ENVIRONMENT AND HEALTH
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1 ENVIRONMENT AND HEALTH The Toxicity of Purified Fumonisin B 1 in Broiler Chicks 1 M. H. Henry,* R. D. Wyatt, 2, * and O. J. Fletcher *Department of Poultry Science, University of Georgia, Athens, Georgia 30602; and College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina ABSTRACT An investigation of the toxicity of fumonisin FB 1 /kg were significantly lower than those of the chicks B 1 (FB 1 ), a toxic metabolite of Fusarium moniliforme, in broiler chicks was conducted. Purified FB 1 (98.1% pure) was incorporated into the diets of broiler chicks at 0, 20, 40, and 80 mg/kg, and fed to chicks from 0 to 21 d of age. Dietary FB 1, at concentrations of 80 mg/kg or less, did not adversely affect body weight, feed efficiency, or water consumption of broiler chicks. The relative weights of the liver, spleen, kidney, proventriculus, and bursa of Fabricius were also unaffected (P < 0.05) by any dietary concentration of FB 1 compared with the control (0 mg/ kg) group. Total liver lipids of chicks fed 40 or 80 mg fed either 0 or 20 mg FB 1 /kg of feed. Liver sphinganine concentration and the sphinganine:sphingosine ratio were increased significantly in all treated groups. Chicks fed dietary FB 1 at 80 mg/kg had significantly higher serum glutamate oxaloacetate aminotransaminase:aspartate aminotransferase ratios and levels of free sphinganine in the serum. The results of this investigation agree with the results previously described, in which FB 1 was supplied to diets from the use of F. moniliforme-contaminated grain; therefore, the use of such material as the source of the mycotoxin in animal feeding studies is appropriate. (Key words: fumonisin B 1, sphinganine, sphingosine, Fusarium moniliforme, mycotoxin) 2000 Poultry Science 79: INTRODUCTION Fusarium moniliforme is a widespread, phytopathogenic mold found as a contaminant on many crops, including corn, rice, wheat, barley, peanut, cotton, sorghum, and sugarcane (Moubasher et al., 1972; Bain, 1973; Lagiere, 1973; Warren and Kommedahl, 1973; Hacking et al., 1976; Jeschke et al., 1987; Ogawa and Takeda, 1990; Tsung-Che et al., 1995). Corn contaminated with F. moniliforme has been demonstrated to cause leukoencephalomalacia (LEM) in horses (Marasas et al., 1976; Kriek et al., 1981) and donkeys (Wilson, 1971), porcine pulmonary edema syndrome (PPE) in pigs (Kriek et al., 1981), and liver cancer in rats (Gelderblom et al., 1988). Fusarium moniliforme-contaminated culture material has been shown to induce toxic responses, including increased mortality, reduced size of the bursa of Fabricius, thymus, and spleen, decreased body weight gain, myocardial degeneration, myocardial hemorrhage, alterations in the hemostatic mechanism, and necrosis of hepatocytes, when fed to chickens, ducklings, and turkey poults (Jeschke et al., 1987; Engelhardt Received for publication February 17, Accepted for publication May 24, Supported in part by State and Hatch funds allocated to the Georgia Agricultural Experiment Stations of The University of Georgia. 2 To whom correspondence should be addressed: rwyatt@arches. uga.edu. et al., 1989; Marijanovic et al., 1991; Javed et al., 1993; Weibking et al., 1993b; Espada, et al., 1997). Fusarium moniliforme is known to produce several secondary metabolites in nature, such as moniliformin, fusarins, fusaric acid, fusariocins, and zearalenone. These toxins cause various metabolic and physiologic disorders when consumed by poultry and other animals. Another family of metabolites, the fumonisins, were extracted and purified from a culture of F. moniliforme (Gelderblom et al., 1988), and later were found to be produced naturally in corn (Sydenham et al., 1990). The major metabolite in this group is fumonisin B 1 (FB 1 ). Fumonisin B 1 produced by F. moniliforme has induced LEM in horses by injection (Marasas et al., 1988), and has induced PPE and hydrothorax in swine by both injection and dietary intake of the toxin (Harrison et al., 1990). Fumonisin B 1 also possesses cancer-promoting activity when fed to rats (Gelderblom et al., 1988). Several natural outbreaks of fusariotoxicosis in birds have occurred in which F. moniliforme was isolated from the feed (Wyatt et al., 1972; Jeschke et al., 1987; Windingstad et al., 1989). In studies to determine the effects of fumonisin on broiler chicks, F. moniliforme-contaminated culture material with known concentrations of FB 1 was incorporated into the diets of poultry. For example, turkey Abbreviation Key: FB 1 = fumonisin B 1 ;LEM= leukoencephalomalacia; PPE = porcine pulmonary edema; SGOT:ASP = serum glutamate oxaloacetate aminotransaminase:aspartate aminotransferase. 1378
2 FUMONISIN TOXICOSIS IN BROILERS 1379 poults were fed FB 1 at concentrations of either 100 or 200 mg/kg of feed (Ledoux et al., 1992b), and in another study, broiler chicks were fed diets containing F. moniliforme-culture material with dietary FB 1 concentrations of 75, 150, 225, 300, 375, 450, or 525 mg/kg (Weibking et al., 1993a). Similarly, Brown et al. (1992) studied the effects of FB 1 (300 mg/kg) on broiler chicks by incorporating F. moniliforme-contaminated culture material into feed. The results of these experiments demonstrated that F. moniliforme-contaminated diets containing FB 1 adversely affected the performance and other physiological functions of poultry. Because F. moniliforme is known to produce several different mycotoxins, all of the responses in animals associated with the feeding of F. moniliforme-culture material may not be attributable solely to FB 1. The accurate characterization of FB 1 toxicosis in poultry has been hampered by the difficulties associated with the production and purification of large quantities of FB 1. Recently, our laboratory has successfully produced and purified sufficient quantities of FB 1 for animal feed studies. This study, therefore, was conducted to determine the responses of broiler chickens to pure FB 1 and compare the observed responses to pure FB 1 with those observed in other studies in which F. moniliforme-culture material and purified FB 1 were used as the sources of the toxin. MATERIALS AND METHODS Day-old male broiler chicks (Arbor Acres) were obtained from a local commercial hatchery and placed in an electrically heated battery brooder with wire floors and continuous fluorescent illumination. The chicks were weighed and separated into 20 pens, with six chicks per replicate pen. Five replicate pens per treatment group were distributed randomly throughout the battery brooder. A total of 120 birds were used in this feeding study. Brooder temperatures of 35 to 39 C and room temperatures of 23 to 28 C, with fan ventilation, were maintained during the entire experiment. The FB 1 used in this study was produced by growing F. moniliforme MRC 826 on sterile, moist, yellow corn. The mold was grown on sterile corn in Fernbach flasks containing 600 g of sterile corn, with the moisture content adjusted to 28% by the aseptic addition of sterile, deionized water. The inoculum was prepared by growing the mold on potato dextrose agar 3 slants for 14 d at 30 C. Sterile water containing 0.005% Triton X was added to each slant culture to cover the entire surface of the mold and shaken gently, and the diluent was recovered from each slant with a sterile pipet. The combined spore suspensions were found to contain viable spores/ml of diluent using dilution and pour-plate meth- 3 Difco Laboratories, Detroit, MI Sigma Chemical Co., St. Louis, MO Waters, Milford, MA EM Separations, Gibbstown, NJ odology, with potato dextrose agar as the plating medium. Each flask of sterile, moist corn was inoculated with viable spores of F. moniliforme and shaken vigorously to insure uniform inoculation of the substrate. All cultures were then incubated statically for 42 d at 25 C. Following incubation, the moldy corn was dried at 60 C for 24 h in a forced-draft oven, and then finely ground to a particle size of <1.0 mm. The FB 1 in the moldy corn was extracted and purified by the methods of Javed et al. (1993) and Gelderblom et al. (1988) with modifications. The extraction solvent was water:acetic acid (95:5, vol:vol), and extraction of the FB 1 from the ground corn was facilitated by sonication of the substrate and extraction solvent mixture in an ultrasonic cleaner for 30 min. Isolation and purification of the FB 1 was attained by use of Amberlite XAD-16 4 as described by Gelderblom et al. (1988) followed with passage of the combined fractions containing only FB 1 through a column (400 mm 20 mm inside diameter) containing 100 g of µbondapak C The FB 1 was eluted from this column with acetonitrile:water (30:70, vol:vol), and 25-mL fractions were collected. Because F. moniliforme produces FB 1,FB 2, and FB 3, the fractions containing only FB 1 were determined by assessment of each fraction by thin layer chromatography, using cm silica gel 60 6 chromatograms in unlined glass developing tanks containing acetonitrile:water (85:15, vol:vol) as the developing solvent. An aliquot (5 µl) of each fraction was spotted on the chromatogram, developed to within 2 cm of the top of the chromatogram, airdried, and sprayed with 0.5% p-anisaldehyde in methanol:sulfuric acid:acetic acid (85:5:10, vol:vol:vol). After spraying, the chromatograms were heated at 110 C for 5 min (Sydenham et al., 1990), and the various fumonisins were detected and identified when compared with an authentic standard of the three fumonisins. 4 The recovered fractions containing only FB 1 were combined. Purity of the isolated and purified FB 1 was determined to be 98.1% using the HPLC method of Shephard et al. (1990) as modified by Chamberlain et al. (1993). The University of Georgia standard unmedicated broiler starter ration served as the basal ration. The purified FB 1 was dissolved in a minimal volume of water and incorporated into the basal diet to attain concentrations of 0, 20, 40, and 80 mg/kg of feed. Each diet was fed ad libitum to five replicates of six chicks from 1 d to 3 wk of age. A total of 120 birds were used in this feeding study. Individual body weights of chicks and total feed and water consumption of replicate pens were determined at 7, 14, and 21 d. On Day 21, a 3-mL blood sample was taken from each bird. The blood was placed in sterile test tubes, allowed to clot, and then placed in a refrigerator to facilitate clot retraction and serum expression. After collection, the serum was pooled by replicate and stored frozen until analysis. The pooled serum samples were analyzed for total protein, albumin, globulin, glucose, cholesterol, triglycerides, calcium, sodium, potassium, chloride, uric acid, lactate dehydrogenase, alkaline phosphatase, and the serum glutamate oxaloacetate aminotransaminase:aspartate aminotransferase (SGOT:AST) ra-
3 1380 HENRY ET AL. tio by an independent laboratory 7 using accepted clinical procedures and methodology. 8 The free sphinganine and sphingosine levels in the serum were determined by the method of Merrill et al. (1988). After bleeding on Day 21, all birds were killed by cervical dislocation, and the liver, kidney, spleen, bursa of Fabricius, and proventriculus were excised, trimmed of adhering tissue, and weighed. Liver, kidney, and brain samples were taken from 10 birds, selected randomly from each dietary treatment, and fixed by immersion in 10% neutral buffered formalin. The livers were pooled by replicate and stored at 5 C until analysis. The lipid content of the livers was determined gravimetrically by the method of Smith and Hamilton (1970). Free sphinganine and sphingosine levels in the livers were determined by the method of Merrill et al. (1988). The fixed liver, kidney, and brain tissues were embedded in paraffin, and sections were cut and stained with hematoxylin and eosin as described by Luna (1960). Histopathological evaluation of the stained sections was then performed as described by Dykstra et al. (1985) with modifications. Coded sections were evaluated by light microscopy for lymphocytes, hyperplasia, myeloid cells, and necrosis. Scores for each criterion were recorded as follows: 1 = absence of lesion, 2 = focal or mild lesions, 3 = multifoci or moderate lesions, and 4 = diffuse or severe lesions. The individual criterion scores for each slide were summed to obtain a total lesion score per slide, and the total lesion scores were averaged for each treatment. Scores for each criterion were also averaged within treatments to obtain a mean criterion score for each treatment. Using this system, the minimum and maximum scores possible for total lesions were 4 and 16, respectively. The data were subjected to a one-way analysis of variance in which an F-ratio was calculated. If the F-ratio was significant, the Fisher s least significant difference among the means was calculated as described by Fryer (1966). Statements of significance are based on P RESULTS Body weights of birds fed rations containing FB 1 at 20, 40, and 80 mg/kg of feed were not significantly different from those of birds fed the control ration (Table 1). Feed conversion ratios for birds fed FB 1 -contaminated diets were not significantly different at Day 7 of the experiment. At 14 and 21 d, the feed conversion ratios of the birds consuming diets containing 0 or 20 mg/kg of FB 1 were significantly higher than the feed conversion ratio of the birds consuming diets containing 80 mg/kg of FB 1. However, the feed conversion of birds on diets containing 20 or 40 mg/kg of FB 1 was not different from that of the controls (Table 2). Similarly, there were no significant 7 St. Mary s Hospital, Athens, GA Kinetic Discrete Analyzer, American Monitor, Indianapolis, IN TABLE 1. The response of weekly body weight of broiler chicks fed diets containing purified fumonisin B 1 (FB 1 ) for 21 d 1 Age Dietary FB 1 0d 7d 14d 21d (mg/kg) (g) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 19 1 No significant differences were observed (P > 0.05) among any treatments at any time interval. 2 Values are means ± SD of five replicates of six chicks each. differences in feed conversion ratios of birds fed dietary fumonisin at 40 and 80 mg/kg at 14 and 21 d. Mortality in all groups was low, and the overall mortality in the experiment was less than 1%. Water consumption was not significantly different as a result of the incorporation of FB 1 in the diets between any two groups at 7, 14, and 21 d. There were no significant differences in the relative weights of the liver, spleen, kidney, and proventriculus among the various treatments and the control group at 21 d (Table 3). Likewise, the dry matter of livers from control birds and the birds consuming the various FB 1 treatments was not significantly different (Table 4). Dietary FB 1 at 40 and 80 mg/kg resulted in a significant decrease in the liver lipids of broiler chicks (Table 4). The liver sphinganine levels in birds consuming diets containing FB 1 were significantly elevated compared with controls, but the liver sphingosine levels were not significantly altered. Therefore, the liver sphinganine:sphingosine ratio was significantly increased by dietary FB 1 (Table 4). The results of analyses of the serum (Table 5) demonstrate that serum total protein, globulin, and uric acid were not altered by the presence of FB 1 in the diet; nor were calcium, potassium, sodium, and chloride concentrations in the serum significantly altered. However, the SGOT:AST ratio in the serum was significantly elevated in birds that consumed a diet with 80 mg/kg of FB 1. Alkaline phosphatase and lactic dehydrogenase were not TABLE 2. The response of the feed conversion ratio of broiler chicks fed purified fumonisin B 1 (FB 1 ) for 21 d Age Dietary FB 1 0to7d 8to14d 15to21d (mg/kg) feed conversion ratio 1, ± 0.04 a 1.34 ± 0.11 a 1.44 ± 0.07 a ± 0.14 a 1.35 ± 0.16 a 1.36 ± 0.08 a ± 0.03 a 1.20 ± 0.04 ab 1.24 ± 0.03 ab ± 0.06 a 1.09 ± 0.03 b 1.19 ± 0.03 b a,b Means within the same column with no common superscript differ significantly (P < 0.05). 1 Values are means ± SD of five replicates of six chicks maintained on diets throughout the experiment. 2 Grams of feed consumed:grams of body weight gained.
4 FUMONISIN TOXICOSIS IN BROILERS 1381 TABLE 3. The response of the relative weights of the spleen, kidney, proventriculus, bursa, and liver in chicks fed purified fumonisin B 1 (FB 1 ) for 21 d 1,2 Dietary Liver Spleen Kidney Proventriculus Bursa FB 1 weight weight weight weight weight (mg/kg) (g/100 g body weight) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± Values are means ± SD of five replicates of six chicks at each dietary treatment. 2 No significant differences were observed (P > 0.05) among the means for any organ. TABLE 4. The response of liver dry matter, liver lipid, and liver sphinganine:sphingosine in chicks fed purified fumonisin B 1 (FB 1 ) for 21 d 1 Dietary FB 1, mg/kg Parameters Liver dry matter (%) 28.8 ± 1.7 a 28.8 ± 1.8 a 27.8 ± 0.8 a 29.5 ± 1.1 a Liver lipids (%) 20.5 ± 3.6 a 15.7 ± 1.4 ab 15.1 ± 0.7 b 13.5 ± 1.1 b Sphinganine (pmol/g) 37.1 ± 8.8 c 247 ± 43.3 b 262 ± 38.5 b 451 ± 111 a Sphingosine (pmol/g) 259 ± 85 a 371 ± 105 a 322 ± 86 a 301 ± 39 a SPA:SPO ± 0.04 c 0.70 ± 0.24 b 0.88 ± 0.33 b 1.55 ± 0.25 a a c Means ± SD within the same row with different superscripts are significantly different (P < 0.05). 1 Values are means ± SD of five replicates of six chicks at each dietary treatment. 2 SPA:SPO = sphinganine:sphingosine ratio. TABLE 5. The response of various serum parameters 1 of broiler chicks to dietary fumonisin B 1 (FB 1 ) Dietary FB 1 (mg/kg) Parameters Total protein 2.72 ± 0.02 a 2.74 ± 0.05 a 2.72 ± 0.08 a 2.84 ± 0.1 a (g/100 ml) Globulin 1.9 ± 0.03 a 1.9 ± 0.04 a 1.9 ± 0.09 a 2.0 ± 0.05 a (g/100 ml) Glucose 250 ± 2.3 a 243 ± 2.5 a 246 ± 5.6 a 263 ± 8.6 a Cholesterol 129 ± 3.1 a 122 ± 3.7 a 124 ± 2.4 a 133 ± 4.1 a Triglycerides 85.5 ± 8.0 a 76.6 ± 6.1 a 86.2 ± 7.3 a 97.0 ± 8.1 a Uric acid 5.5 ± 0.5 a 6.4 ± 0.5 a 5.9 ± 0.3 a 6.1 ± 0.94 a Calcium 7.4 ± 0.23 a 7.6 ± 0.37 a 8.2 ± 0.17 a 8.3 ± 0.32 a Chloride 114 ± 1.4 a 111 ± 0.9 a 113 ± 1.9 a 118 ± 3.8 a (mm/l) Sodium 144 ± 1.4 a 149 ± 5.3 a 149 ± 3.1 a 146 ± 1.3 a (mm/l) Potassium 10.1 ± 0.19 a 10.4 ± 0.38 a 10.1 ± 0.55 a 10.0 ± 0.45 a (mm/l) Alkaline phosphatase 9.6 ± 1.3 a 7.5 ± 0.7 a 8.0 ± 0.6 a 9.6 ± 1.2 a (IU/L) LDH ± 26 a 209 ± 11 a 272 ± 26 a 276 ± 24 a (IU/L) SGOT:ASP ± 3.4 a 175 ± 6.1 a 182 ± 4.8 a 203 ± 4.8 b (IU/L) Sphinganine 10.7 ± 2.0 b 13.4 ± 0.8 b 19 ± 1.1 ab 24.7 ± 2.70 a (pmol/ml) Sphingosine 32.7 ± 3.6 a 29.8 ± 1.7 a 36.1 ± 3.0 a 34.6 ± 4.4 a (pmol/ml) SPA:SPO ± 0.05 b 0.50 ± 0.07 b 0.54 ± 0.07 b 0.73 ± 0.04 a a,b Values within the same row with different superscripts differ significantly (P 0.05). 1 Values are means ± SEM of individual assays on five pooled samples. 2 LDH = lactate dehydrogenase. 3 SGOT:ASP = serum glutamate oxaloacetate aminotransaminase:aspartate aminotransferase ratio. 4 SPA:SPO = sphinganine:sphingosine ratio.
5 1382 HENRY ET AL. FIGURE 1. The relationship between free sphinganine and sphingosine levels in livers of 3-wk-old broiler chicks fed diets containing purified fumonisin B 1 at 0, 20, 40, and 80 mg/kg of feed. altered by the presence of FB 1 in feed. Serum triglycerides and cholesterol were not significantly affected by the presence of up to 80 mg FB 1 /kg feed, and free sphingosine levels in the serum were not affected significantly. The sphinganine:sphingosine ratio and free sphinganine levels of chicks fed 80 mg FB 1 /kg were significantly higher than those of controls. A linear increase in free sphinganine in the liver was observed with increasing dietary FB 1 (Figure 1). Pathological evaluations of the brains of chicks fed 20, 40, and 80 mg FB 1 /kg of feed indicated no differences from those of control chicks. Evaluation of the kidneys revealed hyperplasia and necrosis in some of the kidneys taken from birds consuming FB 1 -contaminated diets; however, the total score of lesions was not significantly different. There were no significant differences in lymphocytes, myeloid cells, hyperplasia, or total lesion scores from liver tissues of FB 1 -fed and control birds. DISCUSSION Corn, a major component of poultry feed, is commonly contaminated with molds from the genus Fusarium, thus potentially exposing broilers to mycotoxins such as the trichothecenes, fusaric acid, moniliformin, fusarin C, and the fumonisins. The fumonisins have been isolated and chemically characterized (Bezeuidenhout et al., 1988; Gelderblom et al., 1988). The characterization of FB 1 -toxicosis is of practical importance, because consumption of FB 1 -contaminated feedstuffs has been associated with LEM in equine species (Marasas et al., 1988) and PPE in swine (Harrison et al., 1990). The present study indicates that the body weight of broiler chicks was not affected by FB 1 when present at dietary levels up to 80 mg/kg. Previous studies reported that dietary FB 1 at concentrations greater than 100 mg/ kg caused a decrease in body weight gain and feed intake of broiler chicks (Brown et al., 1992; Ledoux et al., 1992a; Weibking et al., 1993a). Similarly, in studies with rats and pigs, dietary fumonisin resulted in decreased body weight, variation in daily feed intake, and decreased feed consumption (Voss et al., 1990; Haschek et al., 1992). Liver, kidney, spleen, proventriculus, and bursa weights were not affected by the highest concentration of FB 1 used in this experiment. This result is similar to that of a previous study in which performance parameters and organ weights of broiler chicks fed F. moniliformecontaminated culture material containing fumonisins at 75 mg/kg were unaffected (Weibking et al., 1993a). An analysis of liver lipids suggests that fumonisins cause a decrease in liver lipids. Liver lipid content, as a percentage of liver weight, showed a linear decrease with increasing dietary concentrations of FB 1 in the feed. This response cannot be compared with any previous study, because no previous studies reported on the relationship of dietary FB 1 with the lipid content of the liver. Pathological evaluation of livers obtained from rats fed FB 1 revealed changes in the fatty component (Gelderblom et al., 1988). The implication of this finding is unclear, because the pathological evaluation did not reveal any liver damage. However, the reduction of liver lipids suggests that stored lipids were utilized in the birds fed diets containing FB 1 at 40 and 80 mg of toxin/kg of feed. The increase in the SGOT:AST ratio in the serum of chicks fed FB 1 at 80 mg/kg of feed for 3 wk, suggests that FB 1 at that level may have resulted in damage to the liver. A similar increase in the SGOT:AST ratio was reported when F. moniliforme-contaminated culture material containing the fumonisins was incorporated into broiler and turkey diets (Ledoux et al., 1992a), and rat (Voss et al., 1990) and pig (Osweiler et al., 1992) diets. The structural similarity of the fumonisin backbone to sphingosine and sphinganine led to the hypothesis that the fumonisins may interfere with the sphingolipid metabolic pathway (Weibking et al., 1993a). In vivo experiments by Wang et al. (1991) and others indicated that the fumonisins are inhibitors of sphingolipid biosynthesis. Other studies suggest that the site of inhibition occurs where sphinganine and fatty acyl-coenzyme A combine to form dihydrocermide, which would result in an accumulation of free sphinganine in tissue and serum (Norred et al., 1992; Merrill et al., 1993). Analyses of sphingosine and sphinganine levels in liver and serum revealed an increase in the level of sphinganine, with no change in the level of sphingosine, that resulted in an increase in the sphinganine:sphingosine ratio. Similar results were reported for broiler chicks (Weibking et al., 1993a), pigs (Riley et al., 1993), and horses (Wang et al., 1991, 1992) when FB 1 was incorporated into the diet. This linear increase of sphinganine in the liver demonstrates that there is a dose-response relationship between liver sphinganine and dietary FB 1 up to 80 mg/kg. The present data indicate that FB 1, below a dietary concentration of 80 mg/kg, does not affect broiler chick performance under the described experimental conditions. Javed et al. (1993) fed purified FB 1 to broiler chicks from 1 to 14 d of age at dietary concentrations of 125 and 274 mg/kg, and observed mortality and decreased weight gains. These responses may have been due to the use of
6 FUMONISIN TOXICOSIS IN BROILERS 1383 higher dietary concentrations of FB 1 compared with those used in the present study. The chickens used by Javed et al. (1993) were males, but were of a different strain (Columbia New Hampshire) than the birds used in the present study. Because genetic variability in susceptibility to mycotoxins is known to occur in avian species (Marks and Wyatt, 1979; Wyatt et al., 1987), the strain of chicken used by Javed et al. (1993) may be more sensitive to FB 1 than the strain of bird used in the present study. Furthermore, the purity of the FB 1 used in the earlier study was approximately 90%; thus, the possibility exists for a toxic contaminant to have contributed to the response of these birds. Espada et al. (1997) observed a decrease in the prothrombin time, and an increase in the fibrinogen concentration in blood and the activity of antithrombin III, from birds that had been fed dietary FB 1 at a concentration of 10 mg/kg for only 6 d. 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