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Poult Sci 2007. 86:1887-1893
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IMMUNOLOGY, HEALTH, AND DISEASE

Chronic Toxicity of Fumonisins in Turkeys

D. Tardieu*, J.-D. Bailly*, F. Skiba{dagger}, J.-P. Métayer{dagger}, F. Grosjean{dagger} and P. Guerre*,1

* École Nationale Vétérinaire de Toulouse, Mycotoxicology Unit, 23 chemin des Capelles, BP 87614, 31076 Toulouse Cedex 3, France; and {dagger} Arvalis-Institut du Végétal, 21 chemin de Pau, 64121 Montardon, France

1 Corresponding author: p.guerre{at}envt.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Fumonisins are mycotoxins that are found worldwide. They are mainly produced by Fusarium verticillioides during its development on corn. The main toxic effects of these molecules have been well characterized in poultry in the case of acute exposure, but the subclinical and economic effects of chronic exposure are less known. Whereas the latest European recommendations suggest that maximal levels of fumonisins in corn could reach 60 mg/kg and the maximal contamination of poultry feeds could reach 20 mg/kg, no study is available at this level in turkeys. The aim of the present work was thus to characterize the effects of exposure to fumonisins (concentrations of 0, 5, 10, and 20 mg of fumonisin B1 + fumonisin B2/kg of feed) on feed consumption and growth in turkeys over a period of 9 wk. Main biochemical parameters of the liver and alteration of sphingolipid metabolism were investigated in plasma, liver, and kidney. The main results showed no effect on feed consumption and growth in exposed turkeys. Moreover, no effect was observed on the weight of tissues and markers of liver injury. By contrast, a disruption of sphingolipid metabolism was clear at a level of exposure of 10 and 20 mg of fumonisin B1 + fumonisin B2 mg/kg of feed. Both hepatic and kidney concentrations of sphinganine increased gradually throughout the exposure period. These results reveal that disruption of sphingolipid metabolism is an early and sensitive biomarker of fumonisins exposure in turkeys; the consequences on these alterations remain to be established.

Key Words: fumonisin • turkey • toxicity • mycotoxin • corn


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Fumonisin B1 (FB1) is the major mycotoxin produced by Fusarium verticillioides and Fusarium proliferatum fungi, which are widely found as contaminants in corn and corn screenings (WHO, 2002). Fumonisin B1 was linked to esophageal cancer in humans (Yoshizawa et al., 1994; Marasas, 1995) and was reported to be carcinogenic in rats (Gelderblom et al., 1991, Howard et al., 2001). Hepatic and renal toxicity was observed in several species including horses, pigs, lambs, rats, broilers, turkeys, and ducks; encephalomalacia and pulmonary oedema were reported in horses and pigs (WHO, 2002). Finally, all species appear to be sensitive to the toxin, but toxicity differs from one species to another.

Previous studies conducted in birds showed that high exposure to fumonisins (100 mg of fumonisins/kg of feed and more) reduces performance and is responsible for alterations in serum constituents and enzyme activities and for hepatitis or hepatic hyperplasia in broilers, turkeys, quails, and ducks (Brown et al., 1992; Ledoux et al., 1992, 1996; Weibking et al., 1993a,b, 1995; Espada et al., 1994, 1997; Bermudez et al., 1995, 1997; Kubena et al., 1995a, 1997a, Kubena et al., b; Henry et al., 2000; Bailly et al., 2001; Tran et al., 2003, 2005; Tardieu et al., 2004). These effects are associated with altered sphingolipid biosynthesis and an increased sphinganine to sphingosine (Sa/So) ratio (Weibking et al., 1993a; Ledoux et al., 1996; Henry et al., 2000; Bailly et al., 2001; Broomhead et al., 2002; Tran et al., 2003, 2006; Tardieu et al., 2004, 2006). Although subacute toxicity of FB1 has frequently been investigated in avian species, the chronic effects of FB1 are less well understood. Previous studies conducted in 14- and 18-wk-old turkeys demonstrated that, respectively, 50 and 75 mg of FB1/kg of feed are detrimental to animal performance (Bermudez et al., 1996; Broomhead et al., 1998, 2002). In contrast, FB1 had no effect on BW gain in broilers fed 50 mg of FB1/kg at marketing age (7 wk; Broomhead et al., 2002) or in laying hens fed 200 mg of FB1/kg for 420 d (Kubena et al., 1999). Surprisingly, in ducks, 10 wk of exposure to fumonisins seems to be better tolerated than 1 wk of exposure (Tardieu et al., 2006). Moreover, the effects of fumonisins on protein, cholesterol, alanine aminotransferase, and lactate dehydrogenase (LDH) in plasma were shown to be reversible during chronic exposure, and the increase in free Sa and the Sa/So ratio in liver and kidneys was less pronounced after 10 wk of exposure to the toxin than after 1 wk (Tardieu et al., 2006; Tran et al., 2006).

The objective of the present study was to investigate the chronic effects of feeding different levels of FB1 to 1- to 10-wk-old turkeys. Three levels of FB1 were investigated, the highest being the maximum recommended by the European Union (2006) for fumonisins in avian feed. Response variables used to evaluate toxicity included body weight, feed consumption, relative organ weights, serum chemistry, histopathology, and serum, liver, and kidney Sa/So ratios.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All experimental procedures involving animals were in accordance with the French National Guidelines for the care and use of animals for research purposes.

Preparation of Feed
The feed was formulated and manufactured at the experimental station of Boigneville (ARVALIS–Institut du végétal, Boigneville, France) according to usual practices to provide equal protein contents and energy intake, as well as to meet amino acid (Lys, sulphur amino acids, and Trp) and mineral requirements. A starter diet and 2 growth diets were prepared in the form of a mixture of raw materials not contaminated by mycotoxins and a mixture including different percentages (0 to 20%) of a batch of corn contaminated by fumonisins [FB1 + fumonisin B2 (FB2) = 117 mg/kg] and of a batch of corn of the same origin that was not contaminated (12 to 32%). The levels of contamination of the final feed were as follows: 0, 5, 10, and 20 mg of FB1 + FB2/kg. The absence of other mycotoxins was confirmed by chromatography, ELISA, or both (concentrations of aflatoxin B1, ochratoxine A, zearalenone, deoxynivalenol, and T2 toxin, respectively lower than 10, 10, 50, 250, and 50 µg/kg).

Animals
Three hundred 1-d-old male turkeys of the BUT 9 strain (Sicamen, Volnay, France) were placed in cages in groups of 2 at the experimental station of Pouline (ARVALIS–Institut du végétal, Pouline, Villerable, France) with free access to feed. The noncontaminated starter diet was distributed to all the turkeys for 1 wk. At the end of this phase of adaptation, feed consumption was measured and 150 turkey poults were divided into 4 batches of 36 animals on the basis of their live weight and placed in individual cages. The 6 remaining turkeys were used for the first sample collection. The turkeys were weighed, and the feed consumption was measured on d 14, 21, 28, 42, 56, and 70.

Sample Collection
Feed was removed 8 h before killing. Six animals were taken at the end of the phase of adaptation, and 6 animals per batch were taken randomly at d 14, 21, 28, 42, 56, and 70, weighed, and killed to check for a possible pathology. Blood samples were collected in dry tubes before killing and centrifuged for 15 min at 3,000 x g after coagulation. The serum was removed and stored at –0°C until use. The different organs were separated and weighed to measure the possible effect of fumonisins on tissue mass. Ten grams each of liver and kidney were removed and stored at –20°C until analysis. Ten grams of each organ was also placed in a vessel containing formaldehyde (10% wt/vol), then stored at ambient temperature until microscopic analysis.

Biochemistry
Serum concentrations of alanine aminotransferase (EC 2.6.1.2 [EC] ), aspartate aminotransferase (EC 2.6.1.1 [EC] ), and lactate dehydrogenase (EC 1.1.1.27 [EC] ) were analyzed with a Hitachi 717 clinical chemistry analyzer (Hitachi, Tokyo, Japan) according to international guidelines; values were expressed in units per liter. Cholesterol was measured by enzymatic reaction, and protein was determined using the Biuret method modified according to the recommendations of Hitachi.

Sphingosine and Sphinganine Determination
Free So and free Sa were determined in serum, liver, and kidney by HPLC according to Riley et al. (1994a). Briefly, 0.2 nmol of C20 Sa (BioValley S. A., Marne la Vallée, France) was added to 100 µL of serum or tissue homogenates. Lipids were extracted with alkaline methanolic-chloroform and further hydrolyzed to liberate free Sa and So. The chloroform phase was then washed twice with alkaline water. Samples were dried and suspended in 20 µL of methanol. Extracts were derived with orthophtaldialdehyde and sonicated for 10 min before injection. Sphinganine, So, and C20 Sa concentrations were determined by HPLC using an ICS M2200 solvent delivery module (ICS, Toulouse, France) connected with a programmable fluorescence detector (FD-500 Shimazu, Kyoto, Japan). Operating conditions were analytical Radial-Pak cartridge packed with Nova-Pak C18 and a C18 precolumn filter (Waters Associates Inc., Milford, MA), liquid phase: methanol-water (90:10), flow rate: 1.25 mL/min, excitation wavelength: 335 nm, emission wavelength: 440 nm. Every day a standard solution containing known amounts of So, Sa, and C20 Sa mixture was run to verify the column performance and stability of the orthophtaldialdehyde reagent. Mean retention times were 12, 17, and 29 min for So, Sa, and C20 Sa, respectively.

All other chemicals and reagents were of the highest grade available. They were purchased from Scharlau (Scharlau Chimie S.A., Barcelona, Spain) and Sigma Chemical Co. (Sigma, Saint Quentin Fallavier, France). In all studies, distilled deionized water was used.

Statistical Analysis
Data for all response variables were reported as means ± SD and subjected to 1-way ANOVA. When significant differences were obtained, differences between means were determined by the Tukey’s test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Mortality and Performance
Neither mortality nor signs of pathology were observed in any of the turkeys during the 63-d exposure period. The chronic effect of feeding fumonisin-contaminated feed on BW, feed consumption, and global performance of the turkeys are presented in Figure 1Go and Table 1Go. There was no significant difference in BW or in feed consumption whatever the day of exposure. Moreover, no significant effect was observed on the feed conversion ratio and the average daily weight gain. Only a slight increase in the mean daily consumption was observed in turkeys fed 20 mg of fumonisins/kg of feed.


Figure 1
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  		Figure 1. Effects of fumonisins on BW (A) and feed consumption (B) in turkeys exposed to contaminated feed from 7 to 70 d of age. Values are means obtained from groups of 6 animals receiving: -{circ}- 0, -{blacktriangleup}- 5, -{diamond}- 10, and -{blacksquare}- 20 mg of fumonisins B1+B2/kg of diet.

 

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  		Table 1. Effects of fumonisins on performance and on the weight of liver, kidney, and breast muscle in turkeys exposed to a contaminated feed from 7 to 70 d of age1
 
Organ Weights and Histopathology
Whatever the diet, no macroscopic lesion was found during postmortem examination of tissues. The chronic effects of fumonisins on the weight of liver, kidney, and breast muscle after 63 d of exposure are shown in Table 1Go. There was no significant difference in the relative weight of these tissues whatever the feed ingested. Moreover, a histopathological examination of liver and kidney, confirmed the absence of an effect of the fumonisins at a level of exposure below or equal to 20 mg/kg feed in turkeys.

Serum Biochemistry
The effect of fumonisins on various serum biochemical parameters of turkeys during exposure to fumonisins are presented in Table 2Go. No effect was observed on protein and cholesterol concentrations whatever the day of exposure. Concerning enzyme activities, although a moderate increase in LDH activity occurred in turkeys fed 20 mg of fumonisins/kg of feed from d 21 to 56, this increase was not significant. Moreover, alanine aminotransferase and aspartate aminotransferase activities remained constant throughout the study.


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  		Table 2. Effects of fumonisins on plasma biochemistry in turkeys exposed to contaminated feed from 7 to 70 d of age1,2
 
Sphingolipid Alterations
Free Sa and So were quantified in serum, liver, and kidney, and the Sa/So was calculated. The Sa/So remained nearly constant in serum throughout the study (data not shown), whereas a considerable increase in this parameter was observed in the liver and kidney of turkeys fed the fumonisinscontaminated diet (Figure 2Go). This increase seems to be linked with the dose and the duration of exposure. In liver, significant differences between unexposed and exposed animals were observed after 7 d of exposure (14 d of age) in animals fed 20 mg of fumonisins/kg of feed and after 21 d (28 d of age) in animals exposed to 10 mg/kg. Concerning the kidney, significant differences were also observed between unexposed turkeys and those fed 20 mg of fumonisins/kg of feed after 7 d of exposure (14 d of age), whereas 35 d of exposure was necessary in animals fed 10 mg/kg (42 d of age). Differences between animals fed 5 mg of FB1 + FB2/kg of feed and controls were only obtained after 49 and 63 d of exposure (56 and 70 d of age).


Figure 2
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  		Figure 2. Effects of fumonisins on the sphinganine to sphingosine (Sa/So) ratio in liver (A) and kidney (B) of turkeys exposed to contaminated feed from 7 to 70 d of age. Values are means ± SE obtained from groups of 6 animals receiving: -{circ}- 0, -{blacktriangleup}- 5, -{diamond}- 10, and -{blacksquare}- 20 g of fumonisins B1+B2/kg of diet.

 
As shown in Figures 3Go and 4Go, the effects of fumonisins on Sa/So were mainly due to an increase in free Sa in tissues, whereas So remained nearly constant throughout the study (except in the kidney of ducks fed 20 mg/kg). Indeed, in liver and kidney, significant differences in Sa concentrations between unexposed and exposed animals were obtained after 7 d of exposure in animals fed 20 mg of fumonisins/kg of feed (14 d of age) and after 21 or 35 d in animals exposed to 10 mg/kg (28 or 42 d of age). By contrast, significant differences between exposed and unexposed turkeys in So concentrations in tissues were only observed in kidneys (Figure 4Go) at all days of exposure in animals exposed to 20 mg of FB1 + FB2/kg of feed and after 63 d of exposure in animals fed 10 mg/kg (70 d of age).


Figure 3
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  		Figure 3. Effects of fumonisins on the sphinganine (Sa) and sphingosine (So) concentrations in the liver of turkeys exposed to contaminated feed from 7 to 70 d of age. Values are means ± SE obtained from groups of 6 animals receiving: -{circ}- 0, -{blacktriangleup}- 5, -{diamond}- 10, and -{blacksquare}- 20 mg of fumonisins B1+B2/kg of diet.

 

Figure 4
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  		Figure 4. Effects of fumonisins on the sphinganine (Sa) and sphingosine (So) concentrations in the kidney of turkeys exposed to contaminated feed from 7 to 70 d of age. Values are means ± SE obtained from groups of 6 animals receiving: -{circ}- 0, -{blacktriangleup}- 5, -{diamond}- 10, and -{blacksquare}- 20 mg of fumonisins B1+B2/kg of diet.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results obtained in the present study indicate that the general performance of turkeys was not affected by the consumption of a diet containing fumonisins at a level below or equal to 20 mg of FB1 + FB2/kg. This is the first study conducted at this level, which is the maximum level of fumonisins in avian feed recommended by the European Union (2006). This study completes previous experiments that reported a decrease in the BW of turkeys and broiler chicks receiving FB1 at concentrations greater than 50 and 75 mg of feed/kg for 21 d (Brown et al., 1992; Ledoux et al., 1992; Weibking et al., 1993b; Ledoux et al., 1996; Broomhead et al., 1998) and turkeys fed 50 mg of fumonisins/kg of feed for 14 wk (Broomhead et al., 2002). It demonstrates that turkeys are less sensitive to fumonisin toxicity than ducks (Tran et al., 2005). Another interest of this study is linked to the material used for the assay. Indeed, our results were obtained using naturally contaminated corn, whereas the previous results in turkeys were obtained using fumonisins extracted from culture materials of Fusarium verticillioides (Broomhead et al., 2002). Although the duration and the level of the exposure were slightly lower in our study than in Broomhead et al., there was no marked difference between naturally contaminated corn and culture material (see also discussion of the effects of fumonisins on sphingolipid metabolism below).

In agreement with the lack of effect on performances, we observed no effect on the biochemical parameters used to investigate liver damage whatever the level of fumonisins in the feed. This result agrees with previous data obtained in ducks, which showed that a level of FB1 in feed equal to 32 mg/kg was necessary to increase cholesterol, LDH, and alanine aminotransferase concentrations in serum, whereas 128 mg/kg was necessary to increase proteins and aspartate aminotransferase (Tran et al., 2006). Finally, the lack of effect of fumonisins on biochemistry in turkeys is not surprising because previous studies in turkeys demonstrated that effects on biochemistry were only obtained at levels of exposure higher than that which had an effect on performance (Kubena et al., 1995a,b, 1997a; Ledoux et al., 1996).

Interestingly, although no sign of toxicity and no effect on biochemistry and tissue weight were observed during fumonisins exposure in this study, a marked increase in the Sa/So ratio was obtained in liver and kidney. The magnitude of the increase in the Sa/So ratio at the end of the study is of the same level as in our previously published study, which used fumonisins obtained from culture material of F. verticillioides at the end of the exposure (Broomhead et al., 2002). Interestingly, we demonstrate for the first time in turkeys that a significant increase in Sa/So can be obtained a few days after the beginning of the exposure to fumonisins at a level of 20 mg of FB1 + FB2/kg of feed. This confirms that disruption of sphingolipid metabolism is an early event when animals are exposed to fumonisins. It precedes signs of toxicity, in agreement with data obtained in ducks (Tran et al., 2003, 2006) and mammals (Voss et al., 1999; van der Westhuizen et al., 2001; Zomborszky-Kovacs et al., 2002). However, the increase in the Sa/So ratio in liver and kidney appeared to be less pronounced than that obtained during fumonisin exposure in ducks (Tardieu et al., 2006). This difference confirms that turkeys are more resistant to fumonisins than ducks. In turkeys, the kidney and liver seem to have the same sensitivity to the disruption of sphingolipid metabolism by fumonisins, whereas kidneys were more sensitive in ducks (Tardieu et al., 2006), rats (Riley et al., 1994b; Bondy et al., 1996), and rabbits (LaBorde et al., 1997). In the liver, the increase in the Sa/So ratio results primarily from an increase in Sa concentrations (Figures 3Go and 4Go). By contrast, in the kidney, So concentrations are also slightly higher, especially in turkeys exposed to 20 mg of fumonisins/kg of feed. The latter effect on So in the kidney is in disagreement with what was previously reported in duck, with So remaining nearly constant throughout the exposure period (Tardieu et al., 2006). It confirms the importance of the joint interpretation of the concentrations of Sa and the Sa/So ratio in the determination of exposure to fumonisins. Finally, increases in the Sa/So ratio occur before other signs of toxicity in all avian species in which it has been investigated (Weibking et al., 1993b, 1994; Ledoux et al., 1996; Henry et al., 2000; Bailly et al., 2001; Broomhead et al., 2002; Tran et al., 2003). To date, the consequences of a disruption of sphingolipid metabolism on avian health are unknown because it is not known whether these disruptions have a technological or a gustative impact on meat prepared from exposed animals.

In conclusion, the distribution of a feed containing fumonisins at levels of 5, 10, and 20 mg FB1 + FB2/kg over a 63-d period had no effect on performance or on serum biochemistry. This study confirms that the level of fumonisins in avian feed of 20 mg of FB1 + FB2/kg recommended by the European Commission can be considered as safe for these animals. Nevertheless, the lack of effect of fumonisins on performance and on biochemistry does not mean that these mycotoxins have no effect on turkeys. Indeed, a disruption of sphingolipid metabolism was observed at a level of FB1 + FB2 in feed equal or higher to 10 mg/kg. Finally, the Sa/So ratio appeared to be the best biomarkers of fumonisin exposure in turkeys.


   ACKNOWLEDGMENTS
 
The authors thank H. Clavé (Maïsadour, France), V. Ortega, and C. Florin (Syngenta Seeds, France) for their technical aid and their expertise in the selection of the batches of corn used in this study.

The results presented were obtained thanks to the financial participation of Maïsadour, Syngenta Seeds, the Midi-Pyrenées Region, and the French Ministry of Research within the framework of the RARE program Fusariotoxines 2003–2006.

Received for publication February 27, 2007. Accepted for publication May 26, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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