J. Anim Sci. 2006. 84:2361-2366. doi:10.2527/jas.2005-699
© 2006 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Effects of feeding grains naturally contaminated with Fusarium mycotoxins with and without a polymeric glucomannan mycotoxin adsorbent on reproductive performance and serum chemistry of pregnant gilts1
G. Díaz-Llano and
T. K. Smith2
Department of Animal and Poultry Science, University of Guelph, Guelph, ON, N1G2W1, Canada
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Abstract
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Contamination of animal feedstuffs with Fusarium mycotoxins can cause reduced feed intake and hyperaminoacidemia resulting from reduced hepatic protein synthesis. The current study investigated the effects of feeding grains naturally contaminated with Fusarium mycotoxins on reproductive performance, serum chemistry, ADFI, and ADG of gilts, and tested the ability of a polymeric glucomannan mycotoxin adsorbent (GMA) to reduce or eliminate the effects of the contaminated feeds. Thirty-six Yorkshire gilts were fed 3 diets (n = 12 gilts/diet) from 91 ± 3 d of gestation until farrowing. Diets included 1) control, 2) contaminated grains, and 3) contaminated grains + 0.2% GMA. Diets contaminated with Fusarium mycotoxins did not affect ADFI (P = 0.24), but ADG (P = 0.029) and G:F (P = 0.047) were reduced. Serum concentrations of ß-hydroxybutyrate, haptoglobin, protein, albumin, globulin, urea, glucose, cholesterol, Ca, Na, Mg, P, K, and Cl, and hepatic enzyme activities were not affected by diet. The frequency of stillborn piglets was greater (P = 0.03) for gilts fed contaminated grains compared with that of gilts fed contaminated grains + GMA. The feeding of contaminated grains + GMA also increased (P = 0.026) the percentage of pigs born alive compared with gilts fed the contaminated diets. In conclusion, feeding gilts diets that are naturally contaminated with Fusarium mycotoxins can increase the incidence of stillborn piglets and this effect can be reduced by dietary supplementation with GMA.
Key Words: deoxynivalenol • Fusarium • gilt • metabolism • mycotoxin • reproduction
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INTRODUCTION
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Deoxynivalenol (DON) is a Fusarium trichothecene mycotoxin produced by numerous Fusarium species, including Fusarium graminearum, Fusarium culmorum, Fusarium tricinctum and Fusarium acuminatum. The domestic species most sensitive to feedborne DON is swine (Concova et al., 2003
).
Deoxynivalenol is known to reduce feed intake in swine because of reduced hepatic protein synthesis resulting in hyperaminoacidemia and elevated blood tryptophan concentrations. This results in increased brain uptake of tryptophan across the blood–brain barrier. Tryptophan is the precursor of serotonin and elevated brain serotonin concentrations can result in reduced appetite (Leathwood, 1987). If DON is accompanied by fusaric acid as a cocontaminant, the loss of appetite is greater. This is because fusaric acid competes with tryptophan for binding to blood albumin and, therefore, increases concentrations of free tryptophan in blood. The result is increased brain uptake of free tryptophan and increased serotonin synthesis. This is the basis of the toxicological synergism between DON and fusaric acid (Smith et al., 1997).
There are few reports concerning the effects of feeding gilts grains naturally contaminated with Fusarium mycotoxins during gestation. Gilts fed with naturally contaminated wheat containing 3.45 mg of DON/kg of feed exhibited a significant reduction in feed intake, BW gain, fetal length, and fetal weight at 50 to 54 d of gestation (Friend et al., 1983). Chavez (1984) reported that the feeding of gilts with diets based on naturally contaminated wheat to provide 1.3, 2.4, or 3.3 mg of DON/kg of feed for the last 90 d of pregnancy did not suffer reduced feed intake, although a significant reduction in BW gain was observed with the feeding of 3.3 mg of DON/kg of feed.
The current experiment was conducted to determine the effect of feeding grains naturally contaminated with Fusarium mycotoxins with and without a polymeric glucomannan mycotoxin adsorbent (GMA) on reproduction and metabolism in pregnant gilts.
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MATERIALS AND METHODS
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Experimental Animals and Diets
All animal care and protocol practices were approved by the University of Guelph Animal Care Committee and met the guidelines of the Canadian Council on Animal Care.
To prevent mummies and stillbirths, all gilts were vaccinated i.m. at 130 to 160 d of gestation with 2 mL of porcine reproductive respiratory syndrome virus (Ingelvac PRRS MLV, Boehringer Ingelheim, Vetmedica, Inc., St. Joseph, MI) and 5 mL of parvovirus vaccine (Farrowsure Plus B, Pfizer, Exton, PA). Three weeks later, booster injections of 5 mL of Farrowsure plus B were administered to all gilts. Five weeks before farrowing, 2 mL of Escherichia coli bacterin toxoid (Litterguard LT, Pfizer) and 5 mL of Farrowsure Plus B were administered to each gilt.
The experiment was conducted between the last week of September 2004 and the last week of March 2005. All females were first-parity Yorkshire gilts. Gilts were bred by AI using pooled semen from 3 boars. If estrus was detected in the morning, gilts were bred in the afternoon and 24 h later. If estrus was detected in the afternoon, gilts were bred the next morning and 24 h later. On d 35 after breeding, pregnancy status was evaluated by transabdominal ultrasonography in those gilts that did not return to estrus. Pregnancy status was not reconfirmed before the beginning of the experiment.
Thirty-six gilts at 91 ± 3 d of pregnancy were selected from the breeding herd described above. The experimental design included 12 blocks, 1 replication per block, and 3 diets. Gilts were assigned randomly to each treatment in each block. Each new group entering the study was treated as a new block. The experimental diets were based on corn, wheat, and soybean meal, and were formulated to be isoenergetic and isonitrogenous (Table 1), and to meet or exceed all nutritional requirements of pregnant sows (National Research Council, 1998). The allowance of feed during the experimental period was 2.4 kg/gilt per d. Refused feed was collected and weighed daily, and gilts had ad libitum access to water supplied by nipple waterers. Gilts were housed in individual stalls (0.61 x 2.0 m), in a closed building at the Arkell Swine Research Station of the University of Guelph; the temperature of the building was maintained at 22 ± 2°C.
Contaminated corn, control corn, contaminated wheat, and control wheat were analyzed for CP, fat, NDF, ash, GE, and DM (Table 2). Soybean meal was analyzed for CP. All analyses were conducted according to the Association of Official Analytical Chemists (AOAC, 1980). Diets included (as-fed basis) 1) control (0.2 mg of DON/kg); 2) contaminated grains (5.5 mg of DON/kg, 0.5 mg of 15-acetyl DON/kg, and 0.3 mg of zearalenone/kg); and 3) contaminated grains (5.7 mg of DON/kg, 0.5 mg of 15-acetyl DON/kg, and 0.3 mg of zearalenone/kg) + 0.2% of a GMA (Mycosorb, Alltech Inc., Nicholasville, KY; Table 3).
Analysis of Dietary Mycotoxins
All diets were analyzed at the Veterinary Diagnostic Laboratory of North Dakota State University (Fargo) to determine the contents of DON, 15-acetyl DON, 3-acetyl DON, T-2 tetraol, fusarenone-X, diacetoxyscir-penol, T-2 triol, T-2 toxin, iso-T-2 toxin, scirpentriol, nivalenol, 15-acetoxyscirpenol, neosolaniol, HT-2 toxin, acetyl T-2 toxin, zearalenol, zearalenone, aflatoxin, and fumonisin, using gas chromatography-mass spectrometry, as described by Raymond et al. (2003). Whereas DON, 15-acetyl DON, and zearalenone were detected, all of the other mycotoxins were below the limit of detection. The practical sensitivity (as-fed basis) was 0.02 mg/kg for aflatoxin, 2.0 mg/kg for fumonisin, and 0.2 mg/kg for all the other mycotoxins tested.
Experimental Variables
Gilts were weighed individually on d 1, 7, and 14 of the experiment. The number and BW of newborn piglets were recorded, as were the number of stillborn and mummified piglets.
Blood was collected on d 14 from the retro-orbital sinus of each gilt into vials that did not contain anticoagulant. Serum concentrations of ß-hydroxybutyrate, haptoglobin, total protein, albumin, globulin, glucose, urea, cholesterol, creatinine, and bilirubin, and activities of alkaline phosphatase, glutamate dehydrogenase, aspartate aminotransferase, 
-glutamyltransferase, and creatine kinase were determined using a Hitachi 911 autoanalyzer (Roche Diagnostics, Division of Hoffman-LaRoche, Ltd., Montreal, QC, Canada).
Statistical Analysis
Data were analyzed by ANOVA using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC) as a completely randomized block design with 3 treatments in 12 blocks. Each gilt represented an experimental unit for all variables tested. The independent variables were the experimental diets. Dependent variables were ADFI, ADG, serum chemistry, liver enzyme activities, stillbirth rate, born alive, and BW of the litter at birth.
To assess the effects of feeding mycotoxin-contaminated grains to the gilts, contrasts between the mycotoxin-contaminated diets and the controls were made. Similarly, to assess the efficacy of GMA in preventing the effects of the feeding of Fusarium mycotoxin-contaminated grains, contrasts of data from gilts fed the contaminated diet and gilts fed the contaminated diet supplemented with 0.2% GMA were made. Contrasts between control and GMA were also made to determine if GMA prevented the effects of Fusarium mycotoxins. Means were compared by Tukey’s multiple comparison test, and significance was declared at P < 0.05.
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RESULTS
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Chemical Composition of Raw Materials and Mycotoxin Content of Diets
Crude protein, NDF, fat, and ash were greater for both contaminated corn and contaminated wheat compared with control corn and control wheat, respectively (Table 1
). Concentrations of mycotoxins in the contaminated diets were similar for zearalenone, 15-acetyl DON, and DON (Table 3). There was a combination of Fusarium mycotoxins in both the contaminated diet and in the contaminated diet + GMA (Table 3).
Feed Intake, BW Change, and G:F of Gilts
The average BW of gilts on d 0 was 180 ± 2.76 kg and did not differ among dietary groups. There were no differences in ADFI between gilts fed control and contaminated diets (P = 0.24; Table 4). There was a reduction in ADG resulting from the feeding of contaminated grains (P = 0.03; Table 4) compared with the feeding of the control diet. Average daily gain was not different (P = 0.63; Table 4) when gilts fed the control diet and the diet containing contaminated grains + GMA were compared. Gain to feed was reduced for gilts fed the contaminated diet compared with controls (P = 0.047; Table 4), but there were no differences between gilts fed contaminated diets and gilts fed contaminated diets supplemented with GMA (P = 0.26; Table 4).
Serum Chemistry
There was no effect of diet on serum concentrations of ß-hydroxybutyrate, haptoglobin, total protein, albumin, globulin, albumin:globulin ratio, urea, creatinine, glucose, cholesterol, or on activities of alkaline phosphatase, -glutamyltransferase, aspartate aminotransferase, creatine kinase, glutamate dehydrogenase, total bilirubin, conjugated bilirubin, free bilirubin, calcium, phosphorus, magnesium, sodium, potassium or chloride after feeding gilts for the 14-d period (data not shown).
Reproductive Performance
The percentage of stillbirths was greater for litters of gilts fed the contaminated diet compared with litters of gilts fed with the contaminated diet + GMA (P = 0.03; Table 4) and there was a trend for an increased percentage of stillbirths in litters of gilts fed the contaminated diet compared with control gilts (P = 0.07; Table 4). No differences were observed between litters of gilts fed the control diet compared with litters of gilts fed the contaminated diet + GMA (P = 0.91; Table 4). Piglets born alive as a percentage of total born was reduced for litters of gilts fed the contaminated diet compared with litters of gilts fed the contaminated plus GMA diet (P = 0.03; Table 4). There was no effect of diet on frequency of mummies at birth, total born, or piglets’ BW at birth (Table 4).
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DISCUSSION
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Differences found in raw material composition are similar to those of Friend et al. (1982), Hamilton and Trenholm (1984), and Friend et al. (1986) who reported that contaminated wheat had increased CP content compared with controls. Friend et al. (1982) also found that contaminated wheat had greater values for CP compared with control wheat.
Small differences in concentrations of mycotoxins in diets are a common finding because of uneven distribution of mycotoxins in grains (Davis et al., 1980), errors in sampling, deterioration in storage, and variability in laboratory analysis (Friend et al., 1983). The feeding of grains contaminated naturally with several mycotoxins sometimes has been shown to result in toxicological synergy (Smith et al., 1997).
The lack of differences in ADFI may be explained by the fact that feed intake was restricted to a maximum of 2.4 kg/gilt per d. Differences in ADG are in agreement with Chavez (1984) who reported that pregnant gilts that were fed a diet containing 3.3 mg/kg of DON exhibited a significant reduction in ADG during the last 90 d of gestation compared with gilts fed an uncontaminated diet. This occurred even though the gilts did not have any differences in feed intake during gestation. However, Friend et al. (1983) reported linear reductions in feed intake and BW gain to increasing concentrations of dietary DON in gilts fed ad libitum from d 1 post-breeding until d 51 of pregnancy. Diets in that study contained DON at 0.13, 1.73, and 3.45 mg/kg of BW. The feeding of grain that is naturally contaminated with Fusarium mycotoxins has been shown previously to reduce growth and feed intake of weaned piglets by 34.6 and 32.6%, respectively (Swamy et al., 2002). Feed efficiency was affected for 0 to 7 d and the ratio of 5-hydroxyindoloacetic acid to 5-hydroxytryptamine was increased in the pons. This may explain the decreases in feed intake, emesis, and other behavioral changes in swine consuming Fusarium-contaminated diets. Feeding Fusarium mycotoxins was also shown to reduce the release of dopamine, norepinephrine, and 3,4-dihydroxyphenylacetic acid from the pons (Swamy et al., 2002).
In the present experiment, no emesis was observed in any gilt fed 0.07 mg of DON/kg of BW. Forsyth et al. (1977) reported that the minimal oral dose of DON that resulted in emesis in 9.3-kg pigs was 0.2 mg/kg of BW. This does not include the contributions of conjugated DON (Berthiller et al., 2005) or fusaric acid (Smith and MacDonald, 1991). This is in agreement with Chavez (1984) who fed DON to gilts during gestation and lactation and observed no emetic effects. Friend et al. (1983) also observed no emesis in gilts fed 3.45 mg of DON/kg of BW from breeding until the d 51 of pregnancy.
In the current study, no effects of the feeding of Fusarium mycotoxin-contaminated diets were observed on the serum chemistry variables evaluated. Previous studies involving gilts did not examine these variables (Friend et al., 1983; Chavez, 1984). However, no effects of DON on serum chemistry variables, similar to those measured in the current study, have been observed in piglets (Lun et al., 1985; Prelusky et al., 1994). Swamy et al. (2002) reported no effects of a Fusarium mycotoxin-contaminated diet on activity of L-galactonolactone dehydrogenase or -glutamyltransferase. In the same study there were reductions in serum calcium and phosphorus concentrations due to feeding Fusarium mycotoxin-contaminated diets as well as an increase in serum chloride concentrations. There were no effects observed on other serum chemistry variables.
In the current experiment, the stillbirth rate was greater for piglets from gilts that were fed the contaminated diet compared with gilts fed the contaminated diet supplemented with GMA. These data strongly suggest that the Fusarium mycotoxins caused the increase in the number and percentage of stillborns from gilts that were fed the contaminated diet. To the best of our knowledge, this is the first finding that describes greater percentages of stillborns in gilts fed combinations of Fusarium mycotoxins including DON, 15-acetyl DON, and zearalenone. This finding disagrees with Chavez (1984), who reported no effects on reproduction of the feeding of 3.3 mg of DON/kg to gilts during gestation. Miller et al. (1973) reported that stillbirth, splayleg, and weak newborn piglet syndrome could be caused by feeding gilts a gestation diet containing 50 to 75 µg of zearalenone per 100 g of feed. Simultaneous infection with FS 59E/63 virus during the period that sows were fed the contaminated diet in the study of Miller et al. (1973) may have exaggerated the toxic challenge of zearalenone. Those experimental sows did not demonstrate clinical titers of the virus, suggesting that the viral agent was not the direct cause of the syndrome. Splayleg was not observed in the current experiment.
Despite the low content of zearalenone found in the experimental diets, it is important to take into account the possibility of the presence of masked zearalenone in diets in the form of zearalenone-4ß-D-glucopyranoside. This compound was found in 42% of wheat samples containing zearalenone and correlated with those of zearalenone concentration (r2 = 0.86 and b = 0.10; Schneweis et al., 2002).
Reductions in the percentages of stillborn piglets and increases in piglets born alive in gilts that were fed contaminated diets with GMA vs. those contaminated without GMA indicates that this polymeric glucomannan mycotoxin adsorbent may be protective against Fusarium mycotoxins. The use of GMA may reduce the challenge of Fusarium mycotoxins to the fetuses, and decrease circulating concentrations of toxic metabolites in the gilts. Mummies at birth were not affected by diet because contaminated diets were fed to gilts only at the end of gestation. Total piglets born per litter and BW of piglets at birth were also not affected by diet. These results are in agreement with Chavez (1984) who reported that dietary DON concentrations did not affect litter size, BW, or piglet size at birth.
In summary, we concluded that feeding diets containing grains naturally contaminated with Fusarium mycotoxins to first-parturition gilts from 91 ± 3 d of gestation until farrowing did not reduce ADFI. A reduction in ADG was seen regardless of the lack of effect on ADFI. The lack of an effect of Fusarium mycotoxins on feed intake may have occurred because the feed allowance for the gilts was restricted to 2.4 kg/d. The lack of effect of diet on serum chemistry may reflect the low doses of Fusarium mycotoxins fed per kg of BW. The current study provided experimental evidence indicating that diets contaminated with Fusarium mycotoxins can have toxic effects on fetuses near the end of gestation and these effects could be prevented by the inclusion of GMA in the diets.
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IMPLICATIONS
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Supplementation of glucomannan mycotoxin adsorbent to feed that is naturally contaminated with Fusarium mycotoxins reduces the stillbirth rate compared with contaminated feed without added glucomannan mycotoxin adsorbent.
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Footnotes
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1 This study was supported in part by the Ontario Ministry of Agriculture, Food and Rural Affairs and Alltech Inc. (Nicholasville, KY). The authors thank the staff of the Arkell Swine Research Center including Tom Parker and Troy McElwaine for the valuable help in the management and care of the gilts. The assistance of Mojtaba Yegani during the experimental period is appreciated, as is the expert help of Norman Lindsay in feed manufacturing. 
2 Corresponding author: tsmith{at}uoguelph.ca
Received for publication December 6, 2005.
Accepted for publication March 16, 2006.
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LITERATURE CITED
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AOAC. 1980. Official Methods of Analysis. 13th ed. Association of Official Analytical Chemists, Washington, DC.
Berthiller, F., C. Dall’Asta, R. Schuhmacher, 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][Medline]
Chavez, E. R. 1984. Vomitoxin-contaminated wheat in pig diets: Pregnant and lactating gilts and weaners. Can. J. Anim. Sci. 64:717–723.
Concova, E., A. Laciakova, G. Kovac, and H. Seidel. 2003. Fusarial toxins and their role in animal diseases. Vet. J. 165:214–220.[CrossRef][Medline]
Davis, N. D., J. W. Dickens, R. L. Freie, P. B. Hamilton, O. L. Showell, 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. AOAC 63:95–102.
Forsyth, D. M., T. Yoshizawa, N. Morooka, and J. Tuite. 1977. Emetic and refusal activity of deoxynivalenol to swine. Appl. Environ. Microbiol. 34:547–552.[Abstract/Free Full Text]
Friend, D. W., B. K. Thompson, H. L. Trenholm, K. E. Hartin, and D. B. Prelusky. 1986. Effects of feeding deoxynivalenol (DON)-contaminated wheat diets to pregnant and lactating gilts and on their progeny. Can. J. Anim. Sci. 66:229–236.
Friend, D. W., H. L. Trenholm, J. I. Elliot, B. K. Thompson, and K. E. Hartin. 1982. Effect of feeding vomitoxin-contaminated wheat to pigs. Can. J. Anim. Sci. 62:1211–1222.
Friend, D. W., H. L. Trenholm, P. S. Fiser, B. K. Thompson, and K. E. Hartin. 1983. Effect on dam performance and fetal development of deoxynivalenol (vomitoxin) contaminated wheat in the diet of pregnant gilts. Can. J. Anim. Sci. 63:689–698.
Hamilton, R. M. G., and H. L. Trenholm. 1984. Observations on the chemical and nutritive content of winter and spring wheats contaminated with deoxynivalenol (vomitoxin). Anim. Food Sci. Technol. 11:293–300.[CrossRef]
Leathwood, D. 1987. Tryptophan availability and serotonin synthesis. Proc. Nutr. Soc. 46:143–156.[CrossRef][Medline]
Lun, A. K., L. G. Young, and J. L. Lumsden. 1985. The effects of vomitoxin and feed intake on the performance and blood characteristics of young pigs. J. Anim. Sci. 61:1178–1185.[Abstract/Free Full Text]
Miller, J. K., A. Hacking, J. Harrison, and V. J. Gross. 1973. Stillbirths, neonatal mortality and small litters in pigs associated with the ingestion of Fusarium toxin by pregnant sows. Vet. Rec. 93:555–559.[Medline]
National Research Council. 1998. Nutrient Requirements of Swine. Natl. Acad. Sci., Washington, DC.
Prelusky, D. B., R. G. Gerdes, K. L. Underhill, B. A. Rotter, P. Y. Jui, and H. L. Trenholm. 1994. Effects of low-level dietary deoxynivalenol on haematological and clinical parameters of the pig. Nat. Toxins 2:97–104.[Medline]
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]
Schneweis, I., K. Meyer, G. Engelhardt, and J. Bauer. 2002. Occurrence of zearalenone-4-ß-D-glucopyranoside in wheat. J. Agric. Food Chem. 50:1736–1738.[CrossRef][Medline]
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. MacMillan, 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]
Swamy, H. V. L. N., T. K. Smith, E. J. MacDonald, H. J. Boermans, and E. J. Squires. 2002. Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on swine performance, brain regional neurochemistry, and serum chemistry and the efficacy of a polymeric glucomannan mycotoxin adsorbent. J. Anim. Sci. 80:3257–3267.[Abstract/Free Full Text]
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Abstract
INTRODUCTION
