Feedborne Mycotoxins Beauvericin and Enniatins and Livestock Animals
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
Grantová podpora
Grant Agency of Masaryk University : MUNI/A/1252/2019
Internal Grant Agency University of Veterinary and Pharmaceutical Sciences : 219/2018/FVHE
PubMed
33466409
PubMed Central
PMC7824875
DOI
10.3390/toxins13010032
PII: toxins13010032
Knihovny.cz E-zdroje
- Klíčová slova
- beauvericin, carry-over, enniatins, feed, metabolism, minor mycotoxins,
- MeSH
- depsipeptidy toxicita MeSH
- dobytek MeSH
- jedlá semena toxicita MeSH
- kontaminace potravin analýza MeSH
- krmivo pro zvířata toxicita MeSH
- mykotoxiny * MeSH
- terpeny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- beauvericin MeSH Prohlížeč
- depsipeptidy MeSH
- enniatins MeSH Prohlížeč
- fusaproliferin MeSH Prohlížeč
- mykotoxiny * MeSH
- terpeny MeSH
Mycotoxins are secondary metabolites produced by several species of fungi, including the Fusarium, Aspergillus, and Penicillium species. Currently, more than 300 structurally diverse mycotoxins are known, including a group called minor mycotoxins, namely enniatins, beauvericin, and fusaproliferin. Beauvericin and enniatins possess a variety of biological activities. Their antimicrobial, antibiotic, or ionoforic activities have been proven and according to various bioassays, they are believed to be toxic. They are mainly found in cereal grains and their products, but they have also been detected in forage feedstuff. Mycotoxins in feedstuffs of livestock animals are of dual concern. First one relates to the safety of animal-derived food. Based on the available data, the carry-over of minor mycotoxins from feed to edible animal tissues is possible. The second concern relates to detrimental effects of mycotoxins on animal health and performance. This review aims to summarize current knowledge on the relation of minor mycotoxins to livestock animals.
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Pitt J.I. Toxigenic fungi and mycotoxins. Br. Med. Bull. 2000;56:184–192. doi: 10.1258/0007142001902888. PubMed DOI
Reverberi M., Ricelli A., Zjalic S., Fabbri A.A., Fanelli C. Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl. Microbiol. Biotechnol. 2010;87:899–911. doi: 10.1007/s00253-010-2657-5. PubMed DOI
Escrivá L., Font G., Manyes L., Berrada H. Studies on the Presence of Mycotoxins in Biological Samples: An Overview. Toxins. 2017;9:251. doi: 10.3390/toxins9080251. PubMed DOI PMC
Guerre P. Fusariotoxins in Avian Species: Toxicokinetics, Metabolism and Persistence in Tissues. Toxins. 2015;7:2289–2305. doi: 10.3390/toxins7062289. PubMed DOI PMC
Monti S.M., Fogliano V., Logrieco A., Ferracane R., Ritieni A. Simultaneous Determination of Beauvericin, Enniatins, and Fusaproliferin by High Performance Liquid Chromatography. J. Agric. Food Chem. 2000;48:3317–3320. doi: 10.1021/jf990373n. PubMed DOI
Capriotti A.L., Caruso G., Cavaliere C., Foglia P., Samperi R., Laganà A. Multiclass mycotoxin analysis in food, environmental and biological matrices with chromatography/mass spectrometry. Mass Spectrom. Rev. 2012;31:466–503. doi: 10.1002/mas.20351. PubMed DOI
Bryden W.L. Mycotoxin contamination of the feed supply chain: Implications for animal productivity and feed security. Anim. Feed Sci. Technol. 2012;173:134–158. doi: 10.1016/j.anifeedsci.2011.12.014. DOI
European Food Safety Authority (EFSA) Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to Aflatoxin B1 as undesirable substance in animal feed. EFSA J. 2004;2:39. doi: 10.2903/j.efsa.2004.39. DOI
European Food Safety Authority (EFSA) Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to Deoxynivalenol (DON) as undesirable substance in animal feed. EFSA J. 2004;2:73. doi: 10.2903/j.efsa.2004.73. DOI
European Food Safety Authority (EFSA) Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to Zearalenone as undesirable substance in animal feed. EFSA J. 2004;2:89. doi: 10.2903/j.efsa.2004.89. DOI
European Food Safety Authority (EFSA) Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to ochratoxin A (OTA) as undesirable substance in animal feed. EFSA J. 2004;2:101. doi: 10.2903/j.efsa.2004.101. DOI
European Food Safety Authority (EFSA) Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to fumonisins as undesirable substances in animal feed. EFSA J. 2005;3:235. doi: 10.2903/j.efsa.2005.235. DOI
Hamill R.L., Higgens C.E., Boaz H.E., Gorman M. Structure of Beauvericin, a New Depsipeptide Antibiotic Toxic to Artemia Salina. Tetrahedron Lett. 1969;49:4255–4258. doi: 10.1016/S0040-4039(01)88668-8. DOI
Gupta S., Krasnoff S.B., Underwood N.L., Renwick J.A.A., Roberts D.W. Isolation of beauvericin as an insect toxin from Fusarium semitectum and Fusarium moniliforme var. subglutinans. Mycopathologia. 1991;115:185–189. doi: 10.1007/BF00462223. PubMed DOI
Santini A., Meca G., Uhlig S., Ritieni A. Fusaproliferin, beauvericin and enniatins: Occurrence in food—A review. World Mycotoxin J. 2012;5:71–81. doi: 10.3920/WMJ2011.1331. DOI
Paciolla C., Dipierro N., Mulè G., Logrieco A., Dipierro S. The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiol. Mol. Plant Pathol. 2004;65:49–56. doi: 10.1016/j.pmpp.2004.07.006. DOI
García-Herranz V., Valdehita A., Navas J.M., Fernández-Cruz M.L. Cytotoxicity against Fish and Mammalian Cell Lines and Endocrine Activity of the Mycotoxins Beauvericin, Deoxynivalenol and Ochratoxin-A. Food Chem. Toxicol. 2019;127:288–297. doi: 10.1016/j.fct.2019.01.036. PubMed DOI
Juan C., Manyes L., Font G., Juan-García A. Evaluation of immunologic effect of Enniatin A and quantitative determination in feces, urine and serum on treated Wistar rats. Toxicon. 2014;87:45–53. doi: 10.1016/j.toxicon.2014.05.005. PubMed DOI
Calo’ L., Fornelli F., Nenna S., Tursi A., Caiaffa M.F., Macchia L. Beauvericin cytotoxicity to the invertebrate cell line SF-9. J. Appl. Genet. 2003;44:515–520. PubMed
Macchia L., Caiffa M.F., Fornelli F., Calo L., Nenna S., Moretti A., Logrieco A., Tursi A. Apoptosis induced by the Fusarium mycotoxin beauvericin in mammalian cells. Appl. Genet. 2002;43:363–371.
Taevernier L., Veryser L., Roche N., Peremans K., Burvenich C., Delesalle C., De Spiegeleer B. Human skin permeation of emerging mycotoxins (beauvericin and enniatins) J. Expo. Sci. Environ. Epidemiol. 2016;26:277–287. doi: 10.1038/jes.2015.10. PubMed DOI
Olleik H., Nicoletti C., Lafond M., Courvoisier-Dezord E., Xue P., Hijazi A., Baydoun E., Perrier J., Maresca M. Comparative Structure–Activity Analysis of the Antimicrobial Activity, Cytotoxicity, and Mechanism of Action of the Fungal Cyclohexadepsipeptides Enniatins and Beauvericin. Toxins. 2019;11:514. doi: 10.3390/toxins11090514. PubMed DOI PMC
Escrivá L., Font G., Manyes L. In vivo toxicity studies of fusarium mycotoxins in the last decade: A review. Food Chem. Toxicol. 2015;78:185–206. doi: 10.1016/j.fct.2015.02.005. PubMed DOI
Meca G., Sospedra I., Soriano J.M., Ritieni A., Moretti A., Mañes J. Antibacterial effect of the bioactive compound beauvericin produced by Fusarium proliferatum on solid medium of wheat. Toxicon. 2010;56:349–354. doi: 10.1016/j.toxicon.2010.03.022. PubMed DOI
Madhyastha M.S., Marquardt R.R., Frohlich A.A., Borsa J. Optimization of Yeast Bioassay for Trichothecene Mycotoxins. J. Food Prot. 1994;57:490–495. doi: 10.4315/0362-028X-57.6.490. PubMed DOI
Castlebury L.A., Sutherland J.B., Tanner L.A., Henderson A.L., Cerniglia C.E. Short Communication: Use of a bioassay to evaluate the toxicity of beauvericin to bacteria. World J. Microbiol. Biotechnol. 1999;15:131–133. doi: 10.1023/A:1008895421989. DOI
Wu X.-F., Xu R., Ouyang Z.-J., Qian C., Shen Y., Wu X.-D., Gu Y.-H., Xu Q., Sun Y. Beauvericin Ameliorates Experimental Colitis by Inhibiting Activated T Cells via Downregulation of the PI3K/Akt Signaling Pathway. PLoS ONE. 2013;8 doi: 10.1371/journal.pone.0083013. PubMed DOI PMC
Plattner P.A., Nager U. Über die Chemie des Enniatins. Experientia. 1947;3:325–326. doi: 10.1007/BF02164246. PubMed DOI
Blais L.A., Simon J.W.A., Blackwell B.A., Greenhalgh R., Miller J.D. Isolation and characterization of enniatins from Fusarium avenaceum DAOM 196490. Can. J. Chem. 1992;70:1281–1287. doi: 10.1139/v92-165. DOI
Sy-Cordero A.A., Pearce C.J., Oberlies N.H. Revisiting the enniatins: A review of their isolation, biosynthesis, structure determination and biological activities. J. Antibiot. 2012;65:541–549. doi: 10.1038/ja.2012.71. PubMed DOI PMC
Supothina S., Isaka M., Kirtikara K., Tanticharoen M., Thebtaranonth Y. Enniatin Production by the Entomopathogenic Fungus Verticillium hemipterigenum BCC 1449. J. Antibiot. 2004;57:732–738. doi: 10.7164/antibiotics.57.732. PubMed DOI
Morrison E., Kosiak B., Ritieni A., Aastveit A.H., Uhlig S., Bernhoft A. Mycotoxin Production by Fusarium avenaceum Strains Isolated from Norwegian Grain and the Cytotoxicity of Rice Culture Extracts to Porcine Kidney Epithelial Cells. J. Agric. Food Chem. 2002;50:3070–3075. doi: 10.1021/jf011532h. PubMed DOI
Firakova S., Šturdíková M., Liptaj T., Prónayová N., Bezáková L., Proksa B. Enniatins produced by Fusarium dimerum, an endophytic fungal strain. Pharmazie. 2008;63:539–541. doi: 10.1691/ph.2008.7831. PubMed DOI
Kabak B., Dobson A.D.W., Var I. Strategies to Prevent Mycotoxin Contamination of Food and Animal Feed: A Review. Crit. Rev. Food Sci. Nutr. 2006;46:593–619. doi: 10.1080/10408390500436185. PubMed DOI
Grove J.F., Pople M. The insecticidal activity of beauvericin and the enniatin complex. Mycopathologia. 1980;70:103–105. doi: 10.1007/BF00443075. DOI
Meca G., Sospedra I., Valero M.A., Mañes J., Font G., Ruiz M.J. Antibacterial Activity of the Enniatin B, Produced by Fusarium Tricinctum in Liquid Culture, and Cytotoxic Effects on Caco-2 Cells. Toxicol. Mech. Methods. 2011;21:503–512. doi: 10.3109/15376516.2011.556202. PubMed DOI
Roig M., Meca G., Marín R., Ferrer E., Mañes J. Antibacterial Activity of the Emerging Fusarium Mycotoxins Enniatins A, A1, A2, B, B1, and B4 on Probiotic Microorganisms. Toxicon. 2014;85:1–4. doi: 10.1016/j.toxicon.2014.04.007. PubMed DOI
Ivanova L., Skjerve E., Eriksen G.S., Uhlig S. Cytotoxicity of enniatins A, A1, B, B1, B2 and B3 from Fusarium avenaceum. Toxicon. 2006;47:868–876. doi: 10.1016/j.toxicon.2006.02.012. PubMed DOI
Lu H., Fernández-Franzón M., Font G., Ruiz M.J. Toxicity evaluation of individual and mixed enniatins using an in vitro method with CHO-K1 cells. Toxicol. In Vitro. 2013;27:672–680. doi: 10.1016/j.tiv.2012.11.009. PubMed DOI
Sotnichenko A., Pantsov E., Shinkarev D., Okhanov V. Hydrophobized Reversed-Phase Adsorbent for Protection of Dairy Cattle against Lipophilic Toxins from Diet. Efficiensy In Vitro and In Vivo. Toxins. 2019;11:256. doi: 10.3390/toxins11050256. PubMed DOI PMC
Kouri K., Lemmens M., Lemmens-Gruber R. Beauvericin-induced channels in ventricular myocytes and liposomes. Biochim. Biophys. Acta BBA Biomembr. 2003;1609:203–210. doi: 10.1016/S0005-2736(02)00689-2. PubMed DOI
Uhlig S., Ivanova L., Petersen D., Kristensen R. Structural studies on minor enniatins from Fusarium sp. VI 03441: Novel N-methyl-threonine containing enniatins. Toxicon. 2009;53:734–742. doi: 10.1016/j.toxicon.2009.02.014. PubMed DOI
Kouri K., Duchen M.R., Lemmens-Gruber R. Effects of Beauvericin on the Metabolic State and Ionic Homeostasis of Ventricular Myocytes of the Guinea Pig. Chem. Res. Toxicol. 2005;18:1661–1668. doi: 10.1021/tx050096g. PubMed DOI
Uhlig S., Jestoi M., Parikka P. Fusarium avenaceum—The North European situation. Int. J. Food Microbiol. 2007;119:17–24. doi: 10.1016/j.ijfoodmicro.2007.07.021. PubMed DOI
Behm C., Degen G.H., Föllmann W. The Fusarium toxin enniatin B exerts no genotoxic activity, but pronounced cytotoxicity in vitro. Mol. Nutr. Food Res. 2009;53:423–430. doi: 10.1002/mnfr.200800183. PubMed DOI
Kamyar M., Rawnduzi P., Studenik C.R., Kouri K., Lemmens-Gruber R. Investigation of the electrophysiological properties of enniatins. Arch. Biochem. Biophys. 2004;429:215–223. doi: 10.1016/j.abb.2004.06.013. PubMed DOI
Oliveira C.A.F., Ivanova L., Solhaug A., Fæste C.K. Enniatin B1-Induced Lysosomal Membrane Permeabilization in Mouse Embryonic Fibroblasts. Mycotoxin Res. 2020;36:23–30. doi: 10.1007/s12550-019-00366-8. PubMed DOI
Feed & Food Statistical Yearbook. [(accessed on 3 November 2020)];2018 Available online: https://fefac.eu/wp-content/uploads/2020/07/feedfood2018.pdf.
Schenck J., Müller C., Djurle A., Jensen D.F., O’Brien M., Johansen A., Rasmussen P.H., Spörndly R. Occurrence of filamentous fungi and mycotoxins in wrapped forages in Sweden and Norway and their relation to chemical composition and management. Grass Forage Sci. 2019;74:613–625. doi: 10.1111/gfs.12453. DOI
Ivić D., Domijan A.-M., Peraica M., Miličević T., Cvjetković B. Fusarium spp. Contamination of Wheat, Maize, Soybean, and Pea Grain in Croatia. Arch. Ind. Hyg. Toxicol. 2009;60:435–442. doi: 10.2478/10004-1254-60-2009-1963. PubMed DOI
Scudamore K.A., Livesey C.T. Occurrence and Significance of Mycotoxins in Forage Crops and Silage: A Review. J. Sci. Food Agric. 1998;77:1–17. doi: 10.1002/(SICI)1097-0010(199805)77:1<1::AID-JSFA9>3.0.CO;2-4. DOI
McElhinney C., Danaher M., Elliott C.T., O’Kiely P. On-farm factors relating to mycotoxin occurrence and other chemical compositional traits in grass silages in Ireland. World Mycotoxin J. 2016;9:505–516. doi: 10.3920/WMJ2016.2060. DOI
Jestoi M., Rokka M., Yli-Mattila T., Parikka P., Rizzo A., Peltonen K. Presence and concentrations of the Fusarium-related mycotoxins beauvericin, enniatins and moniliformin in finnish grain samples. Food Addit. Contam. 2004;21:794–802. doi: 10.1080/02652030410001713906. PubMed DOI
Uhlig S., Torp M., Heier B.T. Beauvericin and enniatins A, A1, B and B1 in Norwegian grain: A survey. Food Chem. 2006;94:193–201. doi: 10.1016/j.foodchem.2004.11.004. DOI
Chrpová J., Šíp V., Sumíková T., Salava J., Palicová J., Štočková L., Džuman Z., Hajšlová J. Occurrence of Fusarium species and mycotoxins in wheat grain collected in the Czech Republic. World Mycotoxin J. 2016;9:317–327. doi: 10.3920/WMJ2015.1917. DOI
Svingen T., Lund Hansen N., Taxvig C., Vinggaard A.M., Jensen U., Have Rasmussen P. Enniatin B and beauvericin are common in Danish cereals and show high hepatotoxicity on a high-content imaging platform. Environ. Toxicol. 2017;32:1658–1664. doi: 10.1002/tox.22367. PubMed DOI
Abdallah M.F., Girgin G., Baydar T., Krska R., Sulyok M. Occurrence of multiple mycotoxins and other fungal metabolites in animal feed and maize samples from Egypt using LC-MS/MS: Toxic fungal and bacterial metabolites in feed and maize from Egypt. J. Sci. Food Agric. 2017;97:4419–4428. doi: 10.1002/jsfa.8293. PubMed DOI
Bertero A., Fossati P., Tedesco D.E.A., Caloni F. Beauvericin and Enniatins: In Vitro Intestinal Effects. Toxins. 2020;12:686. doi: 10.3390/toxins12110686. PubMed DOI PMC
Orlando B., Grignon G., Vitry C., Kashefifard K., Valade R. Fusarium Species and Enniatin Mycotoxins in Wheat, Durum Wheat, Triticale and Barley Harvested in France. Mycotoxin Res. 2019;35:369–380. doi: 10.1007/s12550-019-00363-x. PubMed DOI
Mortensen A., Granby K., Eriksen F.D., Cederberg T.L., Friis-Wandall S., Simonsen Y., Broesbøl-Jensen B., Bonnichsen R. Levels and Risk Assessment of Chemical Contaminants in Byproducts for Animal Feed in Denmark. J. Environ. Sci. Health Part B. 2014;49:797–810. doi: 10.1080/03601234.2014.938546. PubMed DOI
Mastanjević K., Lukinac J., Jukić M., Šarkanj B., Krstanović V., Mastanjević K. Multi-(Myco)Toxins in Malting and Brewing By-Products. Toxins. 2019;11:30. doi: 10.3390/toxins11010030. PubMed DOI PMC
Arroyo-Manzanares N., Rodríguez-Estévez V., Arenas-Fernández P., García-Campaña A.M., Gámiz-Gracia L. Occurrence of Mycotoxins in Swine Feeding from Spain. Toxins. 2019;11:342. doi: 10.3390/toxins11060342. PubMed DOI PMC
Juan C., Oueslati S., Mañes J., Berrada H. Multimycotoxin Determination in Tunisian Farm Animal Feed. J. Food Sci. 2019;84:3885–3893. doi: 10.1111/1750-3841.14948. PubMed DOI
Novak B., Rainer V., Sulyok M., Haltrich D., Schatzmayr G., Mayer E. Twenty-Eight Fungal Secondary Metabolites Detected in Pig Feed Samples: Their Occurrence, Relevance and Cytotoxic Effects In Vitro. Toxins. 2019;11:537. doi: 10.3390/toxins11090537. PubMed DOI PMC
Shimshoni J.A., Cuneah O., Sulyok M., Krska R., Galon N., Sharir B., Shlosberg A. Mycotoxins in corn and wheat silage in Israel. Food Addit. Contam. Part A. 2013;30:1614–1625. doi: 10.1080/19440049.2013.802840. PubMed DOI
Reisinger N., Schürer-Waldheim S., Mayer E., Debevere S., Antonissen G., Sulyok M., Nagl V. Mycotoxin Occurrence in Maize Silage—A Neglected Risk for Bovine Gut Health? Toxins. 2019;11:577. doi: 10.3390/toxins11100577. PubMed DOI PMC
Zachariasova M., Dzuman Z., Veprikova Z., Hajkova K., Jiru M., Vaclavikova M., Zachariasova A., Pospichalova M., Florian M., Hajslova J. Occurrence of multiple mycotoxins in European feedingstuffs, assessment of dietary intake by farm animals. Anim. Feed Sci. Technol. 2014;193:124–140. doi: 10.1016/j.anifeedsci.2014.02.007. DOI
McElhinney C., Danaher M., Elliott C.T., O’Kiely P. Mycotoxins in farm silages—A 2-year Irish national survey. Grass Forage Sci. 2016;71:339–352. doi: 10.1111/gfs.12191. DOI
Tangni E.K., Pussemier L., Van Hove F. Mycotoxin contaminating maize and grass silages for dairy cattle feeding: Current state and challenges. J. Anim. Sci. Adv. 2013;23:492–511.
Lindblad M., Gidlund A., Sulyok M., Börjesson T., Krska R., Olsen M., Fredlund E. Deoxynivalenol and other selected Fusarium toxins in Swedish wheat—Occurrence and correlation to specific Fusarium species. Int. J. Food Microbiol. 2013;167:284–291. doi: 10.1016/j.ijfoodmicro.2013.07.002. PubMed DOI
Fredlund E., Gidlund A., Sulyok M., Börjesson T., Krska R., Olsen M., Lindblad M. Deoxynivalenol and other selected Fusarium toxins in Swedish oats—Occurrence and correlation to specific Fusarium species. Int. J. Food Microbiol. 2013;167:276–283. doi: 10.1016/j.ijfoodmicro.2013.06.026. PubMed DOI
Debevere S., De Baere S., Haesaert G., Rychlik M., Fievez V., Croubels S. Development of an UPLC-MS/MS Method for the Analysis of Mycotoxins in Rumen Fluid with and without Maize Silage Emphasizes the Importance of Using Matrix-Matched Calibration. Toxins. 2019;11:519. doi: 10.3390/toxins11090519. PubMed DOI PMC
Dagnac T., Latorre A., Lorenzo B.F., Llompart M. Validation and application of a liquid chromatography-tandem mass spectrometry based method for the assessment of the co-occurrence of mycotoxins in maize silages from dairy farms in NW Spain. Food Addit. Contam. Part A. 2016;33:1850–1863. doi: 10.1080/19440049.2016.1243806. PubMed DOI
Panasiuk L., Jedziniak P., Pietruszka K., Piatkowska M., Bocian L. Frequency and Levels of Regulated and Emerging Mycotoxins in Silage in Poland. Mycotoxin Res. 2019;35:17–25. doi: 10.1007/s12550-018-0327-0. PubMed DOI PMC
Storm I., Rasmussen R., Rasmussen P. Occurrence of Pre- and Post-Harvest Mycotoxins and Other Secondary Metabolites in Danish Maize Silage. Toxins. 2014;6:2256–2269. doi: 10.3390/toxins6082256. PubMed DOI PMC
Wambacq E., Vanhoutte I., Audenaert K., De Gelder L., Haesaert G. Occurrence, prevention and remediation of toxigenic fungi and mycotoxins in silage: A review: Fungi and mycotoxins in silage. J. Sci. Food Agric. 2016;96:2284–2302. doi: 10.1002/jsfa.7565. PubMed DOI
Hu L., Koehler P., Rychlik M. Effect of sourdough processing and baking on the content of enniatins and beauvericin in wheat and rye bread. Eur. Food Res. Technol. 2014;238:581–587. doi: 10.1007/s00217-013-2133-4. DOI
Brodal G., Aamot H.U., Almvik M., Hofgaard I.S. Removal of Small Kernels Reduces the Content of Fusarium Mycotoxins in Oat Grain. Toxins. 2020;12:346. doi: 10.3390/toxins12050346. PubMed DOI PMC
Tittlemier S.A., Blagden R., Chan J., McMillan T.L., Pleskach K., Izydorczyk M.S. Effects of Processing Whole Oats on the Analysis and Fate of Mycotoxins and Ergosterol. World Mycotoxin J. 2020;13:45–56. doi: 10.3920/WMJ2019.2530. DOI
Meca G., Ritieni A., Mañes J. Influence of the heat treatment on the degradation of the minor Fusarium mycotoxin beauvericin. Food Control. 2012;28:13–18. doi: 10.1016/j.foodcont.2012.04.016. DOI
Mansfield M.A., Jones A.D., Kuldau G.A. Contamination of Fresh and Ensiled Maize by Multiple Penicillium Mycotoxins. Phytopathology. 2008;98:330–336. doi: 10.1094/PHYTO-98-3-0330. PubMed DOI
Teller R.S., Schmidt R.J., Whitlow L.W., Kung L. Effect of physical damage to ears of corn before harvest and treatment with various additives on the concentration of mycotoxins, silage fermentation, and aerobic stability of corn silage. J. Dairy Sci. 2012;95:1428–1436. doi: 10.3168/jds.2011-4610. PubMed DOI
Gregori R., Meriggi P., Pietri A., Formenti S., Baccarini G., Battilani P. Dynamics of fungi and related mycotoxins during cereal storage in silo bags. Food Control. 2013;30:280–287. doi: 10.1016/j.foodcont.2012.06.033. DOI
Schaafsma A.W., Limay-Rios V., Paul D.E., Miller J.D. Mycotoxins in fuel ethanol co-products derived from maize: A mass balance for deoxynivalenol: DON in maize ethanol co-product. J. Sci. Food Agric. 2009;89:1574–1580. doi: 10.1002/jsfa.3626. DOI
Klosowski G., Blajet-Kosicka A., Mikulski D., Grajewski J. Assessing the Potential of Reducing Mycotoxin Concentration During the Production Process of Ethanol from Maize Grain Using Pls and Classic Technology. Zywnosc Nauka Technol. Jakosc. 2011;18:89–105. doi: 10.15193/zntj/2011/75/089-105. DOI
Yoshinari T., Suzuki Y., Sugita-Konishi Y., Ohnishi T., Terajima J. Occurrence of beauvericin and enniatins in wheat flour and corn grits on the Japanese market, and their co-contamination with type B trichothecene mycotoxins. Food Addit. Contam. Part A. 2016;33:1620–1626. doi: 10.1080/19440049.2016.1228126. PubMed DOI
Malachova A., Dzuman Z., Veprikova Z., Vaclavikova M., Zachariasova M., Hajslova J. Deoxynivalenol, Deoxynivalenol-3-glucoside, and Enniatins: The Major Mycotoxins Found in Cereal-Based Products on the Czech Market. J. Agric. Food Chem. 2011;59:12990–12997. doi: 10.1021/jf203391x. PubMed DOI
Spanic V., Katanic Z., Sulyok M., Krska R., Puskas K., Vida G., Drezner G., Šarkanj B. Multiple Fungal Metabolites Including Mycotoxins in Naturally Infected and Fusarium-Inoculated Wheat Samples. Microorganisms. 2020;8:578. doi: 10.3390/microorganisms8040578. PubMed DOI PMC
Smith M.-C., Madec S., Coton E., Hymery N. Natural Co-Occurrence of Mycotoxins in Foods and Feeds and Their in vitro Combined Toxicological Effects. Toxins. 2016;8:94. doi: 10.3390/toxins8040094. PubMed DOI PMC
Mallebrera B., Prosperini A., Font G., Ruiz M.J. In vitro mechanisms of Beauvericin toxicity: A review. Food Chem. Toxicol. 2018;111:537–545. doi: 10.1016/j.fct.2017.11.019. PubMed DOI
Prosperini A., Berrada H., Ruiz M.J., Caloni F., Coccini T., Spicer L.J., Perego M.C., Lafranconi A. A Review of the Mycotoxin Enniatin B. Front. Public Health. 2017;5:304. doi: 10.3389/fpubh.2017.00304. PubMed DOI PMC
Fernández-Blanco C., Font G., Ruiz M.-J. Interaction effects of enniatin B, deoxinivalenol and alternariol in Caco-2 cells. Toxicol. Lett. 2016;241:38–48. doi: 10.1016/j.toxlet.2015.11.005. PubMed DOI
Tran V., Viktorova J., Augustynkova K., Jelenova N., Dobiasova S., Rehorova K., Fenclova M., Stranska-Zachariasova M., Vitek L., Hajslova J., et al. In Silico and In Vitro Studies of Mycotoxins and Their Cocktails; Their Toxicity and Its Mitigation by Silibinin Pre-Treatment. Toxins. 2020;12:148. doi: 10.3390/toxins12030148. PubMed DOI PMC
Agahi F., Font G., Juan C., Juan-García A. Individual and Combined Effect of Zearalenone Derivates and Beauvericin Mycotoxins on SH-SY5Y Cells. Toxins. 2020;12:212. doi: 10.3390/toxins12040212. PubMed DOI PMC
Alassane-Kpembi I., Schatzmayr G., Taranu I., Marin D., Puel O., Oswald I.P. Mycotoxins co-contamination: Methodological aspects and biological relevance of combined toxicity studies. Crit. Rev. Food Sci. Nutr. 2017;57:3489–3507. doi: 10.1080/10408398.2016.1140632. PubMed DOI
Khoshal A.K., Novak B., Martin P.G.P., Jenkins T., Neves M., Schatzmayr G., Oswald I.P., Pinton P. Co-Occurrence of DON and Emerging Mycotoxins in Worldwide Finished Pig Feed and Their Combined Toxicity in Intestinal Cells. Toxins. 2019;11:727. doi: 10.3390/toxins11120727. PubMed DOI PMC
Kamyar M.R., Kouri K., Rawnduzi P., Studenik C., Lemmens-Gruber R. Effects of moniliformin in presence of cyclohexadepsipeptides on isolated mammalian tissue and cells. Toxicol. In Vitro. 2006;20:1284–1291. doi: 10.1016/j.tiv.2006.03.001. PubMed DOI
EFSA Panel on Contaminants in the Food Chain (CONTAM) Scientific Opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA J. 2014;12:3802. doi: 10.2903/j.efsa.2014.3802. PubMed DOI
Devreese M., Broekaert N., De Mil T., Fraeyman S., De Backer P., Croubels S. Pilot toxicokinetic study and absolute oral bioavailability of the Fusarium mycotoxin enniatin B1 in pigs. Food Chem. Toxicol. 2014;63:161–165. doi: 10.1016/j.fct.2013.11.005. PubMed DOI
Devreese M., De Baere S., De Backer P., Croubels S. Quantitative determination of the Fusarium mycotoxins beauvericin, enniatin A, A1, B and B1 in pig plasma using high performance liquid chromatography-tandem mass spectrometry. Talanta. 2013;106:212–219. doi: 10.1016/j.talanta.2012.11.068. PubMed DOI
Fraeyman S., Devreese M., Antonissen G., De Baere S., Rychlik M., Croubels S. Comparative Oral Bioavailability, Toxicokinetics, and Biotransformation of Enniatin B1 and Enniatin B in Broiler Chickens. J. Agric. Food Chem. 2016;64:7259–7264. doi: 10.1021/acs.jafc.6b02913. PubMed DOI
Devreese M., Girgis G.N., Tran S.-T., De Baere S., De Backer P., Croubels S., Smith T.K. The effects of feed-borne Fusarium mycotoxins and glucomannan in turkey poults based on specific and non-specific parameters. Food Chem. Toxicol. 2014;63:69–75. doi: 10.1016/j.fct.2013.10.044. PubMed DOI
Ivanova L., Uhlig S., Devreese M., Croubels S., Fæste C.K. Biotransformation of the mycotoxin enniatin B1 in pigs: A comparative in vitro and in vivo approach. Food Chem. Toxicol. 2017;105:506–517. doi: 10.1016/j.fct.2017.04.041. PubMed DOI
Ivanova L., Fæste C.K., Van Pamel E., Daeseleire E., Callebaut A., Uhlig S. Presence of enniatin B and its hepatic metabolites in plasma and liver samples from broilers and eggs from laying hens. World Mycotoxin J. 2014;7:167–175. doi: 10.3920/WMJ2013.1609. DOI
Rodríguez-Carrasco Y., Heilos D., Richter L., Süssmuth R.D., Heffeter P., Sulyok M., Kenner L., Berger W., Dornetshuber-Fleiss R. Mouse tissue distribution and persistence of the food-born fusariotoxins Enniatin B and Beauvericin. Toxicol. Lett. 2016;247:35–44. doi: 10.1016/j.toxlet.2016.02.008. PubMed DOI PMC
Manyes L., Escrivá L., Serrano A.B., Rodríguez-Carrasco Y., Tolosa J., Meca G., Font G. A preliminary study in Wistar rats with enniatin A contaminated feed. Toxicol. Mech. Methods. 2014;24:179–190. doi: 10.3109/15376516.2013.876135. PubMed DOI
Debevere S., Cools A., De Baere S., Haesaert G., Rychlik M., Croubels S., Fievez V. In Vitro Rumen Simulations Show a Reduced Disappearance of Deoxynivalenol, Nivalenol and Enniatin B at Conditions of Rumen Acidosis and Lower Microbial Activity. Toxins. 2020;12:101. doi: 10.3390/toxins12020101. PubMed DOI PMC
Roig M., Meca G., Ferrer E., Mañes J. Reduction of the Enniatins A, A1, B, B1 by an in Vitro Degradation Employing Different Strains of Probiotic Bacteria: Identification of Degradation Products by LC–MS–LIT. Toxicon. 2013;70:44–53. doi: 10.1016/j.toxicon.2013.04.001. PubMed DOI
Ferrer E R.M. Degradation of the Bioactive Compounds Enniatins A, A1, B, B1 Employing Different Strains of Bacillus Subtilis. J. Food Process. Technol. 2014;5 doi: 10.4172/2157-7110.1000334. DOI
Meca G., Zhou T., Li X.-Z., Mañes J. Beauvericin Degradation during Bread and Beer Making. Food Control. 2013;34:1–8. doi: 10.1016/j.foodcont.2013.03.032. DOI
Meca G., Ritieni A., Mañes J. Reduction in Vitro of the Minor Fusarium Mycotoxin Beauvericin Employing Different Strains of Probiotic Bacteria. Food Control. 2012;28:435–440. doi: 10.1016/j.foodcont.2012.04.002. DOI
May H.D., Wu Q., Blake C.K. Effects of the Fusarium spp. mycotoxins fusaric acid and deoxynivalenol on the growth of Ruminococcus albus and Methanobrevibacter ruminantium. Can. J. Microbiol. 2000;46:692–699. doi: 10.1139/w00-045. PubMed DOI
Bacon C.W., Hinton D.M., Hinton A. Growth-inhibiting effects of concentrations of fusaric acid on the growth of Bacillus mojavensis and other biocontrol Bacillus species. J. Appl. Microbiol. 2006;100:185–194. doi: 10.1111/j.1365-2672.2005.02770.x. PubMed DOI
Jestoi M. Emerging Fusarium-Mycotoxins Fusaproliferin, Beauvericin, Enniatins, And Moniliformin—A Review. Crit. Rev. Food Sci. Nutr. 2008;48:21–49. doi: 10.1080/10408390601062021. PubMed DOI
Sebastià N., Meca G., Soriano J.M., Mañes J. Antibacterial effects of enniatins J1 and J3 on pathogenic and lactic acid bacteria. Food Chem. Toxicol. 2011;49:2710–2717. doi: 10.1016/j.fct.2011.06.070. PubMed DOI
Arab M., Sohrabvandi S., Mortazavian A.M., Mohammadi R., Tavirani M.R. Reduction of aflatoxin in fermented milks during production and storage. Toxin Rev. 2012;31:44–53. doi: 10.3109/15569543.2012.738350. DOI
Sangsila A., Faucet-Marquis V., Pfohl-Leszkowicz A., Itsaranuwat P. Detoxification of zearalenone by Lactobacillus pentosus strains. Food Control. 2016;62:187–192. doi: 10.1016/j.foodcont.2015.10.031. DOI
Fuchs S., Sontag G., Stidl R., Ehrlich V., Kundi M., Knasmüller S. Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem. Toxicol. 2008;46:1398–1407. doi: 10.1016/j.fct.2007.10.008. PubMed DOI
Ferrer M., Manyes L., Mañes J., Meca G. Influence of prebiotics, probiotics and protein ingredients on mycotoxin bioaccessibility. Food Funct. 2015;6:987–994. doi: 10.1039/C4FO01140F. PubMed DOI
Koivisto P., Jonsson M., Jestoi M., Peltonen K. Enniatin B mycotoxin is excreted as such to rat urine. Toxicol. Lett. 2015;238:S60–S61. doi: 10.1016/j.toxlet.2015.08.218. DOI
Rodríguez-Carrasco Y., Narváez A., Izzo L., Gaspari A., Graziani G., Ritieni A. Biomonitoring of Enniatin B1 and Its Phase I Metabolites in Human Urine: First Large-Scale Study. Toxins. 2020;12:415. doi: 10.3390/toxins12060415. PubMed DOI PMC
Jestoi M., Rokka M., Järvenpää E., Peltonen K. Determination of Fusarium mycotoxins beauvericin and enniatins (A, A1, B, B1) in eggs of laying hens using liquid chromatography-tandem mass spectrometry (LC–MS/MS) Food Chem. 2009;115:1120–1127. doi: 10.1016/j.foodchem.2008.12.105. DOI
Rossi F., Gallo A., Bertuzzi T. Emerging mycotoxins in the food chain. Mediterr. J. Nutr. Metab. 2020;13:7–27. doi: 10.3233/MNM-190345. DOI
Callebaut F., Tangni E.K., Debongnie P., Stals E., Huybrechts B., Waegeneers N., Delezie E., Van Pamel E., Daeseleire E. Carry-Over of Mycotoxins to Animal Products: Case Study Poultry. Centrum voor Onderzoek in Diergeneeskunde en Agrochemie-Centre d’Étude et de Recherches Vétérinaires et Agrochemiques; Brussels, Belgium: 2011–2012. pp. 141–144. Scientific Report 211/212 CODA-CERVA.
Tolosa J., Font G., Mañes J., Ferrer E. Natural Occurrence of Emerging Fusarium Mycotoxins in Feed and Fish from Aquaculture. J. Agric. Food Chem. 2014;62:12462–12470. doi: 10.1021/jf5036838. PubMed DOI
Tolosa J., Font G., Mañes J., Ferrer E. Mitigation of Enniatins in Edible Fish Tissues by Thermal Processes and Identification of Degradation Products. Food Chem. Toxicol. 2017;101:67–74. doi: 10.1016/j.fct.2016.12.039. PubMed DOI
Nácher-Mestre J., Beltrán E., Strachan F., Dick J.R., Pérez-Sánchez J., Berntssen M.H.G., Tocher D.R. No Transfer of the Non-Regulated Mycotoxins, Beauvericin and Enniatins, from Feeds to Farmed Fish Reared on Plant-Based Diets. Food Chem. 2020;323:126773. doi: 10.1016/j.foodchem.2020.126773. PubMed DOI
Piątkowska M., Sulyok M., Pietruszka K., Panasiuk Ł. Pilot study for the presence of fungal metabolites in sheep milk from first spring milking. J. Vet. Res. 2018;62:167–172. doi: 10.2478/jvetres-2018-0026. PubMed DOI PMC
Rubert J., León N., Sáez C., Martins C.P.B., Godula M., Yusà V., Mañes J., Soriano J.M., Soler C. Evaluation of mycotoxins and their metabolites in human breast milk using liquid chromatography coupled to high resolution mass spectrometry. Anal. Chim. Acta. 2014;820:39–46. doi: 10.1016/j.aca.2014.02.009. PubMed DOI
Braun D., Ezekiel C.N., Abia W.A., Wisgrill L., Degen G.H., Turner P.C., Marko D., Warth B. Monitoring Early Life Mycotoxin Exposures via LC-MS/MS Breast Milk Analysis. Anal. Chem. 2018;90:14569–14577. doi: 10.1021/acs.analchem.8b04576. PubMed DOI
Braun D., Ezekiel C.N., Marko D., Warth B. Exposure to Mycotoxin-Mixtures via Breast Milk: An Ultra-Sensitive LC-MS/MS Biomonitoring Approach. Front. Chem. 2020;8:423. doi: 10.3389/fchem.2020.00423. PubMed DOI PMC