| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
ENVIRONMENT, WELL-BEING, AND BEHAVIOR |
* Department of Veterinary Public Health and Food Science, Institute of Animal Nutrition, University of Veterinary Medicine, A-1210 Vienna, Austria; and Institute for Veterinary Physiology, University of Leipzig, D-04103 Leipzig, Germany
1 Corresponding author: juergen.zentek{at}vu-wien.ac.at
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Key Words: laying hen • deoxynivalenol • Ussing chamber • glucose absorption • sodium glucose-linked transporter-1
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Toxic effects of DON in different animal species have been well documented and focus mainly on the immune system and the gastrointestinal tract. The injury to the gastrointestinal tract involves thickening of the mucosa of the stomach and changes in villi morphology in the small intestine (Rotter et al., 1994; Awad et al., 2006a,b). Consequences are alterations in feed conversion and susceptibility to diseases (Bondy and Pestka, 2000).
It seems likely that the morphological changes in the intestine and the decreased feed conversion are linked to an impaired absorption of nutrients. Intestinal absorption of sugars and amino acids occurs mainly actively through cellular pathways and small quantities passively through a paracellular or a cellular route. Given the active cotransport of D-glucose and sodium via the sodium glucose-linked transporter-1 (SGLT-1), the addition of D-glucose to the luminal side of different parts of small and large intestines of chickens induces a current flow across the epithelium (Amat et al., 1999). This current can be measured in Ussing chambers as short-circuit current (Isc). Awad et al. (2004) found a decreased Isc after addition of D-glucose when artificially-contaminated diets, containing 10 mg of DON/kg, were fed to broilers for 42 d. This can be taken as an indirect indication that DON interferes with SGLT-1 activity in the chicken intestine. However, direct evidence for this suggestion is lacking so far. Therefore, the aim of the first experiment was to verify an effect of DON on small intestinal glucose absorption by direct evaluation of the effect of DON on intestinal glucose uptake in chickens, using an Ussing chamber approach.
The second aim of the study was to evaluate the absorption of DON itself in our in vitro system. In vivo, DON seems to be rapidly and efficiently absorbed, most probably from the upper parts of the small intestine, and is mainly excreted in the urine, with no significant accumulation in tissues (Prelusky et al., 1988; Eriksen et al., 2003). Very little data are available on the transport mechanism of DON through the chicken digestive tract. Therefore, in the second experiment, we have investigated the kinetics of DON permeation in chicken jejunal mucosa.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Lohmann Brown laying hens, 18 to 22 wk of age, weighing 1 to 1.5 kg, were used in the present study. The birds were purchased from a local commercial farm (Erzeugergemeinschaft Agrarprodukte, Wildenhain, Germany). The hens were housed on deep wood shavings litter and were fed a commercial layer diet (Leikra-Qualitätsfutter, Leipzig, Germany). The diet contained 16.5% CP, 3.8% crude fat, 3.8% crude fiber, 12.9% crude ash, and 0.26% Met. The hens were provided with their diets and water ad libitum for the duration of the experiment.
Tissue Preparation
Tissue preparation, incubation in Ussing chambers, and electrophysiological recordings were performed as described earlier (Awad et al., 2004) with a few modifications specified below. Birds were slaughtered by stunning and bleeding. Immediately after exsanguination, the gastrointestinal tract was removed from the abdominal cavity. Segments were taken from the midjejunum. The intestine was rinsed with ice-cold buffer and transported to the laboratory in ice-cold incubation buffer oxygenated with carbogen (95% O2 and 5% CO2). The intestinal segment was opened along the mesenteric border and washed free of intestinal contents with buffer solution at 4°C. The underlying serosal layer was stripped off, and the epithelial sheets were mounted in Ussing chambers. Epithelial sheets had an exposed serosal area of 1.1 cm2 and were incubated with 12 mL of buffer solution on their mucosal and serosal sides under short-circuit conditions.
Buffer Solutions
Buffer solutions used for washing, transport, and incubation of epithelia contained the following chemicals (Sigma-Aldrich Chemie GmbH, Schnelldorf, Germany, in mmol/L): NaCl, 115; KCl, 5; CaCl2, 1.5; MgCl2, 1.2; NaH2PO4, 0.4; Na2HPO4, 2.4; L-glutamine, 1; Na-DL-lactate, 5; HEPES-free acid, 10; NaHCO3, 20; mannitol, 20; and NaOH, 10 (320 ± 5 mosmol/kg; pH 7.4). Isolated epithelia were incubated in D-glucose-free buffer mucosally and glucose (10 mmol/L) containing buffer serosally in Ussing chamber for at least 30 min. The incubation medium was continuously gassed with carbogen, and the temperature of the mixture was kept at 38°C by thermostated water jackets. Continuous oxygenation provided recirculation of the incubation solutions by means of a gas lift.
Glucose Uptake Technique
After a tissue stabilization period of 15 min, the basal measurements of Isc and tissue conductance (Gt) were recorded. The allotment of epithelia to different treatments was based on their tissue conductance values 30 min after mounting. Epithelial tissues used for direct comparison of different treatments were not allowed to differ in their conductance values by >30%. Forty-five minutes before uptake measurement, DON (Biopure GmbH, Tulln, Austria, 10 mg/L, final concentration) was added on the luminal side in the DON-treated group. The inhibitor of SGLT-1, phlorizin (100 µmol/L, final concentration), was added to the mucosal side 2 min before mucosal glucose addition. Deoxynivalenol and phlorizin were dissolved in ethanol. An equal volume of ethanol was added to the luminal side in the control epithelia. Thereafter, measurement of glucose uptake was started following the protocol of Aschenbach et al. (2002). 14C- D-glucose (Amersham Biosciences, Little Chalfont, UK) was added to a final concentration of 200 µmol/L to the bathing solution on the mucosal side (final activity, 16.7 MBq/L). After 1 min of incubation with glucose, epithelia were washed 3 times with ice-cold buffer solution to stop protein-mediated transport processes. Ussing chambers were taken off their holders, and epithelia were transferred quickly to a precooled lysing device. The lysing device consisted of a flat plate on which the epithelia were placed (mucosal side up) and Al cylinders fixed over the epithelia. Epithelial cells were lysed by applying 4 mL of ice-cold NaOH (100 mmol/L) into the Al cylinders for 3 min (exposed area, 0.385 cm2). The lysates were cleared by centrifugation (3,000 x g, 15 min). Glucose contents were determined in the lysate in duplicate. Glucose was measured by scintillation counting after addition of a liquid scintillation fluid (Aquasafe 300 Plus, Zinsser Analytic, Maidenhead, UK).
DON Transport Studies
Isolated epithelia were incubated in D-glucose-free buffer mucosally and D-glucose-(5 mmol/L) containing buffer serosally in Ussing chambers. The epithelia were adapted to experimental conditions for 30 min. Thereafter, DON was introduced to the mucosal side at a final concentration of 1, 5, or 10 mg/L. Unidirectional DON fluxes from the mucosal to the serosal side were determined. At each sampling time (every 30 min), 2 mL of the buffer was withdrawn from the serosal side and replaced by fresh buffer solution. Samples were analyzed for their DON content by HPLC. Mucosal-to-serosal fluxes (J) and apparent permeability (Papp) of DON were calculated from values obtained for serosal DON according to the following formulas: J = dQ/dt·A–1 and Papp = J·C0–1, where dQ/dt = the amount of substance permeating per time unit; A = exposed surface area (i.e., 1.1 cm2); and C0 = the initial concentration in the mucosal chamber.
HPLC with Ultraviolet Detection of DON
The buffer samples from DON transport experiments were analyzed, without any extraction or cleanup, by HPLC with ultraviolet detection. The mobile phase consisted of HPLC-grade water (82%, Fisher Chemical Co., Fairlawn, NJ), methanol (9%), and acetonitrile (9%). One hundred microliters of reconstituted aliquot was injected into the HPLC system with a flow rate of 1 mL/min. The HPLC equipment consisted of an Iso Chrom LC pump (Spectra Physics Co., San Jose, CA) and autosampler AS-2000 (Merck-Hitachi, Tokyo, Japan). Separation of analytes was performed with a Synergy 4µ polar reversed-phase column (250 x 4.6 mm, 4 µm, 80A, Phenomenex, Torrance, CA) and a guard column (4 x 3 mm). The detection was achieved with an ultraviolet detector (Spectra Physics Co.) at 220 nm, and chromatograms were integrated with the help of the software Stratos V.4 (Polymer Laboratories Ltd., Shropshire, UK).
Statistics
Arithmetic means are presented together with their SEM. Data means were compared by Friedman’s repeated measures ANOVA on ranks. Thereafter, Student-Newman-Keuls’ test was used for the multiple comparisons of different treatments. Statements of statistical significance were based on P 
0.05, using the statistical software SigmaStat 2.0 (Systat Software GmbH, Erkrath, Germany). The same software was used to estimate linear regressions parameters.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Glucose uptake was 3.28 ± 0.53 nmol/cm2·min in the control tissues (n = 10; Figure 1
). The contribution of SGLT-1 to total glucose uptake was estimated by inhibiting SGLT-1 with phlorizin. In the presence of phlorizin, glucose uptake was reduced (P < 0.05) to 1.21 ± 0.19 nmol/cm2·min.
|
The effect of DON was tested in the presence and absence of phlorizin. Deoxynivalenol decreased (P < 0.05) the glucose uptake in the absence of phlorizin to 1.81 ± 0.24 nmol/cm2·min. However, it had no additional effect on the glucose uptake in the presence of phlorizin (0.97 ± 0.17 nmol/cm2·min).
DON Transport Studies
In 1 set of DON transport experiments, DON was added at 10 µg/mL on the mucosal side, and its flux was determined in mucosal-to-serosal direction over consecutive 30-min flux periods (Figure 2). Flux rate of DON increased from the first (0 to 30 min) to the second flux period (30 to 60 min) and stayed relatively constant thereafter (30 to 90 min). The mean flux rates of DON in the different flux periods were 181 ± 26 (0 to 30 min), 483 ± 52 (30 to 60 min), 613 ± 111 (60 to 90 min), and 661 ± 91 ng/cm2·h (90 to 120 min). This was equivalent to apparent permeability values of 5.01·10–06, 1.34·10–05, 1.70·10–05, and 1.84·10–05 cm/s, respectively.
|
). The mean flux rate at the different concentrations of DON (1, 5, and 10 µg/mL) was 109 ± 16, 221 ± 31, and 332 ± 34 ng/cm2·h, respectively. Thus, DON transport was proportional to the DON concentration (r = 0.998). The correlation between DON flux rate (J in ng/cm2·h) and the initial DON concentration (C0 in µg/mL) could be described by the following linear regression model: J = (89.1 ± 10.6) + (24.6 ± 1.6) ·C0.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The gastrointestinal tract is the first barrier against ingested chemicals, food contaminants, and natural toxins. Following ingestion of mycotoxin-contaminated food or feed, intestinal epithelial cells can be exposed to high concentrations of toxins (Prelusky et al., 1996; Shephard et al., 1996). Our previous studies in chickens had suggested that the mycotoxin DON decreased both sodium-glucose and sodium-amino acid cotransport (Awad et al., 2004, 2005a,Awad et al., b). The activities of these transport processes were assessed indirectly by changes in Isc. It was thus of interest to analyze the effects of DON on glucose uptake in the intestine of laying hens directly and to elucidate inasmuch the active component of glucose uptake via SGLT-1 is specifically affected.
The results of the present study provided clear evidence that glucose uptake is decreased by 45-min preincubation with DON. The effect of DON was similar to the effect of SGLT-1 inhibition using phlorizin. Furthermore, a combined application of DON and phlorizin reduced D-glucose uptake to the same extent as an application of phlorizin alone. Thus, it can be concluded that the inhibitory action of DON on D-glucose uptake affects specifically the sodium-dependent component via SGLT-1.
The precise mechanism by which DON suppresses the activity of the hen intestinal SGLT-1 is unknown at this time. Previous studies have often ascribed the functional consequences of mycotoxin action to their inhibitory action on RNA and protein synthesis (Rotter et al., 1996). Accordingly, the shortening and thinning of villi in the small intestine of chickens observed in previous investigations after DON feeding (Fairchild et al., 2005; Awad et al., 2006a,b) may suggest that the decrease in glucose absorption observed in this study may just be a consequence of a general impairment of epithelial protein synthesis and function. However, Maresca et al. (2002) reported that low concentrations (<10 µmol/L) of DON applied to human intestinal epithelial cells selectively modulate the activities of specific intestinal transporters, including the D-glucose and D-galactose sodium-dependent transporter, SGLT-1. Based on this study and previous investigations, the DON-sensitive transport in chicken intestine comprise sodium-glucose cotransport by SGLT-1 (Figure 1
; Awad et al., 2005a), L-proline cotransport (Awad et al., 2005b), and amiloride-sensitive sodium transport pathways (Awad et al., 2005a). It is not clear at present whether the interference with these specific intestinal transport pathways occurs mainly at the level of RNA transcription, protein synthesis, or both. The epithelia in the present study were exposed to DON for only 45 min, which might suggest that nontranscriptional inhibition of SGLT-1 could well play a role. Further studies using specific molecular characterization of Na+- D-glucose cotransport after DON exposure may provide a better understanding.
Given the profound effects of DON on nutrient absorption in the small intestine, it is astonishing that poultry performance is often not or only moderately affected by the DON content of feedstuffs (Dänicke et al., 2002; Sypecka et al., 2004). One plausible explanation could be that the decrease in absorption of certain nutrients in the proximal small intestine (Hunder et al., 1991; Awad et al., 2004) displaces absorption to more distal intestinal sites. Chickens are able to absorb D-glucose and amino acids efficiently, even in the large intestine (Bindslev et al., 1997). Future studies should address the question of whether absorptive functions in the large intestine may be better protected against the deleterious effects of DON, either by DON absorption from the proximal digestive tract (see below), by bacterial inactivation of DON, or both (Eriksen et al., 2002).
DON Transport Studies
Very little is known about the metabolism and kinetics of DON when it passes through the digestive tract, which is the first step governing the entry of DON into the organism.
Prelusky et al. (1988), Dänicke et al. (2004a), and Eriksen and Pettersson (2004) have detected DON appearance in the blood of pigs fed with DON-contaminated diets after <30 min following oral exposure to the toxin, with its maximum serum concentration reached 4 h after feeding. The early occurrence of DON in plasma, with its concomitant disappearance from digesta of the small intestine, indicates that the majority of the ingested DON is absorbed in the proximal part of the small intestine. Our data are in agreement with this hypothesis. The time kinetics experiments showed that DON flux rates are quickly equilibrated in the small intestinal epithelium of chickens and that steady state absorption rates are achieved within 30 min (Figure 2). The Papp under steady state conditions was ~1.7·10–05 cm/s. Although there is no comparable data from chicken jejunum in literature, this Papp is roughly comparable to the Papp of human jejunum to mannitol (1.4·10–05 cm/s; Mardones et al., 2004). Mannitol is a small hydrophilic molecule with predominant paracellular permeation. In a recent study in cultures of human colonic epithelial cells (Caco-2), Sergent et al. (2006) had also found very similar Papp for DON (5.0·10–06 cm/s) and the paracellular marker mannitol (3.8·10–06 cm/s). Because Sergent et al. (2006) also found an almost linear increase in DON permeation across Caco-2 cells with increasing DON concentrations, they concluded on a predominantly passive permeation of DON via the paracellular route. In agreement with these results from Caco-2 cultures, Doll et al. (2003) and Dänicke et al. (2004b) found a linear relationship between dietary DON and serum concentrations in pigs. In the present study, we now provide the first report on the concentration dependence of DON absorption directly at the level of the small intestinal epithelium. Our results show that DON transport from the mucosal to the serosal side (i.e., absorption) was directly proportional to its initial concentration (Figure 3). These data suggest that the major part of DON transport across the intestinal epithelium is likely due to simple diffusion. This passive diffusion is probably via the paracellular route. In support of the theory of predominantly passive permeation of DON, in vivo experiments have shown that DON does not accumulate in tissues (Prelusky et al., 1988).
In conclusion, our studies showed that DON (10 mg/L) has a specific inhibitory effect on glucose absorption mediated by SGLT-1. In the longer term, these inhibitory effects of DON on SGLT-1 would be complemented by a decrease of intestinal absorptive area. We reported previously that DON affected small intestinal morphology, especially in the duodenum and the jejunum, as evidenced by shorter and thinner villi. The decrease in villus area and specific inhibition of SGLT-1 by these mycotoxins would commonly impair digestive and absorptive functions.
Also, we found that DON is transported across the chicken intestinal epithelium by using the established Ussing chamber technique. The permeation of DON from the mucosal to the serosal side was proportional to the initial concentration. Absorption kinetics is thus compatible with predominantly passive transfer of DON. At least in part, this passive permeation could be via the paracellular route, although some transcellular permeation may not be ruled out.
Received for publication June 8, 2006. Accepted for publication August 23, 2006.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Aschenbach, J. R., T. Borau, and G. Gäbel. 2002. Glucose uptake via SGLT-1 is stimulated by ß2-adrenoceptors in the ruminal epithelium of sheep. J. Nutr. 132:1254–1257.
Awad, W. A., J. Böhm, 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.
Awad, W. A., J. Böhm, 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.
Awad, W. A., J. Böhm, 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.
Awad, W. A., J. Böhm, E. Razzazi-Fazeli, and J. Zentek. 2005b. Effects of luminal deoxynivalenol and L-proline on electro-physiological parameters in the jejunums of laying hens. Poult. Sci. 84:928–932.
Awad, W. A., J. Böhm, 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. Nutr. Anim. Physiol. 90:32–37.
Bindslev, N., B. A. Hirayama, and E. M. Wright. 1997. Na/D-glucose cotransport and SGLT1 expression in hen colon correlates with dietary Na+. Comp. Biochem. Physiol. A Physiol. 118:219–227.[Medline]
Böhm J. 2000. Fusarientoxine in der Tierernährung. Übersicht Tierern. 28:95–132.
Bondy, G. S., and J. J. Pestka. 2000. Immunomodulation by fungal toxins. J. Toxicol. Environ. Health B Crit. Rev. 3:109–143.[Web of Science][Medline]
Dänicke, S., T. Goyarts, H. Valenta, E. Razzazi, and J. Böhm. 2004a. On the effects of deoxynivalenol (DON) in pig feed on growth performance, nutrients utilization and DON metabolism. J. Anim. Feed Sci. 13:539–556.
Dänicke, S., K. H. Ueberschar, I. Halle, S. Matthes, H. Valenta, and G. Flachowsky. 2002. Effect of addition of a detoxifying agent to laying hen diets containing uncontaminated or Fusarium toxin-contaminated maize on performance of hens and on carryover of zearalenone. Poult. Sci. 81:1671–1680.
Dänicke, S., H. Valenta, and S. Doll. 2004b. On the toxicokinetics and the metabolism of deoxynivalenol (DON) in the pig. Arch. Anim. Nutr. 58:169–180.[Web of Science][Medline]
Doll, S., S. Dänicke, K. Ueberschar, H. Valenta, U. Schnurrbusch, M. Ganter, F. Klobasa, and G. Flachowsky. 2003. Effects of graded levels of Fusarium toxin contaminated maize in diets for female weaning piglets. Arch. Anim. Nutr. 56:263–274.
Eriksen, G., and H. Pettersson. 2004. Toxicological evaluation of trichothecenes in animal feed. Anim. Feed Sci. Technol. 114:205–239.
Eriksen, G. S., H. Pettersson, K. Johnsen, and J. E. Lindberg. 2002. Transformation of trichothecenes in ileal digesta and faeces from pigs. Arch. Tierernahr. 56:263–274.[Web of Science][Medline]
Eriksen, G. S., H. Pettersson, and J. E. Lindberg. 2003. Absorption, metabolism and excretion of 3-acetyl DON in pigs. Arch. Anim. Nutr. 57:335–345.
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.
Hunder, G., K. Schumann, G. Strugala, J. Gropp, B. Fichtl, and W. Forth. 1991. Influence of subchronic exposure to low dietary deoxynivalenol, a trichothecene mycotoxin, on intestinal absorption of nutrients in mice. Food Chem. Toxicol. 12:809–814.
Mardones, P., D. Andrinolo, A. Csendes, and N. Lagos. 2004. Permeability of human jejunal segments to gonyautoxins measured by the Ussing chamber technique. Toxicon 44:521–528.[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.
Prelusky, D., K. Hartin, H. Trenholm, and J. Miller. 1988. Pharmacokinetic fate of 14C-labeled deoxynivalenol in swine. Fundam. Appl. Toxicol. 10:276–286.[Web of Science][Medline]
Prelusky, D. B., H. L. Trenholm, B. A. Rotter, J. D. Miller, M. E. Savard, J. M. Yeung, and P. M. Scott. 1996. Biological fate of fumonisin B1 in food-producing animals. Adv. Exp. Med. Biol. 392:265–278.[Medline]
Razzazi-Fazeli, E., J. Böhm, A. Adler, and J. Zentek. 2003. Fusarientoxine und ihre Bedeutung in der Nutztierfütterung: Eine Übersicht. Wien. Tierarztl. Monatsschr. 90:202–210.
Rotter, B., D. B. Prelusky, and J. J. Pestka. 1996. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48:1–34.[Web of Science][Medline]
Rotter, B. A., B. K. Thomposon, M. Lessard, H. L. Trenholm, and H. Tryphonas. 1994. Influence of exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Fundam. Appl. Toxicol. 23:117–124.[Web of Science][Medline]
Sergent, T., M. Parys, S. Garsou, L. Pussemier, Y. J. Schneider, and Y. Larondelle. 2006. Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol. Lett. 164:167–176.[Web of Science][Medline]
Shephard, G. S., P. G. Thiel, S. Stockenstrom, and E. W. Sydenham. 1996. Worldwide survey of fumonisin contamination of corn and corn-based products. J. AOAC Int. 79:671–687.[Web of Science][Medline]
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.
Sweeney, M. J., and A. D. W. Dobson. 1998. Review: Mycotoxin production by Aspergillus, Fusarium and Penicillium species. Int. J. Food Microbiol. 43:141–158.[Web of Science][Medline]
Sypecka, Z., M. Kelly, and P. Brereton. 2004. Deoxynivalenol and zearalenone residues in eggs of laying hens fed with a naturally contaminated diet: Effects on egg production and estimation of transmission rates from feed to eggs. J. Agric. Food Chem. 52:5463–5471.[Web of Science][Medline]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
