Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme

The mycotoxin zearalenone (ZEN) is a frequent contaminant of animal feed and is well known for its estrogenic effects in animals. Cattle are considered less sensitive to ZEN than pigs. However, ZEN has previously been shown to be converted to the highly estrogenic metabolite α-zearalenol (α-ZEL) in...

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Main Authors: Christiane Gruber-Dorninger, Johannes Faas, Barbara Doupovec, Markus Aleschko, Christian Stoiber, Andreas Höbartner-Gußl, Karin Schöndorfer, Manuela Killinger, Qendrim Zebeli, Dian Schatzmayr
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Language:English
Published: MDPI AG 2021-01-01
Series:Toxins
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Online Access:https://www.mdpi.com/2072-6651/13/2/84
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author Christiane Gruber-Dorninger
Johannes Faas
Barbara Doupovec
Markus Aleschko
Christian Stoiber
Andreas Höbartner-Gußl
Karin Schöndorfer
Manuela Killinger
Qendrim Zebeli
Dian Schatzmayr
author_facet Christiane Gruber-Dorninger
Johannes Faas
Barbara Doupovec
Markus Aleschko
Christian Stoiber
Andreas Höbartner-Gußl
Karin Schöndorfer
Manuela Killinger
Qendrim Zebeli
Dian Schatzmayr
author_sort Christiane Gruber-Dorninger
collection DOAJ
description The mycotoxin zearalenone (ZEN) is a frequent contaminant of animal feed and is well known for its estrogenic effects in animals. Cattle are considered less sensitive to ZEN than pigs. However, ZEN has previously been shown to be converted to the highly estrogenic metabolite α-zearalenol (α-ZEL) in rumen fluid in vitro. Here, we investigate the metabolism of ZEN in the reticulorumen of dairy cows. To this end, rumen-fistulated non-lactating Holstein Friesian cows (<i>n</i> = 4) received a one-time oral dose of ZEN (5 mg ZEN in 500 g concentrate feed) and the concentrations of ZEN and ZEN metabolites were measured in free rumen liquid from three reticulorumen locations (reticulum, ventral sac and dorsal mat layer) during a 34-h period. In all three locations, α-ZEL was the predominant ZEN metabolite and β-zearalenol (β-ZEL) was detected in lower concentrations. ZEN, α-ZEL and β-ZEL were eliminated from the ventral sac and reticulum within 34 h, yet low concentrations of ZEN and α-ZEL were still detected in the dorsal mat 34 h after ZEN administration. In a second step, we investigated the efficacy of the enzyme zearalenone hydrolase ZenA (EC 3.1.1.-, commercial name ZEN<i>zyme</i><sup>®</sup>, BIOMIN Holding GmbH, Getzersdorf, Austria) to degrade ZEN to the non-estrogenic metabolite hydrolyzed zearalenone (HZEN) in the reticulorumen in vitro and in vivo. ZenA showed a high ZEN-degrading activity in rumen fluid in vitro. When ZenA was added to ZEN-contaminated concentrate fed to rumen-fistulated cows (<i>n</i> = 4), concentrations of ZEN, α-ZEL and β-ZEL were significantly reduced in all three reticulorumen compartments compared to administration of ZEN-contaminated concentrate without ZenA. Upon ZenA administration, degradation products HZEN and decarboxylated HZEN were detected in the reticulorumen. In conclusion, endogenous metabolization of ZEN in the reticulorumen increases its estrogenic potency due to the formation of α-ZEL. Our results suggest that application of zearalenone hydrolase ZenA as a feed additive may be a promising strategy to counteract estrogenic effects of ZEN in cattle.
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spelling doaj.art-065777cccd9647e09baa167a558f5e7e2023-12-03T14:22:56ZengMDPI AGToxins2072-66512021-01-011328410.3390/toxins13020084Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading EnzymeChristiane Gruber-Dorninger0Johannes Faas1Barbara Doupovec2Markus Aleschko3Christian Stoiber4Andreas Höbartner-Gußl5Karin Schöndorfer6Manuela Killinger7Qendrim Zebeli8Dian Schatzmayr9BIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaInstitute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, AustriaBIOMIN Research Center, BIOMIN Holding GmbH, 3430 Tulln, AustriaThe mycotoxin zearalenone (ZEN) is a frequent contaminant of animal feed and is well known for its estrogenic effects in animals. Cattle are considered less sensitive to ZEN than pigs. However, ZEN has previously been shown to be converted to the highly estrogenic metabolite α-zearalenol (α-ZEL) in rumen fluid in vitro. Here, we investigate the metabolism of ZEN in the reticulorumen of dairy cows. To this end, rumen-fistulated non-lactating Holstein Friesian cows (<i>n</i> = 4) received a one-time oral dose of ZEN (5 mg ZEN in 500 g concentrate feed) and the concentrations of ZEN and ZEN metabolites were measured in free rumen liquid from three reticulorumen locations (reticulum, ventral sac and dorsal mat layer) during a 34-h period. In all three locations, α-ZEL was the predominant ZEN metabolite and β-zearalenol (β-ZEL) was detected in lower concentrations. ZEN, α-ZEL and β-ZEL were eliminated from the ventral sac and reticulum within 34 h, yet low concentrations of ZEN and α-ZEL were still detected in the dorsal mat 34 h after ZEN administration. In a second step, we investigated the efficacy of the enzyme zearalenone hydrolase ZenA (EC 3.1.1.-, commercial name ZEN<i>zyme</i><sup>®</sup>, BIOMIN Holding GmbH, Getzersdorf, Austria) to degrade ZEN to the non-estrogenic metabolite hydrolyzed zearalenone (HZEN) in the reticulorumen in vitro and in vivo. ZenA showed a high ZEN-degrading activity in rumen fluid in vitro. When ZenA was added to ZEN-contaminated concentrate fed to rumen-fistulated cows (<i>n</i> = 4), concentrations of ZEN, α-ZEL and β-ZEL were significantly reduced in all three reticulorumen compartments compared to administration of ZEN-contaminated concentrate without ZenA. Upon ZenA administration, degradation products HZEN and decarboxylated HZEN were detected in the reticulorumen. In conclusion, endogenous metabolization of ZEN in the reticulorumen increases its estrogenic potency due to the formation of α-ZEL. Our results suggest that application of zearalenone hydrolase ZenA as a feed additive may be a promising strategy to counteract estrogenic effects of ZEN in cattle.https://www.mdpi.com/2072-6651/13/2/84mycotoxinzearalenonerumenmetabolismdegradationhydrolase
spellingShingle Christiane Gruber-Dorninger
Johannes Faas
Barbara Doupovec
Markus Aleschko
Christian Stoiber
Andreas Höbartner-Gußl
Karin Schöndorfer
Manuela Killinger
Qendrim Zebeli
Dian Schatzmayr
Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
Toxins
mycotoxin
zearalenone
rumen
metabolism
degradation
hydrolase
title Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
title_full Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
title_fullStr Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
title_full_unstemmed Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
title_short Metabolism of Zearalenone in the Rumen of Dairy Cows with and without Application of a Zearalenone-Degrading Enzyme
title_sort metabolism of zearalenone in the rumen of dairy cows with and without application of a zearalenone degrading enzyme
topic mycotoxin
zearalenone
rumen
metabolism
degradation
hydrolase
url https://www.mdpi.com/2072-6651/13/2/84
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