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Effects of Feeding Blends of Grains Naturally Contaminated with Fusarium Mycotoxins on Small Intestinal Morphology of Turkeys

Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada N1G 2W1

¹ Corresponding author: tsmith{at}uoguelph.ca

	ABSTRACT

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An experiment was conducted to investigate the effects of feeding grains naturally contaminated with Fusarium mycotoxins on morphometric indices of duodenum, jejunum, and ileum in turkeys. The possible preventative effect of a polymeric glucomannan mycotoxin adsorbent (GMA) was also determined. Three hundred 1-d-old male turkey poults were fed wheat, corn, and soybean meal-based starter (0 to 3 wk), grower (4 to 6 wk), developer (7 to 9 wk), and finisher (10 to 12 wk) diets formulated with control grains, contaminated grains, and contaminated grains + 0.2% GMA. Morphometric indices were measured at the end of each growth phase and included villus height (VH), crypt depth, villus width, thicknesses of submucosa and muscularis, villus-to-crypt ratio, and apparent villus surface area (AVSA). At the end of the starter phase, feedborne mycotoxins significantly decreased the VH in the duodenum, and supplementation of the contaminated diet with GMA prevented this effect. The feeding of contaminated grains also reduced (P < 0.05) VH and AVSA in jejunum, whereas none of the variables were affected in the ileum. Villus width and AVSA of duodenum, VH, and AVSA of jejunum and submucosa thickness of ileum were significantly reduced when birds were fed contaminated grains at the end of the grower phase, and supplementation with GMA prevented these effects in jejunum and ileum. No effects of diets were seen on morphometric variables at the end of the developer and finisher phases. It was concluded that consumption of grains naturally contaminated with Fusarium mycotoxins results in adverse effects on intestinal morphology during early growth phases of turkeys, and GMA can prevent many of these effects.

Key Words: Fusarium mycotoxin • small intestine • morphology • turkey

	INTRODUCTION

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Mycotoxins are structurally diverse compounds produced by filamentous fungi that vary in their chemistry and biological effects (Sudakin, 2003). The presence of mycotoxins in animal and poultry feeds causes significant economic losses to animal industries (Awad et al., 2006a). The major Fusarium mycotoxins occurring in cereal grains, animal feeds, and forages are the trichothecenes, zearalenone (ZEN), and fumonisins. Other important Fusarium mycotoxins include moniliformin and fusaric acid (FA; Smith et al., 2005). The main target of trichothecene mycotoxins are rapidly proliferating and differentiating cells and tissues with a high protein turnover, including small intestine, liver, and the immune system (Feinberg and McLaughlin, 1989). The toxic effects of Fusarium mycotoxins in animals and poultry include reduced growth, feed refusal and vomiting, immunosuppression, gastrointestinal lesions, and neurological and reproductive disorders (Rocha et al., 2005).

The feeding of deoxynivalenol (DON) to broilers at levels below those that cause adverse effects on health and performance may affect small intestinal morphology (Awad et al., 2006a). The feeding of purified DON at 10 mg/kg of feed to broilers for 6 wk resulted in shorter and thinner villi in the duodenum and jejunum (Awad et al., 2006a). Body weight gain and efficiency of feed utilization, however, were not affected by consumption of DON. Feeding turkey poults pure T-2 toxin or diacetoxyscirpenol (DAS) at levels up to 1 mg/kg of feed for 32 d adversely influenced small intestinal morphology but did not affect growth or antibody production (Sklan et al., 2003). The feeding of a combination of T-2 toxin and DAS, however, resulted in severe oral lesions. Awad et al. (2006b) observed an increase in absolute and relative weights of the small intestine after feeding broilers naturally contaminated wheat containing 5 mg of DON/kg of feed for d 21. Performance and absolute and relative weights of organs, however, were not affected. Duodenal villi height and width were significantly decreased after feeding 5 mg of DON/kg of feed to broilers for 21 d. Feeding a combination of FA (300 mg/kg of feed) and DAS (4 mg/kg of feed) to turkey poults for 18 d decreased enterocyte height at midvillus by 59% (Fairchild et al., 2005). Feeding FA alone, however, reduced the relative weight of intestine and serosal thickness, whereas feeding DAS alone increased the serosal thickness.

To the best of our knowledge, there are no reports on the effects of chronic feeding of grains naturally contaminated with Fusarium mycotoxins on small intestinal morphology of turkeys. A polymeric glucomannan mycotoxin adsorbent (GMA) derived from the cell wall of yeast has been shown to prevent some of the deleterious effects of Fusarium mycotoxins on performance and metabolism of poultry (Swamy et al., 2002, 2004; Chowdhury et al., 2005a,b,c). The current experiment was conducted, therefore, to study the effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on small intestinal morphology of turkeys and to determine the efficacy of GMA in preventing these effects.

	MATERIALS AND METHODS

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Experimental Birds, Diets, and Design
Three hundred 1-d-old Hybrid turkey poults (Hybrid Turkeys, Kitchener, Ontario, Canada) were individually weighed, wing-banded, and distributed randomly into groups of 20 poults per floor pen at the Arkell Poultry Research Station of the University of Guelph. Five pens were randomly assigned to each of the 3 diets with each diet fed to 100 poults. Poults were initially maintained at 32°C, and the temperature was gradually reduced by 3°C per week to reach a temperature of 21°C by the end of wk 4. This temperature was maintained for the duration of the experiment. Turkey poults were fed wheat, corn, and soybean meal-based starter (0 to 3 wk), grower (4 to 6 wk), developer (7 to 9 wk), and finisher (10 to 12 wk) diets formulated with control grains, contaminated grains, and contaminated grains + 0.2% GMA (Mycosorb, Alltech Inc., Nicholasville, KY). The control diet was formulated to meet or exceed the minimum nutrient requirements of turkeys according to the NRC (1994). Mycotoxin-contaminated diets were prepared by replacing 10 and 35% of the control corn and wheat with corn and wheat naturally contaminated with Fusarium mycotoxins. The levels of replacement of control grains with the contaminated grains were the same in all growth phases to provide a constant mycotoxin challenge. Feed and water were provided ad libitum. Representative feed samples were taken at the beginning of each phase for proximate and mycotoxin analyses. Dietary contents of protein, DM, and ash were determined according to the Association of Official Analytical Chemists (1980). The diet formulations and nutrient contents are presented in Table 1. The experimental procedures were approved by the University of Guelph Animal Care Committee following the guidelines of the Canadian Council on Animal Care.

Tissue Collection and Morphometric Indices of the Duodenum, Jejunum, and Ileum
At the end of each growth phase, 2 birds/pen (10 birds/ treatment) were euthanized by cervical dislocation. Intestinal segment samples (each 2.5 cm in length) of duodenum, jejunum, and ileum were excised and flushed with 0.9% saline to remove the contents. The intestinal segments were fixed in 10% neutral-buffered formalin for histology. The intestinal segments collected were the loop of the duodenum, midpoint between the bile duct entry and Meckel’s diverticulum (jejunum), and midway between Meckel’s diverticulum and the ileocecal junction (ileum). Samples were dehydrated, cleared, and paraffin-embedded. Intestinal segments from 10 birds/diet were sectioned at 5-µm thickness, placed on glass slides, and processed by hematoxylin and eosin stain for examination by light microscopy, according to Girdhar et al. (2006). Morphometric indices included were villus height (VH) from the tip of the villus to the crypt, crypt depth from the base of the villi to the submucosa, villus width (VW; average of VW at one-third and two-third of the villus), muscularis from the submucosa to the external layer of the intestine, and the villus-to-crypt ratio (Geyra et al., 2001). Apparent villus surface area (AVSA) was calculated by the formula: [(VW at one-third + VW at two-thirds of the height of the villus) x (2)^–1 x villus height], according to Iji et al. (2001). Morphometric measurements were performed on 15 villi chosen from each segment, using a table of random numbers and a computer-aided light microscope image with Openlab software (Openlab Version 2.2.5, Improvision, Waltham, MA; Girdhar et al., 2006).

Statistical Analyses
Data were analyzed by ANOVA using a PROC MIXED model of SAS based on a randomized complete block design with subsampling (Kuehl, 2000; SAS Institute, 2000). Pens were treated as individual experimental units, and rooms were treated as blocks. Multiple comparisons among the treatment least squares means were made using Tukey’s test. Statements of statistical significance were based on P 0.05.

	RESULTS

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Dietary Mycotoxin Concentrations
To maintain similar concentrations of mycotoxins at all growth phases of the experiment, 10 and 35% of control corn and wheat were replaced with contaminated corn and wheat, respectively. Dietary concentrations of DON, 15-acetyl-DON, ZEN, and FA are given in Table 2. Other mycotoxins were in concentrations below the detection limits, which were 0.02 mg/kg for aflatoxin, 2 mg/kg for fumonisins, 0.77 mg/kg for FA, and 0.2 mg/kg for the remaining mycotoxins analyzed.

	DISCUSSION

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Dietary Mycotoxin Concentrations
Diets were formulated to achieve similar concentrations of mycotoxins at all growth phases by incorporating the same levels and sources of contaminated corn and wheat. The major contaminant in all contaminated diets was DON, and concentrations were similar in all growth phases (Table 2). It was found that 15-acetyl-DON and ZEN were present as minor contaminants. Toxicological synergy between DON and ZEN, however, has not been observed in swine (Cote et al., 1985) or mice (Forsell et al., 1986). The cytotoxicity of 15-acetyl-DON is similar to that of DON (Eriksen et al., 2004), and the toxicity of 15-acetyl-DON in the present study may be additive to that of DON. It has been reported that the same level of inclusion of contaminated grains resulted in 1.9 mg of DON/ kg of feed in 1 experiment and 4.4 mg of DON/kg of feed in another experiment (Smith et al., 1997). Failure to achieve the same concentrations of DON in the present experimental diets may be attributable to lack of uniformity in occurrence of mycotoxins in contaminated corn and wheat (Hamilton, 1978) and problems associated with sampling, surveying, postcollection handling, and analysis of mycotoxin-contaminated grains (Davis et al., 1980). It has also recently been shown that some of the Fusarium mycotoxins including DON and ZEN form conjugates with glucose, thereby escaping routine analytical detection procedures (Schneweis et al., 2002; Berthiller et al., 2005).

Deoxynivalenol concentrations of <0.5 to 1.2 mg/kg of feed (starter, grower, and developer) and 0.2 mg of ZEN/ kg during the developer phase were detected in the control diets, thereby indicating that control corn and wheat contained, nevertheless, detectable amounts of mycotoxins. There is no evidence for DON toxicity in turkeys at the concentrations detected in control diets of the present study.

Analyses of feeds and feedstuffs grown in North America for Fusarium mycotoxins have shown DON and FA as frequent contaminants, whereas ZEN is a less common problem (Smith and Sousadias, 1993). It has been shown that acute doses of FA caused vomiting and lethargy in swine (Smith and MacDonald, 1991). Fusaric acid was a common contaminant in all experimental diets (Table 2). It is possible that FA may act synergistically with trichothecene mycotoxins to increase the toxicity of contaminated feedstuffs. Swamy et al. (2002) found FA concentrations of 18 mg/kg of feed in control diet, 20.6 mg/ kg feed in a low level of contaminated grains, and 20.3 mg/kg of feed in a high level of contaminated grains. The concentration of FA ranged from 11.61 to 35.76 µg/ g of feed, which was analyzed in swine feedstuffs (Smith and Sousadias, 1993). It could be hypothesized that occurrence of FA in naturally contaminated diets is not unusual and may be attributable to synergistic toxic effects when present with other Fusarium mycotoxins.

Morphometric Indices
At the end of the starter phase, a significant reduction of VH in duodenum and VH and AVSA in jejunum was observed after feeding contaminated grains; however, no effects were seen on ileum. Shorter and thinner villi, especially in duodenum of broilers, was observed after feeding 5 mg of naturally contaminated DON/kg of feed for 21 d, which was characterized by decreased weight of the small intestine. There were no significant changes, however, in jejunal villi morphology (Awad et al., 2006b). Fairchild et al. (2005) reported significant reduction in relative intestinal weight and jejunal serosa thickness in turkey poults fed 300 mg of purified FA/kg of feed for 18 d. Feeding 4 mg of DAS/kg of feed to turkey poults did not affect the weight of intestine; however, feeding both FA and DAS to poults decreased enterocyte height at midvillus by 59%. This decrease, however, is indicative of Fusarium mycotoxins altering digestive and absorptive function (Fairchild et al., 2005). In the present study, at the end of the grower phase, VW and AVSA of duodenum, VH and AVSA of jejunum, and submucosa thickness of the ileum were significantly affected after feeding contaminated grains. A significant reduction in VH and VW in duodenum and jejunum was observed in broilers after feeding 10 mg of purified DON/kg of feed for 42 d (Awad et al., 2006a). In 2 separate studies, Awad et al. (2006a, b) reported increases in absolute and relative weights of jejunum in the first study but not in the second study. In the present study, small intestinal weights were not measured, because reports on the effects of Fusarium mycotoxins on organ weights of poultry are contradictory and, hence, organ weights might not be a definitive indicator of toxicity of some of the Fusarium mycotoxins. In these previous studies, DON was the only feedborne contaminant; however, the concentrations were higher compared with DON concentrations in the present study. The possible effects seen in the current study may be attributable to feeding of a combination of Fusarium mycotoxins. Deoxynivalenol has been reported to cause adverse effects in poultry when fed in combination with other mycotoxins (Morris et al., 1999). Fusarium mycotoxins in combination exert more pronounced adverse effects in animals than individual mycotoxins (Smith et al., 1997). The effects of Fusarium mycotoxins on small intestinal morphology have been attributed to irritant effects on the gastrointestinal tract (Awad et al., 2006a,b). Multiple inhibitory effects of trichothecenes on eukaryotic cells have been reported by Rocha et al. (2005), including disruption of normal cell function by inhibiting RNA, DNA, and protein synthesis; inhibition of cell division; stimulation of ribotoxic stress response; and activation of mitogen-activated protein kinases. The latter enzymes catalyze reactions in signal transduction related to proliferation, differentiation, and apoptosis (Pestka and Smolinski, 2005).

Sklan et al. (2003) reported that feeding turkey DAS or T-2 toxin up to 1 mg/kg of feed for 32 d adversely affected small intestinal morphology. Feeding DAS to turkey poults decreased VW and area in the duodenum and villus width, length, and area in jejunum. Reduction in length of villus in the duodenum, and both villus length and width in the jejunum, and thus villus area were observed in poults fed T-2 toxin. Increased proliferation of enterocytes in the crypts and along the villi was observed in poults fed DAS or T-2 toxin, whereas feeding T-2 toxin alone reduced the enterocyte migration rate in jejunum of poults (Sklan et al., 2003). In the present study, enterocyte migration rates and proliferation were not measured. Adverse effects of Fusarium mycotoxins on VH, VW, and AVSA, however, might have caused changes in migration rate and proliferation of enterocytes. Increases in the proportion of the proliferating cells during mycotoxicoses may be attributable to mycotoxin-induced stress (Sklan et al., 2003). Trichothecenes cause harmful injury to the mucosa, destroying cells on the tips of villi and radiomimetic injury to rapidly dividing crypt epithelium (Hoerr, 1998). The morphological alterations in villus height, villus width, and AVSA may contribute to reduced nutrient absorption in duodenum and jejunum. Not many changes were observed in ileum, however, after feeding contaminated grains. Inhibitory effects of DON on Na⁺-D-glucose/Na⁺-L-proline cotransporters have been previously reported (Awad et al., 2004, 2005b).

In previous studies, there were no significant changes in poultry performance. Even though small intestinal morphology was significantly affected (Sklan et al., 2003; Awad et al., 2006a,b), it was speculated that under normal conditions the main absorption site for nutrients was in the duodenum and jejunum due to their greater absorptive surface area (Awad et al., 2006a). It has been shown that feeding 10 mg of purified DON/kg of feed decreased the absorption of D-glucose in the jejunum of broilers (Awad et al., 2004) and DON inhibited Na⁺ and Na⁺-D-glucose cotransport in jejunum of laying hens in vitro (Awad et al., 2005a). This could have caused a shift in the absorption site for nutrients to distal parts of the small intestine as a compensatory mechanism, and hence, there were no significant changes observed on performance of poultry (Awad et al., 2006a). Awad et al. (2004) observed an increase in tissue (jejunum) resistance in birds fed 10 mg of DON/kg of feed, and hence, DON appeared to alter gut function. Fumonisin B₁ was found to alter the proliferation and the barrier function of porcine intestinal epithelial cells (Bouhet et al., 2004). The feeding of rice inoculated with Fusarium graminearum to rats for 14 d caused epithelial cell and connective tissue damage in the duodenum (Ozbek et al., 2005). The ability of DON to reduce intestinal absorptive capacity in human intestinal cell lines has been demonstrated by Maresca et al. (2002). The effects of DON on human intestinal cell lines were mainly due to modulation of the activity of intestinal transporters including D-glucose/D-galactose sodium-dependent transporters and D-fructose transporters and L-serine transporters.

The first barrier to nutrient metabolism in animals is the gastrointestinal tract, and its metabolic activity can have an effect on the nutrient supply of the whole animal. The nutrient utilization efficiency would be more if the nutrient loss at the gastrointestinal tract level could be minimized (Iji et al., 2001). The integrity of the intestinal epithelium is important so as to utilize the nutrients to the maximum extent. The changes in the morphology of villi and reduction in absorptive surface area may reduce the nutrient absorption and hence lead to reduced production performance. The feeding of naturally contaminated grains to turkeys for a period of 12 wk reduced the body weight gains during the grower and developer phases; however, no change was observed during the starter phase (Girish et al., 2008) at concentrations of mycotoxins that had altered the small intestinal morphology in the present study. In contrast to previous reports, the changes observed in the morphology of the gastrointestinal tract might have contributed to reduced weight gains. Swamy et al. (2002) reported a significant reduction in broiler weight gains at higher inclusion levels of mycotoxins during the finisher phase, however, there were no significant reductions during the starter phase. This indicates that duration of exposure, concentration, and source of mycotoxins could contribute to cumulative effects of mycotoxins on the physiology of the gastrointestinal tract, which might cause a reduction in the absorption of the nutrients from the gut. Naturally contaminated sources may be more toxic than an equivalent amount of purified compound (Harvey et al., 1991). This is probably due to the presence of the unidentified mycotoxins and precursors in naturally contaminated grains resulting in additive or synergistic effects among mycotoxins (Smith et al., 1997).

A lack of significant changes in poultry performance even with the alterations in small intestinal morphology, gut electrophysiology, and nutrient transport could be due to short duration of exposure and the source of mycotoxins. In previous studies, in contrast to the present study, the experimental duration was restricted to the starter phase (Sklan et al., 2003; Awad et al., 2006b), and DON was the only contaminant of the diets.

There were no significant effects of diet on small intestinal morphology at the end of developer and finisher phases in the current study. The concentrations of mycotoxins, however, during these phases were similar with those during early growth phases including starter and grower phases. This lack of effect of diet on small intestinal morphology during the developer and finisher phases may be due to increased resistance to Fusarium mycotoxins over a period of 9 wk. It could also be possible that the concentration of mycotoxins during the later growth phases may not be sufficient to cause alteration in small intestinal morphology.

Several strategies to prevent mycotoxicoses in animals and poultry including physical, chemical, and biological have been investigated (Diaz and Smith, 2005). Polymeric glucomannan mycotoxin adsorbents have been shown to have beneficial effects in preventing adverse effects of Fusarium mycotoxins in turkeys (Chowdhury et al., 2005c; Chowdhury and Smith, 2007), broiler chickens (Swamy et al., 2002), laying hens (Chowdhury and Smith, 2004), and broiler breeders (Yegani et al., 2006). In the current study, GMA prevented many of the adverse effects on small intestine morphology caused by feeding Fusarium mycotoxins. Interactions between mycotoxins and adsorbents in the intestinal lumen may prevent harmful effects on the intestinal epithelium, the absorption of mycotoxins, and the transfer of mycotoxins to target tissues (Ramos et al., 1996).

In conclusion, Fusarium mycotoxins have been shown to adversely affect small intestine morphology. The mechanism, by which this occurs, however, is not understood. The adverse effects on small intestine reduce the uptake of nutrients from the gut and hence decrease production performance of poultry. Under commercial farm conditions, diets contaminated with Fusarium mycotoxins along with metabolic stresses associated with environment and management might aggravate the harmful effects on the gut leading to economic losses.

	ACKNOWLEDGMENTS

 
Financial support for this study was provided by the Ontario Ministry of Agriculture, Food and Rural Affairs and Alltech Inc. (Nicholasville, KY). We gratefully acknowledge Margaret Quinton for statistical advice and the technical assistance of Mojtaba Yegani (Department of Animal and Poultry Science, University of Guelph).

Received for publication September 12, 2007. Accepted for publication February 7, 2008.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Association of Official Analytical Chemists. 1980. Official Methods of Analysis. 13th ed. AOAC Int., Washington, DC.

Awad, W. A., J. Bohm, E. Razzazi-Fazeli, K. Ghareeb, and J. Zentek. 2006a. Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poult. Sci. 85:974–979.[Abstract/Free Full Text]

Awad, W. A., J. Bohm, E. Razzazi-Fazeli, H. W. Hulan, and J. Zentek. 2004. Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poult. Sci. 83:1964–1972.[Abstract/Free Full Text]

Awad, W. A., J. Bohm, E. Razzazi-Fazeli, and J. Zentek. 2006b. Effects of feeding deoxynivalenol contaminated wheat on growth performance, organ weights and histological parameters of the intestine of broiler chickens. J. Anim. Physiol. Anim. Nutr. (Berl.) 90:32–37.[Medline]

Awad, W. A., J. Bohm, E. Razzazi-Fazeli, and J. Zentek. 2005a. In vitro effects of deoxynivalenol on electrical properties of intestinal mucosa of laying hens. Poult. Sci. 84:921–927.[Abstract/Free Full Text]

Awad, W. A., H. Rehman, J. Bohm, E. Razzazi-Fazeli, and J. Zentek. 2005b. Effects of luminal deoxynivalenol and L-proline on electrophysiological parameters in the jejunums of laying hens. Poult. Sci. 84:928–932.[Abstract/Free Full Text]

Berthiller, F., C. Dallasta, R. Schumacher, M. Lemmens, G. Adam, and R. Krska. 2005. Masked mycotoxins: Determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography-tandem mass spectrometry. J. Agric. Food Chem. 53:3421–3425.[CrossRef][Web of Science][Medline]

Bouhet, S., E. Hourcade, N. Loiseau, A. Fikry, S. Martinez, M. Roselli, P. Galtier, E. Mengheri, and I. P. Oswald. 2004. The mycotoxin fumonisin B₁ alters the proliferation and the barrier function of porcine intestinal epithelial cells. Toxicol. Sci. 77:165–171.[Abstract/Free Full Text]

Chowdhury, S. R., and T. K. Smith. 2004. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of laying hens. Poult. Sci. 83:1849–1856.[Abstract/Free Full Text]

Chowdhury, S. R., and T. K. Smith. 2007. Effects of feed-borne Fusarium mycotoxins on performance, plasma chemistry and hepatic fractional protein synthesis rates of turkeys. Can. J. Anim. Sci. 87:543–551.

Chowdhury, S. R., T. K. Smith, H. J. Boermans, A. E. Sefton, R. Downey, and B. Woodward. 2005a. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance, metabolism, hematology and immunocompetence of ducklings. Poult. Sci. 84:1179–1185.[Abstract/Free Full Text]

Chowdhury, S. R., T. K. Smith, H. J. Boermans, and B. Woodward. 2005b. Effects of feed-borne Fusarium mycotoxins on hematology and immunology of laying hens. Poult. Sci. 84:1841–1850.[Abstract/Free Full Text]

Chowdhury, S. R., T. K. Smith, H. J. Boermans, and B. Woodward. 2005c. Effects of feed-borne Fusarium mycotoxins on hematology and immunology of turkeys. Poult. Sci. 84:1698–1706.[Abstract/Free Full Text]

Cote, L. M., V. R. Beasley, P. M. Bratich, S. P. Swanson, H. L. Shivaprasad, and W. B. Buck. 1985. Sex-related reduced weight gains in growing swine fed diets containing deoxynivalenol. J. Anim. Sci. 61:942–950.[Abstract/Free Full Text]

Davis, N. D., J. W. Dickens, R. L. Freie, P. B. Hamilton, O. L. Shotwell, T. D. Wyllie, and J. F. Fulkerson. 1980. Protocols for surveys, sampling, post-collection handling, and analysis of grain samples involved in mycotoxin problems. J. Assoc. Off. Anal. Chem. 63:95–102.[Medline]

Diaz, D. E., and T. K. Smith. 2005. Mycotoxin sequestering agents: Practical tools for the neutralization of mycotoxins. Pages 323–339 in The Mycotoxin Blue Book. D. Diaz, ed. Nottingham Univ. Press, Nottingham, UK.

Eriksen, G. S., H. Pettersson, and T. Lundh. 2004. Comparative cytotoxicity of deoxynivalenol, nivalenol, their acetylated derivatives and de-epoxy metabolites. Food Chem. Toxicol. 42:619–624.[CrossRef][Web of Science][Medline]

Fairchild, A. S., J. L. Grimes, J. K. Porter, W. J. Croom Jr., L. R. Daniel, and W. M. Hagler Jr. 2005. Effects of diacetoxyscirpenol and fusaric acid on poults: Individual and combined effects of dietary diacetoxyscirpenol and fusaric acid on turkey poult performance. Int. J. Poult. Sci. 4:350–355.

Feinberg, B., and C. S. McLaughlin. 1989. Biochemical mechanism of action of trichothecene mycotoxins. Pages 27–35 in Trichothecene Mycotoxicosis: Pathophysiologic Effects. Vol I, V. R. Beasley, ed. CRC Press, Boca Raton, FL.

Forsell, J. H., M. F. Witt, J. H. Tai, R. Jensen, and J. J. Pestka. 1986. Effects of 8-week exposure of the B6C3F1 mouse to dietary deoxynivalenol (vomitoxin) and zearalenone. Food Chem. Toxicol. 24:213–219.[CrossRef][Web of Science][Medline]

Geyra, A., Z. Uni, and D. Sklan. 2001. Enterocyte dynamics and mucosal development in the posthatch chick. Poult. Sci. 80:776–782.[Abstract/Free Full Text]

Girdhar, S. R., J. R. Barta, F. A. Santoyo, and T. K. Smith. 2006. Dietary putrescine (1,4-diaminobutane) influences recovery of turkey poults challenged with a mixed coccidial infection. J. Nutr. 136:2319–2324.[Abstract/Free Full Text]

Girish, C. K., T. K. Smith, H. J. Boermans, and N. A. Karrow. 2008. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance, hematology, metabolism and immunocompetence of turkeys. Poult. Sci. 87:421–432.[Abstract/Free Full Text]

Groves, F. D., L. Zhang, Y. S. Chang, P. F. Ross, H. Casper, W. P. Norred, W. C. You, and J. F. Fraumeni Jr. 1999. Fusarium mycotoxins in corn and corn products in a high-risk area for gastric cancer in Shandong province, China. J. AOAC Int. 82:657–662.[Web of Science][Medline]

Hamilton, B. 1978. Fallacies in our understanding of mycotoxins. J. Food Prot. 41:404–408.[Web of Science]

Harvey, R. B., L. F. Kubena, W. E. Huff, M. H. Elissalde, and T. D. Phillips. 1991. Hematologic and immunologic toxicity of deoxynivalenol (DON)-contaminated diets to growing chickens. Bull. Environ. Contam. Toxicol. 46:410–416.[CrossRef][Web of Science][Medline]

Hoerr, F. J. 1998. Pathogenesis of enteric diseases. Poult. Sci. 77:1150–1155.[Abstract/Free Full Text]

Iji, P. A., A. Saki, and D. R. Tivey. 2001. Body and intestinal growth of broiler chicks on a commercial starter diet. 1. Intestinal weight and mucosal development. Br. Poult. Sci. 42:505–513.[CrossRef][Web of Science][Medline]

Kuehl, R. O. 2000. Design of Experiments: Statistical Principles of Research Design and Analysis. Duxbury Press, Toronto, Ontario, Canada.

Leung, M. C. K., T. K. Smith, N. A. Karrow, and H. J. Boermans. 2007. Effects of feeding diets naturally contaminated with Fusarium mycotoxins on feed intake, body weight, hematology, and nutrient digestibility of mature beagles. Am. J. Vet. Res. 68:1122–1129.[Web of Science][Medline]

Maresca, M., R. Mahfoud, N. Garmy, and J. Fantini. 2002. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 132:2723–2731.[Abstract/Free Full Text]

Matsui, Y., and M. Watanabe. 1988. Quantitative analysis of fusaric acid in the cultural filtrate and soybean plants inoculated with Fusarium oxysporum var. redolens. J. Rakuno Gakuen Univ. Nat. Sci. 13:159–167.

Morris, C. M., Y. C. Li, D. R. Ledoux, A. J. Bermudez, and G. E. Rottinghaus. 1999. The individual and combined effects of feeding moniliformin, supplied by Fusarium fujikuroi culture material, and deoxynivalenol in young turkey poults. Poult. Sci. 78:1110–1115.[Abstract/Free Full Text]

NRC. 1994. Nutrient Requirements of Poultry. 9th. ed. Natl. Acad. Press, Washington, DC.

Ozbek, E., A. Ozbek, and Z. Calik. 2005. Histopathological effects of dietary Fusarium graminearum on rat duodenum. J. Int. Med. Res. 33:520–527.[Web of Science][Medline]

Pestka, J. J., and A. T. Smolinski. 2005. Deoxynivalenol: Toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 8:39–69.[Web of Science][Medline]

Porter, J. K., C. W. Bacon, E. M. Wray, and W. M. Hagler Jr. 1995. Fusaric acid in Fusarium moniliforme cultures, corn, and feeds toxic to livestock and the neurochemical effects in the brain and pineal gland of rats. Nat. Toxins 3:91–100.[CrossRef][Medline]

Ramos, A. J., J. Fink-Gremmels, and E. Hernandez. 1996. Prevention of toxic effects of mycotoxins by means of nonnutritive adsorbent compounds. J. Food Prot. 59:631–641.[Web of Science]

Raymond, S. L., T. K. Smith, and H. V. L. N. Swamy. 2003. Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on feed intake, serum chemistry, and hematology of horses, and the efficacy of a polymeric glucomannan mycotoxin adsorbent. J. Anim. Sci. 81:2123–2130.[Abstract/Free Full Text]

Rocha, O., K. Ansari, and F. M. Doohan. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: A review. Food Addit. Contam. 22:369–378.[CrossRef][Web of Science][Medline]

SAS Institute. 2000. SAS User’s Guide: Statistics. 8th ed. SAS Inst. Inc., Cary, NC.

Schneweis, I., K. Meyer, G. Engelhardt, and J. Bauer. 2002. Occurrence of zearalenone-4-β-D-glucopyranoside in wheat. J. Agric. Food Chem. 50:1736–1738.[CrossRef][Web of Science][Medline]

Sklan, D., M. Shelly, B. Makovsky, A. Geyra, E. Klipper, and A. Friedman. 2003. The effect of chronic feeding of diacetox-yscirpenol and T-2 toxin on performance, health, small intestinal physiology and antibody production in turkey poults. Br. Poult. Sci. 44:46–52.[Web of Science][Medline]

Smith, T. K., G. Diaz, and H. V. L. N. Swamy. 2005. Current concepts in mycotoxicoses in swine. Pages 235–248 in The Mycotoxin Blue Book. D. Diaz, ed. Nottingham Univ. Press, Nottingham, UK.

Smith, T. K., and E. J. MacDonald. 1991. Effect of fusaric acid on brain regional neurochemistry and vomiting behavior in swine. J. Anim. Sci. 69:2044–2049.[Abstract]

Smith, T. K., E. G. McMillan, and J. B. Castillo. 1997. Effect of feeding blends of Fusarium mycotoxin-contaminated grains containing deoxynivalenol and fusaric acid on growth and feed consumption of immature swine. J. Anim. Sci. 75:2184–2191.[Abstract/Free Full Text]

Smith, T. K., and M. G. Sousadias. 1993. Fusaric acid content of swine feedstuffs. J. Agric. Food Chem. 41:2296–2298.[CrossRef][Web of Science]

Sudakin, D. L. 2003. Trichothecenes in the environment: Relevance to human health. Toxicol. Lett. 143:97–107.[CrossRef][Web of Science][Medline]

Swamy, H. V. L. N., T. K. Smith, P. F. Cotter, H. J. Boermans, and A. E. Sefton. 2002. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on production and metabolism in broilers. Poult. Sci. 81:966–975.[Abstract/Free Full Text]

Swamy, H. V. L. N., T. K. Smith, N. A. Karrow, and H. J. Boermans. 2004. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on growth and immunological parameters of broiler chickens. Poult. Sci. 83:533–543.[Abstract/Free Full Text]

Yegani, M., T. K. Smith, S. Leeson, and H. J. Boermans. 2006. Effects of feeding grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of broiler breeders. Poult. Sci. 85:1541–1549.[Abstract/Free Full Text]

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