar Lysine Methionine Calcium Phosphorus Sodium Provided per kilogram: 185 g of calcium; 58 g of phosphorus; 50 g of methionine; 25 g of sodium; 250,000 IU of vitamin A; 82,500 IU of vitamin D 3 ; 826 mg of vitamin E; 50 mg of vitamin B 1 ; 225 mg of vitamin B 2 ; 75 mg of vitamin B 6 ; 825 mg of vitamin B 12 ; 37 mg of vitamin K 3 ; 12,500 mg of cholinchloride; 1,000 mg of nicotinic acid; 245 mg of Capantothenate; 25 mg of folic acid; 1,240 mg of biotin; 1,500 mg of iron; 500 mg of copper; 1,750 mg of manganese; 1,250 mg of zinc; 32 mg of iodine; 5 mg of cobalt; 6 mg of selenium. 2 Ten milligrams of deoxynivalenol (DON)/kg were added to starter and grower diets to constitute the DON group. Ten milligrams of DON/ kg plus cfu/kg Eubacterium sp. DSM (PB) were added to constitute the DON-PB group. 3 Biomin GTI GmbH, Herzogenburg, Austria. 4 Based on a dry matter content of 88%. 5 Based on a dry matter content of 91%. vidually weighed and distributed randomly into groups at the research farm of the Veterinary Medicine University of Vienna. Chicks were fed starter diets from d1to 13 and grower diets from d 14 to 42 (Table 1) based on wheat, soybean meal, maize, rapeseed oil, and a premix with vitamins, minerals, amino acids, salt, and dicalcium phosphate. Group 1 received the control diets (n = 91); group 2 received the control diets supplemented with 10 mg of DON (Biomin GTI GmbH, Herzogenburg, Austria)/kg of diet (n = 95); and group 3 received the control diets contaminated with 10 mg of DON/kg and supplemented with cfu/kg of Eubacterium sp. DSM (PB; Biomin GTI GmbH; n = 91). Nutrient concentrations met or exceeded minimum requirements according to the National Research Council (1994). The chicks were initially maintained at 35 C; the temperature was gradually lowered by 2 C/wk to 25 C by the end of wk 5, and this temperature was maintained for the duration of the experiment. During the first 2 wk, continuous lighting was provided after which the duration of light was decreased gradually (2 h daily) to

3 976 AWAD ET AL. Table 2. Effects of deoxynivalenol (DON) with and without probiotic (PB) on absolute organs weights of broiler chickens (g) Group 1 Control DON DON-PB Organ (n = 15) (n = 15) (n = 15) P-value Gizzard 69 ± 5 71 ± 4 73 ± Liver 45 b ± 2 50 ab ± 3 55 a ± Heart 14 ± 1 14 ± 1 14 ± Duodenum 14 ± 1 16 ± 1 17 ± Jejunum 55 b ± 5 71 a ± 6 75 a ± Spleen 3 ± ± ± Pancreas 4 ± ± ± Colon 4 a ± a ± b ± Cecum 23 b ± 2 26 ab ± 2 30 a ± a,b Within the same row, means with different letters are significantly different (Duncan s test). Results are reported as means ± SEM. 1 n = number of birds. 20 h by wk 3, which was maintained throughout the experiment. Feed and water were provided ad libitum. Some of those birds used for studying the effects of DON on the electrical properties are published in separate paper. Representative feed samples were taken at the beginning of the starter and grower periods and were analyzed for nutrient and mycotoxin content. Deoxynivalenol, acetyldeoxynivalenol, nivalenol, and fusarenon-x were determined in the diets using a HPLC technique (Valenta et al., 2002). Traits Body Weight and Feed Consumption. Chicks were weighed individually, and the feed consumption was measured weekly during the 6-wk experiment. Cumulative weight gain and feed consumption were determined, whereas weekly and cumulative feed:gain ratio was calculated. Organ Weights. At the end of experiment, following weighing, 15 birds per treatment were killed by cervical dislocation. Gizzard, heart, liver, pancreas, spleen, duodenum, jejunum, cecum, and colon were excised and weighed. The gastrointestinal tract was weighed after removal of the content. Tissue Sampling. The samples of the whole intestinal tract were removed, and segments of approximately 2 cm were taken from the crop near the esophageal junction, the midpoint of proventriculus, the midpoint of duodenum (duodenum), the midpoint between the bile duct entry and Meckel s diverticulum (jejunum), proximal cecum, and rectum. Segments were fixed in 10% neutral buffered formalin solution and embedded in paraffin wax. All histological studies were performed on 5- m sections, stained by haematoxylin and eosin, and examined by light microscope. The tissue morphology was graded, and the severity of lesions was scored (Zentek et al., 2002). Measurement of Villus Height and Width. In the duodenum and jejunum (4 sections for each segment per bird), the villus length was measured from the villus tip to the bottom, not including the intestinal crypt. The villus width measured at the bottom of villi. The measurement was done with the Scion Image Program (Scion Corporations, Frederick, MD). The mean villus heights and widths from 15 birds were expressed as a mean villus height for 1 treatment group. Statistical Analysis The SPSS (SPSS GmbH, Munich, Germany) program version 11.0 was used for data analysis. The Kolmogorov Smirnov test was used to test the normal distribution of the data. Results are given as means ± SEM. The BW gain, feed intake, feed conversion, organ weights, and height and width of the villi were compared between groups by 1-way ANOVA and subsequent Duncan s Multiple Range Test. Statements of statistical significance were based on P RESULTS Feed Consumption and Feed Efficiency Feed consumption, BW gains, and feed efficiency were not affected by the dietary inclusion of DON over the course of the whole experiment (P > 0.05; data not shown). The supplementation of PB to the diets contaminated with 10 mg of DON/kg slightly improved the general performance of broilers. The mean BW gain and the mean feed consumption over the course of the experiment were numerically higher for broilers fed the DONcontaining diet supplemented with PB compared with the control or DON-fed birds. Organ Weights The effects of feeding DON-contaminated diets on the absolute and relative weights of the liver, heart, gizzard, duodenum, jejunum, spleen, pancreas, colon, and cecum at 42 d of age are shown in Tables 2 and 3. The absolute or relative weights of the gizzard, duodenum, pancreas, heart, colon, cecum, and spleen remained unaltered by the dietary inclusion of DON (P > 0.05). Moreover, the

4 MICROBIAL DEGRADATION OF DEOXYNIVALENOL 977 Table 3. Effects of deoxynivalenol (DON) with and without probiotic (PB) on organs weights relative to body weight of broiler chickens (%) Group 1 Control DON DON-PB Organ (n = 15) (n = 15) (n = 15) P-value Gizzard 3.27 ± ± ± Liver 2.20 ± ± ± Heart 0.63 ± ± ± Duodenum 0.66 ± ± ± Jejunum 2.42 b ± a ± a ± Spleen 0.12 ± ± ± Pancreas 0.18 ± ± ± Colon 0.16 ± ± ± Cecum 1.02 b ± ab ± a ± a,b Within the same row, means with different letters are significantly different (Duncan s test). Results are reported as means ± SEM. 1 n = number of birds. relative liver weight was numerically decreased in broilers fed the diet containing DON compared with controls and the DON-PB group. The microbial feed additive (Eubacterium sp.) supplementation to the contaminated diet increased (P < 0.05) the absolute and relative weights of the jejunum and cecum compared with the control and numerically increased from the DON group, whereas the absolute and relative weights of the gizzard, duodenum, pancreas, heart, and spleen were not altered. The PB supplementation to the contaminated diet had numerically increased the relative weights of liver. Intestinal Lesions In some of the chicks given DON, some mild intestinal changes and some slight diarrhea were observed. However, no other gross pathological lesions were found. Histology of the crop, proventriculus, ileum, cecum, and rectum did not reveal any abnormalities. Intestinal Morphology The DON altered small intestinal morphology, especially in the duodenum and jejunum where the villi were shorter (1,237 ± 10 m and 976 ± 5 m, respectively) and thinner (190 ± 2 m and 158 ± 1 m, respectively) compared with controls (length was 1,667 ± 4 m and 1,064 ± 5 m, and width was 249 ± 3 m and 175 ± 2 m, in the duodenum and jejunum respectively), (Table 4). The PB supplementation to the contaminated diet significantly (P < 0.05) diminished the effects of toxin on the villus height of the duodenum (1,548 ± 7 m) and the jejunum (1,050 ± 6 m). DISCUSSION Fusarium species produce a vast array of mycotoxins, many of which are economically important in regard to animal production. If a mycotoxin is found in a contaminated feed source, there is a high chance of additional mycotoxins being present, produced by several or a single species of mold (Prelusky et al., 1994b). Concentrations of individual mycotoxins are usually low enough not to cause problems with animal performance, but there is a potential for interactions between metabolites that result in net effects of additive or even synergistic relationships. Deoxynivalenol is a common secondary metabolite produced by Fusarium graminearum or Fusarium culmorum. After the addition of DON to the feed at 10 mg/kg in the current study, the overall effects of DON on feed consumption, weight gain, or feed efficiency examined in this study were in general similar to previous reports in chicks where DON was fed at higher or moderate concentrations (Hulan and Proudfoot, 1982; Kubena et al., 1997; Harvey et al., 1997; Swamy et al., 2002). The mean BW gain and the mean feed consumption over the course of the experiment were slightly improved for broilers fed the DON-con- Table 4. The effect of deoxynivalenol (DON) with and without probiotic (PB) on the morphology of small intestine of broiler chickens 1 Duodenum Jejunum Control DON DON-PB Control DON DON-PB (n = 15) (n = 15) (n = 15) P (n = 10) (n = 10) (n = 10) P Villus height ( m) 1,667 a ± 4 1,237 c ± 10 1,548 b ± ,064 a ± b ± 5 1,050 a ± Villus width ( m) 249 a ± b ± b ± a ± b ± b ± a c Within the same row for each organ, means with no common superscripts are significantly different (P 0.05; ANOVA followed by Duncan s test). Results are reported as means ± SEM. 1 n = number of birds.

5 978 AWAD ET AL. taining diet supplemented with PB by approximately 4% compared with the control and 2% compared with the DON-fed birds. The probiotic could have a positive effect on bacterial population (such as Lactobacillus sp.) in the gastrointestinal tract (Smirnov et al., 2005), and the addition of probiotic to diets has been found to improve growth performance (Jin et al., 1997). The absolute or relative weights of the gizzard, duodenum, pancreas, heart, colon, cecum, and spleen remained unaltered by the dietary inclusion of DON. The relative liver weight was numerically decreased in broilers fed the diet containing DON compared with controls and the DON-PB group. However, the absolute and relative jejunum weights were increased. The effects of feeding DON-contaminated grains on organ weights of broiler chickens are very contradictory. Kubena et al. (1985) found that the absolute and relative weights of the liver were decreased in growing chicks fed DONcontaminated grains. Furthermore, Kubena and Harvey (1988) observed no changes in organ weights (liver, spleen, kidney, and bursa of Fabricius). In another study, Kubena et al. (1989) reported increased weight of bursa of Fabricius. In all these studies the chickens were fed 16 mg of DON/kg from contaminated wheat for 21 d. The outcome of these studies was highly variable, indicating that organ weights might not be a relevant indicator of toxicity of some Fusarium mycotoxins. The exposure time of the toxin may be a significant factor for toxin effects on organ weights because the organ initially swells with a short-time exposure followed by shrinkage with long-time exposure (Swamy et al., 2004). The supplementation of the contaminated diet with the probiotic feed additive (Eubacterium sp.) increased the absolute and relative weights of the jejunum and cecum compared with the control. Whether this is only due to the detoxification of DON or to some other effects remains open. The increase in organ weight could also be related to the increased digestion of nutrients and energy, especially in the small intestine (Tortuero and Fernandez, 1995). In the present study, mild intestinal changes such as slight villus atrophy and irregular crypts were observed, but no pathological lesions were found. However, DON altered small intestinal morphology, especially in the duodenum and jejunum. This could be attributed to the irritant effects of DON on the upper gastrointestinal tract. This finding is similar to that reported by Awad et al. (2004a), who observed that feeding of broilers with naturally DON-contaminated wheat (5 mg of DON/kg) for 21 d caused histological alterations in small intestinal morphology, especially in the duodenum, as evidenced by shorter and thinner villi. Fairchild et al. (2005) found that feeding both fusaric acid and diacetoxyscripenol for 18 d to poults decreased enterocyte height at midvillus by 59%. The decrease in enteroctye height is highly indicative that these mycotoxins are altering digestive and absorptive function. This is supported by Sklan et al. (2003), who indicated that feeding of T-2 toxin or diacetoxyscripenol at levels up to 1 ppm for 32 d to poults did not depress but enhanced growth and did not influence antibody production but caused changes in small intestinal morphology, especially in the jejunum where villi were shorter and thinner. These changes appear as indirect response to the dietary trichothecenes. We speculate that this may be explained by the fact that under normal circumstances the major absorption of nutrients occurs in the duodenum and proximal jejunum (Noy and Sklan, 1995), and the small intestine apparently has surplus absorptive capacity (Noy and Sklan, 1996). Feeding of DON decreases the absorption of some nutrients such as D-glucose in the proximal small intestine (Hunder et al., 1991; Awad et al., 2004b), and this could displace some of the uptake to more distal intestinal sites. Therefore, DON appeared to alter the gut function, but overall compensatory capacity is so high that this might not impair performance. The DON is degraded by Eubacterium sp. DSM 11798, which transforms DON into its metabolite DOM-1, the nontoxic de-epoxide of DON (Binder et al., 1997, 1998). Fuchs et al. (2002) also reported that this Eubacterium sp. is specifically capable of detoxifying DON. In the present study, PB was found to be beneficial in counteracting the histological alterations caused by DON. This finding was substantiated by former findings that Eubacterium sp. DSM counteracted the toxic effects of DON on intestinal glucose transport of broilers fed the probiotic and DON-containing diet. In conclusion, feeding DON-contaminated diets at 10 mg/kg did not depress the growth performance of broilers. However, DON altered the small intestinal morphology, especially in the duodenum and jejunum. Furthermore, the results indicate that supplementation of PB (Eubacterium sp.) is beneficial in counteracting the toxicity of DON in commercial broilers at the gut level. REFERENCES Awad, W. A., J. Böhm, E. Razzazi-Fazeli, K. Faukal, and J. Zentek. 2004a. Effects of feeding deoxynivalenol contaminated wheat on the performance of broiler chickens. Pages in Proc. 8. Symp. Eur. Soc.Vet. Comparat. Nutr., Budapest, Hungary. Awad, W. A., J. Böhm, E. Razzazi-Fazeli, H. W. Hulan, and J. Zentek. 2004b. Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poult. Sci. 83: Bergsjo, B., and M. 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