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Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on brain regional neurochemistry of starter pigs and broiler chickens¹

H. V. L. N. Swamy^*, T. K. Smith^*,2 and E. J. MacDonald

^* Department of Animal and Poultry Science, University of Guelph, Guelph, ON N1G 2W1 Canada; and and Department of Pharmacology and Toxicology, University of Kuopio, Fin-70211 Kuopio, Finland

	Abstract

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Two experiments were conducted to compare the effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on brain regional neurochemistry of starter pigs and broiler chickens. A polymeric glucomannan mycotoxin adsorbent (GM polymer) was also tested for its efficacy in preventing Fusarium mycotoxicoses. In Exp. 1, a total of 150 starter pigs (initial weight = 9.3 ± 1.1 kg) were fed five diets (six pens of five pigs per diet) for 21 d. Diets (as-fed basis) included control, 17% contaminated grains, 24.5% contaminated grains, 24.5% contaminated grains + 0.2% GM polymer, and a pair-fed control for comparison with pigs receiving 24.5% contaminated grains. In Exp. 2, 360 1-d-old male broiler chicks were fed for 56 d one of four diets containing the same source of contaminated grains as was fed to pigs. The diets included control, 37% contaminated grains, 58% contaminated grains, and 58% contaminated grains + 0.2% GM polymer (as fed). Neurotransmitter concentrations in the cortex, hypothalamus, and pons were analyzed by HPLC. The following brain neurotransmitter alterations (P 0.05) were observed. In pigs, inclusion of contaminated grains in the diet 1) linearly increased cortex 5-hydroxytryptamine (5HT, serotonin) concentrations, while linearly decreasing hypothalamic tryptophan concentrations; 2) quadratically increased hypothalamic and pons 5-hydroxyindoleacetic acid (5HIAA):5HT ratios, whereas the ratio decreased linearly in the cortex; and 3) linearly increased the ratio of hypothalamic 3,4-dihydroxyphenylacetic acid:dopamine (DA) concentrations, whereas hypothalamic norepinephrine (NRE) and pons DA and homovanillic acid (HVA) concentrations linearly decreased. In broiler chickens, inclusion of contaminated grains in the diet 1) linearly increased concentrations of 5HT and 5HIAA in the pons and 5HT concentrations in the cortex; 2) linearly decreased 5HIAA:5HT ratio; and 3) linearly increased pons NRE, 3-methoxy-4-hydroxyphenylethylene glycol, DA, and HVA concentrations. Supplementation of GM polymer to the contaminated diet decreased (P < 0.05) 5HT and 5HIAA concentrations in the cortex of pigs. It was concluded that the differences in alterations of brain neurochemistry might explain the species differences in the severity of Fusarium mycotoxin-induced feed refusal.

Key Words: Broiler chickens • Fusarium • Mycotoxins • Neurochemistry • Pigs • Vomitoxin

	Introduction

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Deoxynivalenol (DON, vomitoxin) is the most common trichothecene mycotoxin detected globally in contaminated feedstuffs (Placinta et al., 1999). Chronic trichothecene mycotoxicoses in animals are characterized by loss of appetite, reduced weight gains, and increased susceptibility to diseases (Smith, 1992). Pigs are more susceptible to DON toxicity than are poultry (Trenholm et al., 1984). Though fusaric acid (FA) has a low toxicity when present alone in contaminated grains, a synergistic interaction between FA and DON on growth rate of pigs had been demonstrated (Smith et al., 1997).

Purified DON (Prelusky, 1993) and FA (Smith and MacDonald, 1991) have been shown to sequentially elevate brain tryptophan, 5-hydroxytryptamine (5HT, serotonin), and 5-hydroxyindoleacetic acid (5HIAA) concentrations, and this has been linked to a decrease in feed intake (Leathwood, 1987). No such information is available in broiler chickens. The feeding of T-2 toxin, another of the trichothecene mycotoxins, however, increased dopamine (DA) and decreased norepinephrine (NRE) concentrations in brains of broiler chickens, but 5HT concentrations were unaltered (Chi et al., 1981). Swamy et al. (2002b) reported an increased brain 5HIAA:5HT ratio in pigs fed grains naturally contaminated with DON, FA, zearalenone, and 15-acetyl DON, but no such information is available in broiler chickens.

It was hypothesized that the differences in alterations of brain neurochemistry in broiler chickens and starter pigs might be one of the possible mechanisms for species differences in the severity of Fusarium mycotoxin-induced feed refusal. Therefore, two experiments were conducted to determine the effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on regional brain neurochemistry of starter pigs and broiler chickens. A polymeric glucomannan mycotoxin adsorbent (GM polymer) was also tested for its efficacy to prevent Fusarium mycotoxin-induced brain neurotransmitter alterations.

	Materials and Methods

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Experimental Animals
Starter Pigs.
One hundred fifty Yorkshire pigs with an initial BW of 9.3 ± 1.1 kg were housed in floor pens at the Arkell Swine Research Station of the University of Guelph. Five pigs of mixed sexes (gilts and barrows) were randomly allotted to each experimental unit (pen). Each treatment group consisted of 15 gilts and 15 barrows. The ambient temperature was 23 to 25°C. Pens provided 2.25 m² of floor space with one nipple drinker and one stainless steel three-hole feeder per pen. Animals had free access to feed and water and were observed daily for any adverse clinical signs. Lighting was provided for 16 to 18 h daily throughout the experiment.

Broiler Chickens.
Three hundred and sixty 1-d-old male broiler chicks of a commercial strain (Ross x Ross; Maple Leaf Poultry, New Hamburg, ON, Canada) were individually weighed, wing banded, and distributed randomly into groups of 30 chicks per floor pen at the Arkell Poultry Research Station. Chicks were initially maintained at 31°C, and the temperature was subsequently lowered by 2°C/wk to reach 21°C by the end of wk 5 and then maintained for the duration of the experiment. Continuous lighting and water ad libitum were provided throughout the experiment. The birds were vaccinated for infectious bronchitis on farm with one eye drop of Mildvac-Ma5 Mass Type live virus (Intervet Inc., Millsboro, DE) on d 14-after hatching. Both chicken and swine projects were approved by the University of Guelph Animal Care Committee and met the guidelines of the Canadian Council on Animal Care.

Experimental Diets
Starter Pigs.
The experiment comprised six blocks, with time as the basis for blocking. In each block, pigs in a pen were fed one of five diets for 21 d. The control diet (Table 1) was formulated to meet all nutritional requirements of 8- to 20-kg starter pigs (NRC, 1998). The mycotoxin-contaminated diets (Table 1) were formulated by replacing control corn and wheat with corn and wheat naturally contaminated with Fusarium mycotoxins. To evaluate the effect of reduced feed intake alone, a pair-feeding regimen was used. The amount of feed consumed by the five pigs per pen fed the diet containing 24.5% contaminated grains (High) was determined daily. A pen of five pair-fed animals received the same amount of control diet as the pigs fed the High diet had consumed the previous day. The meals for the pair-fed animals were subdivided and provided twice daily. To test the efficacy of GM polymer in preventing Fusarium mycotoxicoses, the High diet was supplemented with 0.2% GM polymer (Mycosorb, Alltech Inc., Nicholasville, KY).

Statistical Analyses
Starter Pigs.
Data from pigs and chickens were subjected to Levene’s homogeneity of variances test before the analysis for treatment differences. Data were analyzed by ANOVA using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC) in a completely randomized block design with subsamples. Each pen with a group of five pigs was an experimental unit. Orthogonal polynomial contrasts were used to determine the nature of the response exhibited in neurotransmitter concentrations to the feeding of graded levels of mycotoxin-contaminated grains. The pigs fed the control diet were compared with pair-fed pigs to determine the effect of reduced feed intake on the measurements. The pair-fed pigs were tested against pigs fed the diet with a high level of contaminated grains to identify any metabolic toxicity of Fusarium mycotoxins. The ability of the GM polymer to prevent Fusarium mycotoxin-induced effects was also tested by a simple contrast between the pigs fed the diets containing a high level of contaminated grains with and without 0.2% GM polymer (Kuehl, 2000). Statements of statistical significance were based on P 0.05.

Broiler Chickens.
Data were analyzed by ANOVA using the GLM procedure of SAS in a completely randomized design with subsamples. Orthogonal polynomial contrasts were used to determine the nature of the response exhibited by neurotransmitter concentrations to the dietary inclusion of contaminated grains. The efficacy of a supplemental GM polymer in preventing Fusarium mycotoxicoses was determined by employing a simple contrast between highly contaminated diets with and without GM polymer (Kuehl, 2000). Statements of statistical significance were based on P 0.05.

	Results

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Starter Pigs
Inclusion of contaminated grains in the diet linearly increased cortex 5HT concentrations, whereas tryptophan concentrations in hypothalamus were linearly decreased (Tables 5 and 6; P 0.05). Hypothalamic and pons 5HIAA:5HT ratios responded quadratically to the inclusion of contaminated grains, whereas the ratios decreased linearly in cortex (Tables 5, 6, and 7; P 0.05). The ratio of hypothalamic DOPAC:DA was linearly increased, whereas NRE concentrations were linearly decreased in response to the inclusion of contaminated grains (Table 5; P 0.05). Pons DA and HVA concentrations linearly decreased with the increase in the inclusion of contaminated grains (Table 7; P 0.05). Supplementation of 0.2% GM polymer to the diet containing 24.5% contaminated grains decreased the 5HT (P < 0.001) and 5HIAA (P = 0.021) concentrations in cortex (Table 6).

Broiler Chickens
Hypothalamic neurotransmitter concentrations were not affected by the inclusion of contaminated grains in the diet (Table 5; P > 0.05). In the pons, dietary inclusion of contaminated grains linearly increased concentrations of 5HT and 5HIAA, and linearly decreased the ratio of 5HIAA:5HT (Table 7) (P 0.05). The concentrations of 5HT in cortex linearly increased with the inclusion of contaminated grains, whereas the 5HIAA:5HT ratio linearly decreased (Table 7; P 0.05).

Dietary inclusion of contaminated grains resulted in a linear increase in pons concentrations of NRE, MHPG, DA, and HVA, whereas there was a linear decrease in DOPAC:DA ratio (Table 6; P 0.05). Supplementation of GM polymer to the contaminated diet increased the hypothalamic 5HIAA:5HT ratio (Table 6; P 0.05).

	Discussion

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Brain Neurotransmitter Concentrations in Pigs
The adverse effects of feeding Fusarium mycotoxin-contaminated grains to pigs can be delineated as 1) reduced feed intake and 2) specific metabolic alterations (Swamy et al., 2003). Rotter et al. (1994) reported lower skin temperature, better feed efficiency, a more corrugated stomach, decreased -globulin levels, and lower antibody titers to sheep red blood cells in pigs consuming Fusarium mycotoxin-contaminated diet compared with the pair-fed control pigs. The appearance of the stomach and antibody titers, however, was not altered in pigs fed contaminated diet compared with pigs fed control diet ad libitum. It can be concluded, therefore, that the effects observed on the stomach appearance and antibody titers do not represent a direct effect of mycotoxins. These effects, however, may be related to the stress of pair feeding. In the current study, brain concentrations of DOPAC and HVA were decreased in pair-fed control pigs compared with those fed the control diet ad libitum. This might indicate the decreased conversion of DA to DOPAC. Chi et al. (1981) correlated these neurochemical changes to stressful effect of T-2 toxin. Lowered serotonergic activity (5HIAA:5HA) of pair-fed control pigs in comparison with pigs fed the control diet ad libitum in the current study further indicate the stress of pair feeding.

In general, acute stress activates the serotonergic, dopaminergic, and noradrenergic neurons (Cooper et al., 1996). This can initially lead to release of neurotransmitters, and thus the ratio of metabolite to amine increases. Many compensatory mechanisms, such as presynaptic receptors, increase in the rate of amine synthesis, and reuptake efficiency, however, soon come into play, and this can make interpretation of data difficult. The metabolite:amine ratio is a very crude index of turnover, and with subacute stress, as was the case in the current study, it is difficult to state the significance of changes. However, changes do reflect stress-induced altered brain neurochemistry.

Although hypothalamic and pons 5HT and 5HIAA concentrations were not significantly altered by the feeding of contaminated diets, the 5HIAA:5HT ratio was elevated in a quadratic fashion. This enhanced ratio indicated that feeding contaminated grains significantly increased the metabolism of 5HT to 5HIAA and is in accordance with previous findings (Swamy et al., 2002b). Pigs fed the high-toxin diet had very high 5HIAA:5HT ratios in the hypothalamus and pons compared with pair-fed pigs. This further illustrated that in spite of the similar nutritional status of pigs fed the above two diets, there was increased metabolism of 5HT to 5HIAA in pigs fed the high toxin diet. The quadratic response of the 5HIAA:5HT ratio indicated that there is a threshold for toxin levels to cause apparent alterations in brain serotonergic neurotransmitter metabolism. The feeding of low levels of contaminated grains may not be sufficient to cause apparent alterations in the 5HIAA:5HT ratio. A decreased 5HIAA:5HT ratio in cortex may be due to the significant increase in the cortex 5HT concentrations. Cortex has relatively less serotonergic activity than does pons and hypothalamus and, therefore, 5HT might not have been metabolized into 5HIAA.

It is evident from the findings of the current study that dopaminergic neurotransmitters in different sections of brain responded differently to the feeding of contaminated grains. Increased hypothalamic DOPAC:DA ratio in the current study might be due to the inhibitory effect of FA on dopamine beta-hydroxylase (Hidaka, 1971). Inhibition of this enzyme can lead to decreased synthesis of NRE, as observed in the current study. If DA cannot be converted to NRE, then it would be metabolized by monoamine oxidase into the inactive metabolite, DOPAC. Lowered NRE concentration in the hypothalamus of pigs fed contaminated grains is consistent with earlier observations (Swamy et al., 2002b) and therefore seems to be a consistent effect of Fusarium mycotoxins. In the pons, on the other hand, DA and HVA concentrations were significantly decreased in the pigs fed contaminated grains, which can be explained by the partial inhibitory effect of FA on tyrosine hydroxylase (Wang and Ng, 1999). Tyrosine is the precursor for the synthesis of DA, DOPAC, and HVA.

In the current study, supplementation of GM polymer to the mycotoxin-contaminated diet significantly reduced mycotoxin-induced increases in cortex 5HT and 5HIAA concentrations. Some beneficial effects of GM polymer in preventing mycotoxin-induced negative effects were earlier reported in livestock and poultry (Raju and Devegowda, 2000; Raymond et al., 2003; Swamy et al., 2002a,b; Aravind et al., 2003).

Brain Neurotransmitter Concentrations in Broiler Chickens
Many experiments in laboratory animals and pigs have suggested altered brain neurotransmitter concentrations as one of the possible mechanisms for Fusarium mycotoxin-induced feed refusal. Chi et al. (1981) investigated the acute effect of T-2 toxin on brain neurochemistry of broiler chickens and observed increased DA, but decreased NRE concentrations. Serotonin concentrations, however, were unaltered. These authors concluded that altered catecholamine concentrations might be due to the stressful effect of T-2 toxin. Altered feed intake and weight gains in the finisher period of the first broiler trial (Swamy et al., 2002a) prompted an investigation of the effects on brain neurochemistry. Neurotransmitter concentrations in the pons were highly influenced by the feeding of contaminated grains, whereas those in hypothalamus were not affected. This is in contradiction to earlier studies in pigs, wherein the neurotransmitter concentrations were affected both in pons and hypothalamus to a similar extent (Swamy et al., 2002b).

Increased DA concentrations in pons of the current study are in agreement with Chi et al. (1981). Deoxynivalenol, like T-2 toxin (but to a lesser extent), can cause inflammation, contact erosion, and irritation, which can be considered chemical stresses (Hunder et al., 1991). Various acute stimuli have been shown to alter catecholamine dynamics. In contrast to Chi et al. (1981), the current study showed elevated NRE concentrations and, therefore, might eliminate the possibility that FA and/or DON had inhibited dopamine ß-hydroxylase enzyme in broiler chickens. Increased HVA and MHPG concentrations in the pons of birds fed contaminated diets further support enhanced dopaminergic activity in the current study. Decreased DOPAC to DA ratio indicated that mycotoxins might have increased the synthesis of HVA via the action of catechol-O-methyl transferase, but not through monoamine oxidase (Cooper et al., 1996).

Enhanced concentrations of 5HT and 5HIAA in pons further supported the concept that Fusarium mycotoxins enhance serotonergic activity in the brain and cause subsequent feed refusal (Prelusky et al., 1992; Prelusky, 1993; Smith and MacDonald, 1991). Decreased 5HIAA:5HT ratios in the pons suggested that the synthesis of 5-HT was increased and there was also increased turnover to 5HIAA. Because the synthesis was more than the release, the ratio dropped slightly. Although the feed intake and weight gain by birds fed contaminated grains recovered during the finisher phase, alterations in brain neurotransmitter concentrations were still apparent. It would be of further interest to study these neurotransmitter changes at the end of starter and grower period as well. The reason for the increase in the 5HIAA:5HT ratio of broilers fed the GM polymer-supplemented diet vs. the unsupplemented contaminated diet is not readily apparent.

Comparison of Brain Neurotransmitter Concentrations in Pigs and Broiler Chickens
In the current study, starter pigs were fed approximately half the amount of mycotoxin-contaminated grains that was fed to broiler chickens. Feed intake and weight gains in starter pigs fed contaminated grains were reduced by 32 and 34%, respectively (Swamy et al., 2003), whereas the decreases in broiler chickens were 15 and 12% (our unpublished observations). It was concluded that starter pigs are more susceptible to the feeding of contaminated grains than are broiler chickens with respect to growth measurements.

Precise mechanisms behind the feed refusal effect of Fusarium mycotoxins are not clear. Previous studies using purified DON and FA, however, have led to the conclusion that altered brain neurochemistry is the most likely cause of Fusarium mycotoxin-induced feed refusal. The current studies using a mixture of Fusarium mycotoxins from naturally contaminated grains clearly implicated altered brain regional neurochemistry as a potential mechanism for the feed refusal effect of Fusarium mycotoxins. Mycotoxin-induced increases in the concentrations of serotonergic neurotransmitters were common to both species, whereas changes in the concentrations of noradrenergic and dopaminergic neurotransmitters varied.

The current studies showed decreased DA, DOPAC, HVA, and NRE concentrations in the pigs fed contaminated diets. The opposite effect, however, was observed in broiler chickens. Though the precise role of these neurotransmitters in mediating mycotoxin-induced altered feeding behavior is not well defined, it is known that the activities of these neurotransmitters form a necessary element of the interneuronal network that regulate control of eating (Prelusky, 1993). The medial hypothalamus of the brain is richly populated both with serotonergic and 2-noradrenergic receptors. The stimulation of these receptors with the neurotransmitters has important implications on feeding behavior. There is strong evidence that serotonergic and 2-noradrenergic systems interact antagonistically through medial hypothalamic satiety mechanisms (Leibowitz and Shor-Posner, 1986). Serotonergic neurotransmitter concentrations were increased, whereas NRE concentrations were decreased in the brains of pigs fed contaminated grains. The lack of an antagonistic interaction of these two systems on feed intake might explain feed refusal in pigs. In contrast, both NRE and serotonergic neurotransmitter concentrations were increased in broiler chickens, thus permitting the possible antagonistic interaction between two systems. This situation might explain the less severe feed refusal seen in broiler chickens.

Glucomannan polymer has a greater effect in swine than in poultry in preventing mycotoxin-induced brain neurotransmitter alterations. This difference may be a result of the greater role of neurotransmitters in Fusarium mycotoxin-induced reduced feed intake in pigs than in broiler chickens.

	Implications

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Altered brain regional neurochemistry in pigs and broiler chickens chronically fed Fusarium mycotoxin-contaminated diets provided a mechanistic basis for the negative effect of Fusarium mycotoxins on feed intake. The pattern of brain neurotransmitter alterations, however, differed between the two species, which might explain species differences in the severity of reduced feed intake and the subsequent growth depression. These findings suggest that caution should be exercised in diverting Fusarium mycotoxin-contaminated grains from swine to poultry feed.

	Footnotes

 
¹ This study was supported by the Ontario Ministry of Agriculture and Food and by Alltech Inc., Nicholasville, KY.

² Correspondence—phone: 519-824-4120, ext. 53746; fax: 519-822-7897; e-mail: tsmith{at}uoguelph.ca.

Received for publication September 26, 2003. Accepted for publication March 22, 2004.

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