The role of roughage provision on the absorption and disposition of the mycotoxin deoxynivalenol and its acetylated derivatives in calves: from field observations to toxicokinetics

Abstract

A clinical case in Belgium demonstrated that feeding a feed concentrate containing considerable levels of deoxynivalenol (DON, 1.13 mg/kg feed) induced severe liver failure in 2-to 3-month-old beef calves. Symptoms disappeared by replacing the highly contaminated corn and by stimulating ruminal development via roughage administration. A multi-mycotoxin contamination was demonstrated in feed samples collected at 15 different veal farms in Belgium. DON was most prevalent, contaminating 80% of the roughage samples (mixed straw and maize silage; average concentration in positives: 637 ± 621 µg/ kg, max. 1818 µg/kg), and all feed concentrate samples (411 ± 156 µg/kg, max. 693 µg/kg). In order to evaluate the impact of roughage provision and its associated ruminal development on the gastro-intestinal absorption and biodegradation of DON and its acetylated derivatives (3-and 15-ADON) in calves, a toxicokinetic study was performed with two ruminating and two non-ruminating male calves. Animals received in succession a bolus of DON (120 µg/kg bodyweight (BW)), 15-ADON (50 µg/kg BW), and 3-ADON (25 µg/kg) by intravenous (IV) injection or per os (PO) in a cross-over design. The absolute oral bioavailability of DON was much higher in non-ruminating calves (50.7 ± 33.0%) compared to ruminating calves (4.1 ± 4.5%). Immediately following exposure, 3-and 15-ADON were hydrolysed to DON in ruminating calves. DON and its acetylated metabolites were mainly metabolized to DON-3-glucuronide, however, also small amounts of DON-15-glucuronide were detected in urine. DON degradation to deepoxy-DON (DOM-1) was only observed to a relevant extent in ruminating calves. Consequently, toxicity of DON in calves is closely related to roughage provision and the associated stage of ruminal development.Keywords Biodegradation · Calf · Deoxynivalenol · 3-and 15-Acetyldeoxynivalenol · Mycotoxin · Toxicokinetics Bonnie Valgaeren and Léonard Théron contributed equally to this work.Alfons Callebaut: Deceased. Electronic supplementary materialThe online version of this article (https ://doi.

A Review of the Impact of Mycotoxins on Dairy Cattle Health: Challenges for Food Safety and Dairy Production in Sub-Saharan Africa

“…In contrary, Seeling et al [41] reported no effect on feed intake on feeding approximately 3.4 mg DON per kg at a reference DM of 88% complete ration, similar to Winkler et al using 5 mg DON/kg feed showed no effect on performance parameters on dairy cattle [65]. In calves, Valgaeren et al [49] reported severe liver failure in 2-3 months old calves with no functioning rumen induced by 1.13 mg DON/kg feed, indicating the significance of rumen microbiota in DON degradation.…”

“…The intact ruminal epithelium is an effective barrier against DON and ZEN [47]. DON is degraded by the ruminal microbiota to the less toxic metabolite de-epoxy DON (DOM-1) [48,49]. A study by Seeling et al [48] reported 94%-99% biotransformation of DON to DOM-1.…”

“…Keese et al [47] reported no significant amount of unmetabolized DON passing through the ruminal epithelium in cattle fed 50% concentrate proportion and 5.3 mg DON/kg DM, nor if a ration with 60% concentrate and 4.6 mg/kg DM fed for a total period of 29 weeks; however, DOM-1 was present in serum, which indicates systemic uptake. Valgaeren et al [49] studied the role of roughage provision on the absorption and disposition of DON and its acetylated derivatives in calves and observed an absolute DON oral bioavailability of 4.1% in ruminating calves compared to 50.7% in non-ruminating calves, indicating the ability of the rumen to degrade DON. Recently, Debevere et al [50] showed the degradation of DON was hampered when ruminal pH was low (pH 5.8), as is the case in cattle suffering from sub-acute rumen acidosis.…”

In Vitro Rumen Simulations Show a Reduced Disappearance of Deoxynivalenol, Nivalenol and Enniatin B at Conditions of Rumen Acidosis and Lower Microbial Activity

“…However, in high-productive dairy cows, mycotoxin-associated subclinical health problems may occur, reflected by vague and non-specific symptoms and periodic decrease in milk production [2]. One possible reason could be the higher proportion of maize silage in the ration of higher yielders [2], which is more vulnerable to contamination with multiple mycotoxins than e.g., grassland products [12][13][14]. However, in Belgium and the Netherlands, maize silage is also given to non-lactating cows instead of grassland products as maize silage is low in calcium and potassium which diminish the incidence of milk fever at the beginning of lactation [15,16].…”

Deoxynivalenol: Masked forms, fate during food processing, and potential biological remedies

“…DON‐3‐GlcA was the major metabolite of DON and acetylated forms. Scarce DON‐15‐GlcA was found in urine (Valgaeren et al., 2019). Another study conducted both in vivo (in human liver, small intestine, and kidney) and in vitro (in HepG2 cells, Caco‐2 cells, and T84 cells) confirmed complete deacetylation fate of 3‐ADON and 15‐ADON, and liver and small intestine were identified as the main site of deacetylation reaction in humans (Figure 2d).…”