J. Anim Sci. 2006. 84:1935-1942. doi:10.2527/jas.2005-355
© 2006 American Society of Animal Science
Ingestion of low doses of deoxynivalenol does not affect hematological, biochemical, or immune responses of piglets1
F. Accensi*,2,
P. Pinton*,2,
P. Callu
,
N. Abella-Bourges
,
J.-F. Guelfi,
F. Grosjean and
I. P. Oswald*,3
* INRA, UR66, Laboratoire de Pharmacologie-Toxicologie, 180 chemin de tournefeuille, Toulouse, France;
and
ARVALIS Institut du végétal, 27 rue de la Vistule, 75013 Paris, France;
and
Ecole Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, Toulouse, France
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Abstract
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Deoxynivalenol (DON), a mycotoxin produced by Fusarium spp., is a frequent contaminant of cereals. Because of their rich cereal diet, pigs could be exposed to this mycotoxin. Pigs are among the animal species showing the greatest sensitivity to DON. Effects of intermediate to high levels of DON on pigs are well known and include feed refusal, decreased feed intake, and alteration of the immune response. Effects of low levels of DON, which are commonly detected in contaminated feed, remain unknown. The aim of this study was to investigate the effect of a diet naturally contaminated with a low concentration of DON (0, 280, 560, or 840 µg/kg of feed) on performance of weanling piglets and on 34 hematological, biochemical, and immune variables. Low doses of DON did not alter the animal performances (feed intake and BW gain). Such low levels of DON did not modify the 9 hematological variables measured (including white blood cell, red blood cell, and platelet counts, relative numbers of neutrophils and lymphocytes, and hematocrit and hemoglobin concentrations) or the 18 biochemical variables tested (including cations, glucose, urea, creatinine, bilirubin, cholesterol and triglyceride concentrations, and plasma enzyme activity). Similarly, no effect of low doses of DON was observed on the immune responses of the animals (immunoglobulin subset concentration, lymphocyte proliferation, and cytokine production).
Key Words: deoxynivalenol • immune response • immunology • mycotoxin • piglet • swine
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INTRODUCTION
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Mycotoxins are secondary metabolites of fungi that may contaminate animal and human feeds. Syndromes caused by mycotoxins range from acute mortality to slow growth and reduced reproductive efficiency. Consumption of mycotoxins may also result in impaired immunity and decreased resistance to infectious diseases (Oswald et al., 2003
, 2005; Halloy et al., 2005).
Deoxynivalenol (DON), a mycotoxin produced by Fusarium spp. and classified as a type B trichothecene, is commonly detected in cereals and grains, particularly in wheat, barley, corn, and their by-products (SCOOP, 2003). The initial adverse effect observed after DON exposure is reduced feed intake. At greater concentration, vomiting, feed refusal, and reduced BW gain will occur. Deoxynivalenol also affects the immune response. In mice, dietary exposure to 10 to 25 mg of DON/kg of feed increases immunoglobulin (Ig) A and decreases IgM plasma concentrations (Rotter et al., 1996). Ingestion of feed contaminated with 5 mg/kg of toxin also reduces lymphocyte proliferation upon mitogenic stimulation (Pestka and Smolinski, 2005). In pigs, ingestion of 2 to 5 mg of DON-contaminated feed/kg upregulates IgA concentration in serum (Bergsjo et al., 1993; Dänicke et al., 2004).
Because of the high percentage of wheat in pig diets, swine could be exposed to this toxin. Most performance and toxicological data in pigs have been obtained with medium to high doses of DON (2 to 10 mg/kg of feed; Prelusky et al., 1994; Swamy et al., 2002). However, such high doses are not usually found in cereals used for animal feed. Most North American and European data show that cereals are contaminated with lower DON concentrations. A survey on 11,022 cereal samples from 12 European countries showed that 57% were positive for DON, but only 7% contained DON concentrations of 750 µg/kg or greater (SCOOP, 2003).
The aim of this study was to determine the effect of low concentrations of DON on animal performance and hematological, biochemical, and immunological variables of piglets.
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MATERIALS AND METHODS
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Animals
Animals were cared for in accordance with Guidelines National Institutes of Health Guide and the French Ministry of Agriculture for the care and use of laboratory animals. Twenty-four castrated male and 24 female crossbred pigs (P76 sire x Naïma dam) were used for the experiments. They were acquired locally just after weaning, at 4 wk of age, and acclimatized for 13 d in the pig-rearing house of the experimental station of Arvalis Institut du Végétal (Pouline, Villerable, France). Piglets were then allocated to 1 of the 4 experimental groups according to sex and BW (11.2 ± 1.4 kg). Pigs were housed individually with free access to feed and water. They were weighed at d 1, 14, and 28 of the experiment.
Experimental Diets
The experimental diets were prepared locally and formulated according to energy and amino acid requirements for piglets (INRA, 2002). Two different batches of wheat were used in the diets: 1 control batch free from mycotoxin contamination and 1 batch naturally contaminated with DON (Table 1). The NE and digestible amino acid content of the wheat batches were estimated according to INRA (2002). Their amino acid content was estimated from their CP content according to Mossé and Huet (1990). Four diets were prepared from the aforementioned wheat batches, soybean meal, amino acids, and a vitamin and mineral premix to achieve a digestible Lys:net energy ratio of 4.7, and digestible Met + Cys:Lys, digestible Thr:Lys, and digestible Trp:Lys ratios of 60, 66, and 18.2% (Sève, 1994), respectively.
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Table 1. Composition and mycotoxin contamination of the raw materials used to formulate the different experimental diets
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Net energy of the diets was estimated according to Noblet et al. (1994) from the equation NE (MJ/kg of DM) = [0.703 x DE (MJ/kg of DM)] + [0.0066 x ether extract (g/kg of DM)] + [0.0020 x starch (g/kg of DM)] – [0.0041 x CP (g/kg of DM)] – [0.0041 x crude fiber (g/kg of DM)]. The DE, ether extract, starch, CP, crude fiber, and digestible amino acid contents of the diets were estimated by the additive method from characteristic contents of each feedstuff (Noblet et al., 1994). Deoxynivalenol content in the 4 different diets was 0, 280, 560, and 840 µg of DON/kg as-fed (Tables 1
and 2).
Analysis of Mycotoxins
Dietary contents of DON, 3-acetyl deoxynivalenol, 15-acetyl deoxynivalenol, nivalenol, diacetoxyscirpenol, T-2 toxin, HT-2 toxin, T-2 tetraol, zearalenone, ochratoxin A, and fumonisin B1 and B2 were analyzed in the raw materials by Qualtech (Vandoeuvre les Nancy, France). Trichothecenes were analyzed using gas chromatography-mass spectrometry, and HPLC techniques were used to measure fumonisin B1, fumonisin B2, ochratoxin A, and zearalenone levels in the raw materials. Table 2 presents the mean values obtained from 11, 2, and 2 determinations performed on the contaminated batch of wheat, the control wheat, and the soybean meal, respectively. The detection limit for these mycotoxins was 40 µg/kg for the type A trichothecenes (diacetoxyscirpenol, T-2 toxin, HT-2 toxin, and T-2 tetraol), 30 µg/kg for the type B trichothecenes (DON, 3-acetyl deoxynivalenol, 15-acetyl deoxynivalenol, and nivalenol), 10 µg/kg for fumonisin B1, 15 µg/kg for fumonisin B2, 0.5 µg/kg for ochratoxin A, and 15 µg/kg for zearalenone (as-is basis).
Blood Sampling
At the end of the experiment, blood samples were aseptically collected from the left jugular vein. Blood was collected in tubes (Vacutainer, Becton-Dickinson Le pont de Claix, France) containing EDTA for hematological analysis, and sodium heparin for biochemical and immunological analysis, respectively. Plasma samples, obtained after centrifugation of heparinized blood at 600 x g, were stored at –20°C until analyzed.
Plasma Biochemistry
Plasma concentrations of sodium, potassium, chloride, carbon dioxide, total proteins, calcium, phosphorus, urea, creatinine, bilirubin, glucose, cholesterol, and triglycerides, and activities of alkaline phosphatase, glutamyl oxaloacetic transaminase, glutamyl pyruvic transaminase, lactate dehydrogenase, and gamma-glutamyl transferase were determined on a Vitros 950 IRC analyzer (Ortho Clinical Diagnostics, Johnson and Johnson Company, Raritan, NJ) at the Laboratory of Biochemistry, Rangueil Hospital (Toulouse, France).
Hematology
White blood cell count, red blood cell count, platelet count, mean corpuscular volume, hematocrit, hemoglobin, mean corpuscular hemoglobin, and mean corpuscular hemoglobin concentration were carried out using an MS9 impedance counter (Melet Schloesing, Cergy-Pontoise, France). A 5-part white blood cell differential count was made manually on 100 leukocytes on May-Grünwald Giemsa-stained smears.
Measurement of Total Immunoglobulin Subsets
Total concentrations of the different immunoglobulin subsets (IgG, IgA, and IgM) were measured by ELISA, as recommended by the manufacturer (Bethyl, Interchim, Montluçon, France). Briefly, goat anti-pig IgA (alpha chain-specific), goat anti-pig IgG (Fc fragment-specific), and goat anti-pig IgM (mu chain-specific) were used as capture antibodies. Horseradish peroxidase-labeled goat anti-pig immunoglobulin subset was used as the detection antibody in conjunction with TMB (3,3',5,5'-tetramethyl benzidine; Pierce, France) substrate. The enzyme-substrate reaction was stopped by addition of 1 N H2SO4. Absorbance was read at 450 nm using an ELISA plate reader (Spectra thermo, Tecan, Trappes, France) and the Biolise 2.0 data management software. Plasma samples diluted 1:4,000, 1:60,000, and 1:6,000 (Tris-buffered saline 0.05 M; tween 20 0.05%; BSA 1%) to detect IgA, IgG, and IgM, respectively, were quantified by reference to standard curves constructed with known amounts of pig immunoglobulin subsets. The detection limits were 12.5 ng/mL for IgA and IgG, and 10 ng/mL for IgM. The intraassay CV were 3.2, 5.7, and 4.0% for IgA, IgG, and IgM, respectively.
Determination of Lymphocyte Proliferation
Heparinized blood samples were diluted 1:30 in complete culture medium consisting of DMEM (Dulbecco’s Modified Eagle Medium; Eurobio, Les Ulis, France) supplemented with 5% fetal calf serum (Hyclone, Perbio, Brebières, France), 2 mM L-glutamine, 100 U of penicillin/mL, and 50 µg of streptomycin/mL (Eurobio). The diluted blood samples were seeded into 96-well plates (200 µL/well) and stimulated with 10 µg/mL of concanavalin A or with 50 ng/mL of phorbol 12-myristate 13-acetate and 1 µg/mL of Ionomycin (PMA-Iono; Sigma, St. Quentin Fallavier, France). The lymphocytes from control wells containing only blood remained unstimulated. After 48 h of incubation, 0.5 mCi of 3H-methyl-thymidine (ICN, Orsay, France) was added to each well. After another 24 h of incubation, cells were harvested through glass-fiber filters (Whatman, Maidstone, UK) by means of an automatic harvester (Titerteck-Skatron, Molecular Devices, St. Grégoire, France). Incorporation of thymidine was measured with a liquid scintillation counter (Kontron Instruments, St. Quentin en Yvelines, France), and the results were expressed as mean counts per minute of the triplicate cultures.
Determination of IL-4 and Interferon-
Production
Cytokine production was also measured in whole blood supernatant as previously described for human samples (De Groote et al., 1996). Briefly, heparinized blood diluted 1:5 in complete culture medium was stimulated with PMA-Iono. Cytokine content was analyzed in the supernatants using the CytoSet ELISA kit (Bio-source International, Camarillo, CA) as previously described (Taranu et al., 2005). Briefly, purified fractions of antiswine IL-4 and interferon- (IFN- clones A155B 16F2 and A151D 5B8, respectively) were used as capture antibodies, in conjunction with the biotinylated antiswine IL-4 and IFN- monoclonal antibodies (clones A155B 15C6 and A151D 13C5, respectively). Streptavidin-horseradish peroxidase (Biosource) and TMB were used for detection. Absorbance was read at 450 nm using an ELISA plate reader and the Biolise 2.0 data management software. Recombinant swine IL-4 and IFN- were used as standards. The detection limits were 60 pg/mL and 91 pg/mL for IL-4 and IFN-, respectively, and the intraassay CV were 8.5 and 8.3% for IL-4 and IFN-, respectively.
Statistical Analysis
Performance, biochemical, and hematological variables were analyzed by ANOVA for a completely random design having a 2 (sex) x 4 (diet) factorial arrangement of treatments. Sex x diet interactions were not detected; therefore, main effect means are presented throughout the manuscript. When significant diet effects were detected, means were separated using linear and quadratic contrasts. Analyses were computed using the GLM procedure of SAS (version 8.01, SAS Inst. Inc., Cary, NC).
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RESULTS
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Effect of Low Concentration of DON on Animal Performance
One of the main adverse effects observed after DON exposure is reduced feed intake. In the present experiment, feed refusal was not observed during any period (d 1 to 14; d 15 to 28; or d 1 to 28) or by castrated male or female pigs. Moreover, natural contamination of the feed with 280 to 840 µg/kg of DON did not affect feed consumption or BW gain (Table 3).
Effect of Low Concentration of DON on Hematological and Biochemical Variables
At the end of the experiment, blood samples were taken from all the animals to investigate the effect of low concentration of DON on hematological and biochemical variables. As demonstrated in Table 4, low levels of DON in the diet did not alter white blood cell, red blood cell, or platelet counts as well as the relative number of granulocyte neutrophils and lymphocytes. A linear contrast analysis between control animals and treated animals regardless of DON level indicated an increase in neutrophils (P = 0.04) and lymphocytes (P = 0.03). Natural contamination of pig feed with 280 to 840 µg/kg of DON did not influence hematocrit, hemoglobin concentration, mean corpuscular hemoglobin concentration, and mean corpuscular volume. Biochemical variables were also analyzed (Table 5) and did not reveal an influence of low level of DON on biochemical parameters (Ca, Cl, K, Na, CO2, glucose, total proteins, urea, creatinine, bilirubin, cholesterol, triglycerides) and in the activity of plasmatic enzymes (alkaline phosphatase, glutamyl oxaloacetic, transaminase, glutamyl pyruvic transaminase, lactate dehydrogenase, and gamma-glutamyl transferase). A significant diet effect was shown for P (P = 0.025); the linear contrast was not significant (P = 0.671), but the quadratic contrast was significant (P = 0.017). No significant differences were observed on hematological and biochemical variables between castrated males and females (data not shown).
Effect of Low Concentration of DON on Immunological Variables
Effect of contamination of the diet with low doses of DON was also investigated on the immune response of the animals. The humoral response (concentration of the different immunoglobulin subsets in the plasma) and the cellular response (lymphocyte proliferation and cytokine production upon mitogenic treatment) were investigated. As described in Table 6, diets significantly affect the plasma concentration of IgA (P = 0.016). However, the linear contrast was not significant (P = 0.536), and only the quadratic contrast was significant (P = 0.002). Diets did affect the concentration of IgG and IgM. Similarly, the cellular response of the animals was not modified by the ingestion of feed contaminated with low doses of toxins. The capacity of blood cells to proliferate after concanavalin A or PMA-Iono stimulation (Figure 1) was not altered as well as the cytokine production upon PMA-Iono treatment (Table 6). No significant differences were observed between the castrated males and the females (data not shown).
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Figure 1. Effect of ingestion of deoxynivalenol (DON)-contaminated feed on lymphocyte proliferation. Pigs received a control diet or a diet contaminated with 280, 560, or 840 µg of DON/kg of diet (as-fed basis) for 4 wk. Blood samples were taken at the end of the experiment, diluted in cell culture media, and stimulated with concanavalin A or with phorbol-myristate-acetate(PMA)-ionomycin. After 48 h of incubation, cells were pulsed with 3H-methyl-thymidine before being harvested. Results are expressed as thymidine incorporation (counts per minute) from 12 animals (6 castrated males, 6 females) per group (means ± SEM).
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DISCUSSION
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In this experiment, diets containing 0, 280, 560, and 840 µg of DON/kg of feed were given to weanling piglets for 4 wk. These levels were chosen because they are in the range of the levels commonly found in European and North American cereals (Placinta et al., 1999; SCOOP, 2003; Schothorst and van Egmond, 2004). Although many studies have investigated the effect of DON on piglets, most have been performed with much greater concentration than those used in the current study.
It is well established that DON consumption reduces feed intake in pigs (Rotter et al., 1994; Smith et al., 1997; Dänicke et al., 2004). This effect is usually observed with feed contamination above 1,000 to 2,000 µg/kg (D’Mello et al., 1999; Swamy et al., 2003; Dänicke et al., 2004). Contamination of the feed with a greater level of toxin can lead to complete feed refusal and vomiting (Rotter et al., 1996). In the current study, feed was contaminated with low doses of toxin (up to 840 µg/kg) and we did not observe decreased feed consumption or BW. These results agree with those obtained by Döll et al. (2003), who observed no effect on performance in female pigs fed diets contaminated with 800 and 1,000 µg/kg of DON. Likewise, Rotter et al. (1994) found no differences in BW gain of animals when using diets contaminated with 750, 1,500 and 3,000 µg/kg of DON. However, they observed decreased feed intake of 2, 10, and 18% in animal fed with increasing doses of toxins (Rotter et al., 1994).
Limited information is available concerning the hematological and biochemical effects of low DON exposure (Harvey et al., 1989; Rotter et al., 1994; Drochner et al., 2004). In the current study, no effects of DON were observed on the 18 biochemical variables tested and on the 9 hematological variables measured (Tables 4 and 5). Using greater doses of DON in the feed (3,000 to 5,800 µg/kg feed), a decrease in Ca, P, Cl, total protein, and globulin was observed (Prelusky et al., 1994; Rotter et al., 1994; Swamy et al., 2002, 2003). In our trial, the linear effect of DON on P is not significant, and the quadratic effect is difficult to interpret because the range of variation between means is small, so we consider the effect inconsistent. No signs of liver damage (alteration of glutamyl oxaloacetic transaminase, lactate dehydrogenase, and gamma-glutamyl transferase) or liver protein synthesis (modification of total serum proteins) were observed in starter and growing pigs fed contaminated diets containing 3,500 to 4,100 µg/kg (Dänicke et al., 2004). Concerning the hematological variables, Rotter et al. (1994) observed increases of 10.3, 8.7, and 31% in total leukocyte count in pigs fed increasing concentrations of DON of 750, 1,500, and 3,000 µg/kg, respectively. Such increases were mainly due to an increase in the number of segmented neutrophils.
The immune system is very sensitive to DON (Pestka et al., 2004; Pestka and Smolinski, 2005). In mice, many in vivo and in vitro studies have described effects of DON on cellular and humoral response leading to altered cytokine synthesis, decreased lymphocyte proliferation, and increased IgA synthesis (Meky et al., 2001; Pestka et al., 2004). In swine, attempts to evaluate the effect of DON on humoral immune response have provided contradictory results. An increase in serum IgA has been described in some experiments, whereas other investigations report no significant changes in serum immunoglobulins. For example, IgA upregulation was detected in studies using 600 µg/kg of DON for 56 d (Drochner et al., 2004); 1,600 µg/kg of DON for 34 d (Pinton et al., 2004) or 4,600 µg/kg of DON for 21 d (Swamy et al., 2002). By contrast, other studies using 3,900 µg/kg of DON for 35 d (Döll et al., 2003) 4,600 µg/kg of DON for 14 d (Dänicke et al., 2004) or 5,800 µg/kg of DON for 21 d (Swamy et al., 2003) did not report any significant changes in the IgA levels. In the current study, there was no sign of impaired immunoglobulin production (IgA, IgM, or IgG) or disturbed functional capacity of lymphocytes (proliferation capacity and ability to produce IL-4 and IFN-) in pigs fed low doses of DON. Drochner et al. (2004) established a significant linear DON effect on log (IgA) level in female piglets consuming 300, 6,000, and 12,000 µg/kg of DON-contaminated diet for 8 wk. Such IgA levels ranged from 0.9 mg/mL in control animals to 0.9, 1.1, and 1.1 mg/mL in the animal group fed with contaminated diet. The increased IgA concentration in plasma was demonstrated by using a mixed model analysis allowing for autocorrelation among repeated measures and a logarithmic transformation (Drochner et al., 2004). In our trial, the linear effect of DON on IgA is not significant, and the quadratic effect is difficult to bind with the literature results obtained with greater DON levels, so we consider the effect of low levels is inconsistent. Results concerning the lymphocytes proliferation capacity agree with those reported by Rotter et al. (1994) who did not observe an effect on peripheral blood mononuclear cell proliferation in animals fed 750 µg/kg of DON-contaminated diet.
In conclusion, DON contamination of feed at very low doses (below 840 µg/kg) appears to have no effect on swine immune response or other biochemical and animal performance responses. These data could be of utility when setting legal limits for DON in swine feeds.
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Footnotes
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1 Acknowledgments: F. Accensi was supported by postdoctoral fellowships from INRA and from the French ministry of foreign affairs. This work was supported in part by the Transversalité INRA (Mycotoxines-P00263) Paris, France. 
2 These authors equally contributed to this work.
3 Corresponding author: ioswald{at}toulouse.inra.fr
Received for publication July 4, 2005.
Accepted for publication February 2, 2006.
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Abstract
INTRODUCTION
