The purpose of this review is to present information about raw materials that can be used in pig and poultry diets and the factors responsible for variations in their mycotoxin contents. The levels of mycotoxins in pig and poultry feeds are calculated based on mycotoxin contamination levels of the raw materials with different diet formulations, to highlight the important role the stage of production and the raw materials used can have on mycotoxins levels in diets. Our analysis focuses on mycotoxins for which maximum tolerated levels or regulatory guidelines exist, and for which sufficient contamination data are available. Raw materials used in feed formulation vary considerably depending on the species of animal, and the stage of production. Mycotoxins are secondary fungal metabolites whose frequency and levels also vary considerably depending on the raw materials used and on the geographic location where they were produced. Although several reviews of existing data and of the literature on worldwide mycotoxin contamination of food and feed are available, the impact of the different raw materials used on feed formulation has not been widely studied.
Fungal species and toxin contamination were determined in 110 cereal samples (54 maize, 35 wheat, and 21 barley) collected in the southeastern part of Romania from 2002 to 2004. The most frequent fungal contaminants belonged to Aspergillus and Fusarium, and maize was the most contaminated cereal. The main toxigenic species identified were Aspergillus flavus, Aspergillus fumigatus, Fusarium graminearum, and Fusarium culmorum in all cereals and Fusarium verticillioides in maize. The presence of aflatoxin B1 (AFB1), deoxynivalenol (DON), zearalenone (ZEA), fumonisins, and ochratoxin A was determined by enzyme-linked immunosorbent assay. More than 90% of the samples were contaminated with at least one toxin. Around 30% of maize samples were contaminated with AFB1, and in 20% of these samples the level of toxin exceeded that allowed by European Union regulations. In 48 and 42% of samples, levels of DON and ZEA, respectively, exceeded those allowed by the European Union. Neither fumonisins nor ochratoxin A were found in samples from any year or cereal. These results indicate that cereals produced in Romania have a particular pattern of mycoflora and mycotoxin contamination because DON and ZEA in addition to AFB1 were found.
The interactions between mycotoxins and gut microbiota were discovered early in animals and explained part of the differences in susceptibility to mycotoxins among species. Isolation of microbes present in the gut responsible for biotransformation of mycotoxins into less toxic metabolites and for binding mycotoxins led to the development of probiotics, enzymes, and cell extracts that are used to prevent mycotoxin toxicity in animals. More recently, bioactivation of mycotoxins into toxic compounds, notably through the hydrolysis of masked mycotoxins, revealed that the health benefits of the effect of the gut microbiota on mycotoxins can vary strongly depending on the mycotoxin and the microbe concerned. Interactions between mycotoxins and gut microbiota can also be observed through the effect of mycotoxins on the gut microbiota. Changes of gut microbiota secondary to mycotoxin exposure may be the consequence of the antimicrobial properties of mycotoxins or the toxic effect of mycotoxins on epithelial and immune cells in the gut, and liberation of antimicrobial peptides by these cells. Whatever the mechanism involved, exposure to mycotoxins leads to changes in the gut microbiota composition at the phylum, genus, and species level. These changes can lead to disruption of the gut barrier function and bacterial translocation. Changes in the gut microbiota composition can also modulate the toxicity of toxic compounds, such as bacterial toxins and of mycotoxins themselves. A last consequence for health of the change in the gut microbiota secondary to exposure to mycotoxins is suspected through variations observed in the amount and composition of the volatile fatty acids and sphingolipids that are normally present in the digesta, and that can contribute to the occurrence of chronic diseases in human. The purpose of this work is to review what is known about mycotoxin and gut microbiota interactions, the mechanisms involved in these interactions, and their practical application, and to identify knowledge gaps and future research needs.
The objective of this study was to measure the effects of chronic exposure to fumonisins via the ingestion of feed containing naturally contaminated corn in growing pigs infected or not with Salmonella spp. This exposure to a moderate dietary concentration of fumonisins (11.8 ppm) was sufficient to induce a biological effect in pigs (Sa/So ratio), but no mortality or pathology was observed over 63 days of exposure. No mortality or related clinical signs, even in cases of inoculation with Salmonella (5 × 104 CFU), were observed either. Fumonisins, at these concentrations, did not affect the ability of lymphocytes to proliferate in the presence of mitogens, but after seven days post-inoculation they led to inhibition of the ability of specific Salmonella lymphocytes to proliferate following exposure to a specific Salmonella antigen. However, the ingestion of fumonisins had no impact on Salmonella translocation or seroconversion in inoculated pigs. The inoculation of Salmonella did not affect faecal microbiota profiles, but exposure to moderate concentrations of fumonisins transiently affected the digestive microbiota balance. In cases of co-infection with fumonisins and Salmonella, the microbiota profiles were rapidly and clearly modified as early as 48 h post-Salmonella inoculation. Therefore under these experimental conditions, exposure to an average concentration of fumonisins in naturally contaminated feed had no effect on pig health but did affect the digestive microbiota balance, with Salmonella exposure amplifying this phenomenon.
The development of fungal endophytes of the genus Epichloë in grasses results in the production of different groups of alkaloids, whose mechanism and biological spectrum of toxicity can differ considerably. Ergot alkaloids, when present in endophyte-infected tall fescue, are responsible for “fescue toxicosis” in livestock, whereas indole-diterpene alkaloids, when present in endophyte-infected ryegrass, are responsible for “ryegrass staggers”. In contrast, peramine and loline alkaloids are deterrent and/or toxic to insects. Other toxic effects in livestock associated with the consumption of endophyte-infected grass that contain ergot alkaloids include the “sleepy grass” and “drunken horse grass” diseases. Although ergovaline is the main ergopeptine alkaloid produced in endophyte-infected tall fescue and is recognized as responsible for fescue toxicosis, a number of questions still exist concerning the profile of alkaloid production in tall fescue and the worldwide distribution of tall fescue toxicosis. The purpose of this review is to present ergot alkaloids produced in endophyte-infected grass, the factors of variation of their level in plants, and the diseases observed in the mammalian species as relate to the profiles of alkaloid production. In the final section, interactions between ergot alkaloids and drug-metabolizing enzymes are presented as mechanisms that could contribute to toxicity.
Perennial ryegrass (Lolium perenne) infected by Epichloë festucae var. lolii contains alkaloids that are responsible for toxicosis in several countries, but few cases are reported in Europe. Lolitrem B is generally the most abundant alkaloid and is recognized to be responsible for livestock staggers, whereas ergovaline is less frequently documented in perennial ryegrass. Lolitrem B and ergovaline were monitored over a three-year period in endophyte-infected perennial ryegrass 'Samson' sown in southern France. Alkaloid concentrations were strongly influenced by the stage of maturity of the plant; maximum concentrations were always measured at the fully ripe stage. Over the three years of analysis, variations in lolitrem B in the whole plant at the fully ripe stage were low (from 1296 to maximum 1871 μg/kg dry matter), whereas ergovaline varied considerably (from 526 to 2322 μg/kg dry matter), suggesting that abiotic factors play a key role in determining ergovaline levels in endophyte-infected perennial ryegrass.
Fusarium mycotoxins (FUS) occur frequently in poultry diets, and regulatory limits are laid down in several countries. However, the limits were established for exposure to a single mycotoxin, whereas multiple contamination is more realistic, and different studies have demonstrated that it is not possible to predict interactions between mycotoxins. The purpose of this study was thus to compare the toxic effect of deoxynivalenol (DON), fumonisins (FB) and zearalenone (ZON), alone and in combination on broiler chickens, at the maximum tolerated level established by the EU for poultry feed. Experimental corn-soybean diets incorporated ground cultured toxigenic Fusarium strains. One feed was formulated for chickens 0 to 10 days old and another for chickens 11 to 35 days old. The control diets were mycotoxin free, the DON diets contained 5 mg DON/kg, the FB diet contained 20 mg FB1 + FB2/kg, and the ZON diet contained 0.5mg ZON/kg. The DONFBZON diet contained 5, 20, and 0.5 mg/kg of DON, FB1 + FB2, and ZON, respectively. Diets were distributed ad libitum to 70 broilers (male Ross PM3) separated into five groups of 14 chickens each reared in individual cages from one to 35 days of age. On day 35, after a starvation period of 8 h, a blood sample was collected, and all the animals were killed and autopsied. No difference between groups that could be attributed to FUS was observed in performances, the relative weight of organs, biochemistry, histopathology, intestinal morphometry, variables of oxidative damage, and markers of testicle toxicity. A significant increase in sphinganine and in the sphinganine to sphingosine ratio was observed in broilers fed FB. Taken together, these results suggest that the regulatory guidelines established for single contamination of broiler chickens fed with DON, FB, and ZON can also be used in the case of multiple contamination with these toxins.
Fusariotoxins are mycotoxins produced by different species of the genus Fusarium whose occurrence and toxicity vary considerably. Despite the fact avian species are highly exposed to fusariotoxins, the avian species are considered as resistant to their toxic effects, partly because of low absorption and rapid elimination, thereby reducing the risk of persistence of residues in tissues destined for human consumption. This review focuses on the main fusariotoxins deoxynivalenol, T-2 and HT-2 toxins, zearalenone and fumonisin B1 and B2. The key parameters used in the toxicokinetic studies are presented along with the factors responsible for their variations. Then, each toxin is analyzed separately. Results of studies conducted with radiolabelled toxins are compared with the more recent data obtained with HPLC/MS-MS detection. The metabolic pathways of deoxynivalenol, T-2 toxin, and zearalenone are described, with attention paid to the differences among the avian species. Although no metabolite of fumonisins has been reported in avian species, some differences in toxicokinetics have been observed. All the data reviewed suggest that the toxicokinetics of fusariotoxins in avian species differs from those in mammals, and that variations among the avian species themselves should be assessed.
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