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Articles

Mixtures of mycotoxins, phytoestrogens and pesticides co-occurring in wet spent brewery grains (BSG) intended for dairy cattle feeding in Austria

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Pages 1855-1877 | Received 15 Jun 2022, Accepted 28 Aug 2022, Published online: 21 Sep 2022

References

  • Aichinger G, Del Favero G, Warth B, Marko D. 2021. Alternaria toxins—Still emerging? Compr Rev Food Sci Food Saf. 20(5):4390–4406. doi:10.1111/1541-4337.12803
  • Aichinger G, Krüger F, Puntscher H, Preindl K, Warth B, Marko D. 2019. Naturally occurring mixtures of Alternaria toxins: anti-estrogenic and genotoxic effects in vitro. Arch Toxicol. 93(10):3021–3031. doi:10.1007/s00204-019-02545-z
  • Almeida MC, Resende DI, da Costa PM, Pinto M, Sousa E. 2021. Fumiquinazoline related alkaloids: synthesis and evaluation of their antibacterial activities. Proceedings of the 7th International Electronic Conference on Medicinal Chemistry; 2021 November 1–30; Basel, Switzerland: MDPI. doi:10.3390/ECMC2021-11474
  • Alonso VA, Pereyra CM, Keller LAM, Dalcero AM, Rosa CAR, Chiacchiera SM, Cavaglieri LR. 2013. Fungi and mycotoxins in silage: an overview. J Appl Microbiol. 115(3):637–643. doi:10.1111/jam.12178
  • Ambra R, Pastore G, Lucchetti S. 2021. The role of bioactive phenolic compounds on the impact of beer on health. Molecules. 26(2):486. doi:10.3390/molecules26020486
  • Andersen B, Krøger E, Roberts RG. 2002. Chemical and morphological segregation of Alternaria arborescens, A. infectoria and A. tenuissima species-groups. Mycol Res. 106(2):170–182. doi:10.1017/S0953756201005263
  • Ariza MR, Larsen TO, Peterson BO, Duus JO, Barrero AF. 2002. Penicillium digitatum metabolites on synthetic media and citrus fruits. J Agric Food Chem. 50(22):6361–6365. doi:10.1021/jf020398d
  • Awapak D, Petchkongkaew A, Sulyok M, Krska R. 2021. Co-occurrence and toxicological relevance of secondary metabolites in dairy cow feed from Thailand. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 38(6):1013–1027. doi:10.1080/19440049.2021.1905186
  • Bacon C, Porter J, Norred W, Leslie J. 1996. Production of fusaric acid by Fusarium species. Appl Environ Microbiol. 62(11):4039–4043. doi:10.1128/aem.62.11.4039-4043.1996
  • Bai G, Shaner G. 2004. Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol. 42:135–161. doi:10.1146/annurev.phyto.42.040803.140340
  • Barnett EA, Charlton AJ, Fletcher MR. 2007. Incidents of bee poisoning with pesticides in the United Kingdom, 1994–2003. Pest Manag Sci. 63(11):1051–1057. doi:10.1002/ps.1444
  • Basak M, Ahmed Choudhury R, Goswami P, Kumar Dey B, Ahmed Laskar M. 2021. A review on non-target toxicity of deltamethrin and piperonyl butoxide: aynergist. J Pharm Res Int. 33(51B):85–89.
  • Battilani P, Palumbo R, Giorni P, Dall’Asta C, Dellafiora L, Gkrillas A, Toscano P, Crisci A, Brera C, De Santis B. 2020. Mycotoxin mixtures in food and feed: holistic, innovative, flexible risk assessment modelling approach: MYCHIF. EFSA Support. 17:1757E.
  • Bauer JI, Gross M, Gottschalk C, Usleber E. 2016. Investigations on the occurrence of mycotoxins in beer. Food Control. 63:135–139. doi:10.1016/j.foodcont.2015.11.040
  • Becher R, Miedaner T, Wirsel SGR. 2013. Biology, diversity and management of FHB-causing Fusarium species in small-grain cereals. In: Seiten, Kempken F, editor. The mycota. XI. Agricultural applications. 2nd ed. Berlin, Germany: Springer-Verlag; p. 199–241.
  • Becker JO, Loffredo A, Edwards S, Becker Smith J, Ploeg A. 2020. Seed-delivered fluopyram mitigates root-knot nematode damage in fresh market carrot field trials. Poster session presented at: virtual SON 2020. [accessed 2022 June 11]. doi:10.6084/m9.figshare.13356596.v1.
  • Bianco A, Budroni M, Zara S, Mannazzu I, Fancello F, Zara G. 2020. The role of microorganisms on biotransformation of brewers’ spent grain. Appl Microbiol Biotechnol. 104(20):8661–8678. doi:10.1007/s00253-020-10843-1
  • Bocquier F, González-García E. 2010. Sustainability of ruminant agriculture in the new context: feeding strategies and features of animal adaptability into the necessary holistic approach. Animal. 4(7):1258–1273. doi:10.1017/S1751731110001023
  • Bottalico A, Perrone G. 2002. Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol. 108(7):611–624. doi:10.1023/A:1020635214971
  • Brennan KM, Oh SY, Yiannikouris A, Graugnard DE, Karrow NA. 2017. Differential gene expression analysis of bovine macrophages after exposure to the Penicillium mycotoxins citrinin and/or ochratoxin A. Toxins. 9(11):366. doi:10.3390/toxins9110366
  • Chan J, Jamison TF. 2003. Synthesis of (−)-terpestacin via catalytic, stereoselective fragment coupling: Siccanol is terpestacin, not 11-epi-terpestacin. J Am Chem Soc. 125(38):11514–11515. doi:10.1021/ja0373925
  • Chanie D, FieVez V. 2017. Review on preservation and utilization of wet brewery spent grain as concentrate replacement feed for lactating dairy cows. J Anim Health Prod. 5(1):10–13.
  • Cinar A, Onbaşı E. 2019. Mycotoxins: the hidden danger in foods. In: Sabuncuoğlu S, editor. Mycotoxins and food safety. London: IntechOpen; p. 2020.
  • Clardy J, Springer JP, Buchi G, Matsuo K, Wightman R. 1975. Tryptoquivaline and tryptoquivalone, two tremorgenic metabolites of Aspergillus clavatus. J Am Chem Soc. 97(3):663–665. doi:10.1021/ja00836a045
  • Connolly L. 2009. Endocrine-disrupting chemicals: origins, fates and transmission into the food chain. In: Shaw I, editor. Endocrine disrupting chemicals in food. Cambridge: Woodhead Publishing Limited; p. 103–125.
  • Conrad HR, Rogers JA. 1977. Comparative value of brewers’ wet and brewers’ dried grains for dairy cattle. St. Louis (MO): US Brewers Association Feed Conference; p. 26–33.
  • Cope RB. 2018. Trichothecenes. In: Gupta RC, editor. Veterinary toxicology. 3rd ed. Cambridge (MA): Academic Press; p. 1043–1053.
  • Coufal-Majewski S, Stanford K, McAllister T, Blakley B, McKinnon J, Chaves AV, Wang Y. 2016. Impacts of cereal ergot in food animal production. Front Vet Sci. 25(3):15.
  • Cozma P, Apostol LC, Hlihor RM, Simion IM, Gavrilescu M. 2017. Overview of human health hazards posed by pesticides in plant products. Proceedings of 2017 E-Health and Bioengineering Conference (EHB). Sinaia, Romania; June 22–24; Piscataway (NJ): IEEE. doi:10.1109/EHB.2017.7995419
  • D’Mello JPF, Placinta CM, Macdonald AMC. 1999. Fusarium mycotoxins: a review of global implications for animal health, welfare, and productivity. Anim Feed Sci Technol. 80(3–4):183–205. doi:10.1016/S0377-8401(99)00059-0
  • Damalas CA, Eleftherohorinos IG. 2011. Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res. 8(5):1402–1419.
  • Deshpande S. 2002. Handbook of food toxicology. NY, USA: CRC Press.
  • Dong X, Fu J, Yin X, Cao S, Li X, Lin L, Ni J. 2016. Emodin: a review of its pharmacology, toxicity and pharmacokinetics. Phytother Res. 30(8):1207–1218. doi:10.1002/ptr.5631
  • Dreinert A, Wolf A, Mentzel T, Meunier B, Fehr M. 2018. The cytochrome bc1 complex inhibitor Ametoctradin has an unusual binding mode. Biochim Biophys Acta Bioenerg. 1859(8):567–576. doi:10.1016/j.bbabio.2018.04.008. 29704498
  • Dzidic A, Prgomet C, Mohr A, Meyer K, Bauer J, Meyer HHD, Pfaffl MW. 2006. Effects of mycophenolic acid on inosine monophosphate dehydrogenase I and II mRNA expression in white blood cells and various tissues in sheep. J Vet Med Series A. 53(4):163–169. doi:10.1111/j.1439-0442.2006.00809.x
  • [EC] European Commission. 2002. Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed. O J Eu L. 140:10–21.
  • [EC] European Commission. 2005. Commission regulation (EC). 2005. No 396/2005 of the European parliament and of the council, maximum residue levels of pesticides in or on food and feed of plant and animal origin. O J Eu L. 70:1–16.
  • [EC] European Commission. 2006. Commission recommendation of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding (2006/576/EC). O J Eu L. 229:7–9.
  • [EC] European Commission. 2012. Commission recommendation 2012/154/EU of 15 March 2012 on the monitoring of the presence of ergot alkaloids in feed and food. O J Eu L. 77:20–21.
  • [EC] European Commission. 2013. Commission recommendation of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products (2013/165/EU). O J Eu L. 91:12–15.
  • Edwards S, Barrier-Guillot B, Clasen PE, Hietaniemi V, Pettersson H. 2009. Emerging issues of HT-2 and T-2 toxins in European cereal production. WMJ. 2(2):173–179. doi:10.3920/WMJ2008.1126
  • [EFSA] European Food Safety Authority, Anastassiadou M, Bernasconi G, Brancato A, Carrasco Cabrera L, Greco L, Jarrah S, Kazocina A, Leuschner R, Magrans JO. 2020. Review of the existing maximum residue levels for fluopyram according to Article 12 of Regulation (EC) No 396/2005. EFSA J. 18(4):6059. [accessed 2022 June 11]. doi:10.2903/j.efsa.2020.6059.
  • [EFSA] European Food Safety Authority, Arena M, Auteri D, Barmaz S, Bellisai G, Brancato A, Brocca D, Bura L, Byers H, Chiusolo A. 2017. Peer review of the pesticide risk assessment of the active substance trifloxystrobin. EFSA J. 15(10):4989.
  • [EFSA] European Food Safety Authority, Brancato A, Brocca DLC, Cabrera C, De Lentdecker L, Ferreira L, Greco J, Janossy S, Jarrah D, Kardassi R, Leuschner C. 2018. Modification of the existing maximum residue levels for prochloraz in various commodities. EFSA J. 16(4):5241.
  • [EFSA] European Food Safety Authority. 2011. Scientific opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food. EFSA J. 9(10):1–97.
  • [EFSA] European Food Safety Authority. 2012. Scientific Opinion on Ergot alkaloids in food and feed. EFSA J. 10(7):2798.
  • [EFSA] European Food Safety Authority. 2014. Scientific opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA J. 12(8):1–174.
  • Ertl P, Zebeli Q, Zollitsch W, Knaus W. 2015. Feeding of by-products completely replaced cereals and pulses in dairy cows and enhanced edible feed conversion ratio. J Dairy Sci. 98(2):1225–1233. doi:10.3168/jds.2014-8810
  • Escrivá L, Oueslati S, Font G, Manyes L. 2017. Alternaria mycotoxins in food and feed: An overview. J. Food Qual. 2017:1–20. doi:10.1155/2017/1569748
  • [EU] European Union. 2021. Commission Regulation (EU) 2021/1399 of 24 August 2021 amending Regulation (EC) No 1881/2006 as regards maximum levels of ergot sclerotia and ergot alkaloids in certain foodstuffs. Off J European Union. 301:1–5.
  • [EU-MRL-Database]. 2022. European union maximum residue limit; [accessed 2022 June 11]. https://ec.europa.eu/food/plants/pesticides/eu-pesticides-database_en.
  • Evans TJ. 2011. Diminished reproductive performance and selected toxicants in forages and grains. Vet Clin North Am Food Anim Pract. 27(2):345–371. doi:10.1016/j.cvfa.2011.03.001
  • Eze UA, Huntriss J, Routledge MN, Gong YY, Connolly L. 2019. The effect of individual and mixtures of mycotoxins and persistent organochloride pesticides on oestrogen receptor transcriptional activation using in vitro reporter gene assays. Food Chem Toxicol. 130:68–78. doi:10.1016/j.fct.2019.05.014
  • [FAO and WHO] Food and Agriculture Organization of the United Nations and World Health Organization. 2019. Hazards Associated with Animal Feed: Joint FAO/WHO Expert Meeting FAO Headquarters; Rome, Italy; 12–15 May 2015. FAO animal production and health/report No. 14. Geneva, Switzerland: World Health Organization. [accessed 2022 June 11]. https://www.fao.org/3/ca6825en/CA6825EN.pdf.
  • Fink-Gremmels J. 2005. Mycotoxins in forages. In: Diaz DE, editor. The mycotoxin blue book. Nottingham: Nottingham University Press; p. 249–268.
  • Fink-Gremmels J. 2008. The role of mycotoxins in the health and performance of dairy cows. Vet J. 176(1):84–92. doi:10.1016/j.tvjl.2007.12.034
  • Gallo A, Ghilardelli F, Atzori AS, Zara S, Novak B, Faas J, Fancello F. 2021. Co-occurrence of regulated and emerging mycotoxins in corn silage: relationships with fermentation quality and bacterial communities. Toxins. 13(3):232. doi:10.3390/toxins13030232
  • Gallo A, Giuberti G, Frisvad JC, Bertuzzi T, Nielsen KF. 2015. Review on mycotoxin issues in ruminants: occurrence in forages, effects of mycotoxin ingestion on health status and animal performance and practical strategies to counteract their negative effects. Toxins. 7(8):3057–3111. doi:10.3390/toxins7083057
  • Geissen V, Silva V, Lwanga EH, Beriot N, Oostindie K, Bin Z, Pyne E, Busink S, Zomer P, Mol H, et al. 2021. Cocktails of pesticide residues in conventional and organic farming systems in Europe–Legacy of the past and turning point for the future. Environ Pollut. 278:116827. doi:10.1016/j.envpol.2021.116827
  • Gil-Serna J, Vázquez C, Gonzaléz-Jaén MT, Patiño B. 2014. Mycotoxins: Toxicology. In: Batt C, Tortorello ML, editors. Encyclopedia of Food Microbiology. 2nd ed. St. Louis, MO, USA: Elsevier. p. 887–892.
  • Gonzalez Pereyra M, Rosa C, Dalcero A, Cavaglieri L. 2011. Mycobiota and mycotoxins in malted barley and brewer’s spent grain from Argentinean breweries. Lett Appl Microbiol. 53(6):649–655. doi:10.1111/j.1472-765X.2011.03157.x
  • Grenier B, Oswald I. 2011. Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. World Mycotoxin J. 4(3):285–313. doi:10.3920/WMJ2011.1281
  • Grgic D, Varga E, Novak B, Müller A, Marko D. 2021. Isoflavones in animals: metabolism and effects in livestock and occurrence in feed. Toxins. 13(12):836. doi:10.3390/toxins13120836
  • Groten JP, Feron VJ, Sühnel J. 2001. Toxicology of simple and complex mixtures. Trends Pharmacol Sci. 22(6):316–322. doi:10.1016/s0165-6147(00)01720-x
  • Guo H, Ji J, Wang J-S, Sun X. 2020. Co-contamination and interaction of fungal toxins and other environmental toxins. Trends Food Sci Technol. 103:162–178. doi:10.1016/j.tifs.2020.06.021
  • Gupta RC, Evans TJ, Nicholson SS. 2018. Ergot and fescue toxicoses. In: Gupta RC, editor. Veterinary toxicology. Amsterdam, The Netherlands: Elsevier; p. 995–1001.
  • Hajnal EJ, Kos J, Malachová A, Steiner D, Stranska M, Krska R, Sulyok M. 2020. Mycotoxins in maize harvested in Serbia in the period 2012–2015. Part 2: non-regulated mycotoxins and other fungal metabolites. Food Chem. 317:126409. doi:10.1016/j.foodchem.2020.126409
  • Harp T, Godwin J, Scalliet G, Walter H, Stalker A, Bartlett D, Ranner D. 2011. Isopyrazam, a new generation cereal fungicide. Asp Appl Biol. 106:113–120.
  • Hessenberger S, Botzi K, Degrassi C, Kovalsky P, Schwab C, Schatzmayr D, Schatzmayr G, Fink-Gremmels J. 2017. Interactions between plant-derived oestrogenic substances and the mycoestrogen zearalenone in a bioassay with MCF-7 cells. Pol J Vet Sci. 20(3):513–520. doi:10.1515/pjvs-2017-0062
  • Huang F, Subramanyam B. 2005. Management of five stored-product insects in wheat with pirimiphos-methyl and pirimiphos-methyl plus synergized pyrethrins. Pest Manag Sci. 61(4):356–362. doi:10.1002/ps.968
  • Hussein HS, Brasel JM. 2001. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology. 167(2):101–134. doi:10.1016/s0300-483x(01)00471-1
  • Igbedioh S. 1991. Effects of agricultural pesticides on humans, animals, and higher plants in developing countries. Arch Environ Health. 46(4):218–224. doi:10.1080/00039896.1991.9937452
  • Inoue T, Nagatomi Y, Suga K, Uyama A, Mochizuki N. 2011. Fate of pesticides during beer brewing. J Agric Food Chem. 59(8):3857–3868. doi:10.1021/jf104421q
  • José C, Prinsen P, Gutiérrez A. 2013. Chemical composition of lipids in brewer’s spent grain: a promising source of valuable phytochemicals. J Cereal Sci. 58(2):248–254. doi:10.1016/j.jcs.2013.07.001
  • Juan C, Oueslati S, Manes J, Berrada H. 2019. Multimycotoxin determination in tunisian farm animal feed. J Food Sci. 84(12):3885–3893. doi:10.1111/1750-3841.14948
  • Kamboh AA. 2017. Review on preservation and utilization of wet brewery spent grain as concentrate replacement feed for lactating dairy cows. J Anim Health Prod. 5(1):10–13.
  • Kanungo M, Joshi J. 2014. Impact of pyraclostrobin (F-500) on crop plants. Plant Sci Today. 1(3):174–178. doi:10.14719/pst.2014.1.3.60
  • Keane P. 1999. The use of piperonyl butoxide in formulations for the control of pests of humans, domestic pets, and food animals. In: Jones DG, editor. Piperonyl butoxide. The insect synergist. London: Academic Press; p. 289–300.
  • Kemboi DC, Ochieng PE, Antonissen G, Croubels S, Scippo M-L, Okoth S, Kangethe EK, Faas J, Doupovec B, Lindahl JF, et al. 2020. Multi-mycotoxin occurrence in dairy cattle and poultry feeds and feed ingredients from Machakos Town, Kenya. Toxins. 12(12):762. doi:10.3390/toxins12120762
  • Kindbom S. 2012. Ensiling wet brewer’s waste in peri-urban areas of Kampala. Uganda: Degree project/Swedish University of Agricultural Sciences, Department of Animal Nutrition and Management.
  • Kiyoshi K, Taketoshi K, Hideki M, Jiro K, Yoshinori N. 1984. A comparative study on cytotoxicities and biochemical properties of anthraquinone mycotoxins emodin and skyrin from Penicillium islandicum Sopp. Toxicol Lett. 20(2):155–160. doi:10.1016/0378-4274(84)90141-3
  • Kong Z, Li M, Chen J, Gui Y, Bao Y, Fan B, Jian Q, Francis F, Dai X. 2016. Behavior of field-applied triadimefon, malathion, dichlorvos, and their main metabolites during barley storage and beer processing. Food Chem. 211:679–686. doi:10.1016/j.foodchem.2016.05.058
  • Kovač M, Bulaić M, Jakovljević J, Nevistić A, Rot T, Kovač T, Dodlek Šarkanj I, Šarkanj B. 2021. Mycotoxins, pesticide residues, and heavy metals analysis of Croatian cereals. Microorganisms. 9(2):216. doi:10.3390/microorganisms9020216
  • Křížová L, Dadáková K, Dvořáčková M, Kašparovský T. 2021. Feedborne mycotoxins beauvericin and enniatins and livestock animals. Toxins. 13(1):32. doi:10.3390/toxins13010032
  • Lake BG, Price RJ, Scott MP, Chatham LR, Vardy A, Osimitz TG. 2020. Piperonyl butoxide: mode of action analysis for mouse liver tumour formation and human relevance. Toxicology. 439:152465. doi:10.1016/j.tox.2020.152465
  • Lamberth C, Jeanguenat A, Cederbaum F, De Mesmaeker A, Zeller M, Kempf H-J, Zeun R. 2008. Multicomponent reactions in fungicide research: the discovery of mandipropamid. Bioorg Med Chem. 16(3):1531–1545. doi:10.1016/j.bmc.2007.10.019
  • Lao EJ, Dimoso N, Raymond J, Mbega ER. 2020. The prebiotic potential of brewers’ spent grain on livestock’s health: a review. Trop Anim Health Prod. 52(2):461–472. doi:10.1007/s11250-019-02120-9
  • Larsen TO, Perry NB, Andersen B. 2003. Infectopyrone, a potential mycotoxin from Alternaria infectoria. Tetrahedron Lett. 44(24):4511–4513. doi:10.1016/S0040-4039(03)01018-9
  • Laupacis A, Keown P, Ulan R, McKenzie N, Stiller C. 1982. Cyclosporin A: a powerful immunosuppressant. Can Med Assoc J. 126(9):1041–1046.
  • Lazzari V, Arcangeli G, Boebel A, Gualco A, Lazzati S, Risi C, Cantoni A. 2012. Bixafen: a new fungicide active substance effective against foliar diseases of wheat and barley. Proceedings in Giornate Fitopatologiche 2012Milano; Marittima (RA); Marz 13–16; Bologna, Italy: Università di Bologna; p. 213–218.
  • Liggins J, Mulligan A, Runswick S, Bingham S. 2002. Daidzein and genistein content of cereals. Eur J Clin Nutr. 56(10):961–966. doi:10.1038/sj.ejcn.1601419
  • Lilly V, Birch M, Garscadden B. 1980. The preservation of spent brewers’ grains by the application of intermediate moisture food technology. J Sci Food Agric. 31(10):1059–1065. doi:10.1002/jsfa.2740311014
  • Lindell AE, Zimmermann-Kogadeeva M, Patil KR. 2022. Multimodal interactions of drugs, natural compounds, and pollutants with the gut microbiota. Nat Rev Microbiol. 20(7):431–443. doi:10.1038/s41579-022-00681-5
  • Lunn D. 2010. Fluopyram (243) the first draft was prepared by Mr David Lunn. Wellington, New Zealand: New Zealand Food Safety Authority; p. 1415. https://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/JMPR/Evaluation12/Fluopyram.pdf.
  • Lynch KM, Steffen EJ, Arendt EK. 2016. Brewers’ spent grain: a review with an emphasis on food and health. J Inst Brew. 122(4):553–568. doi:10.1002/jib.363
  • Malachova A, Cerkal R, Ehrenbergerova J, Dzuman Z, Vaculova K, Hajslova J. 2010. Fusarium mycotoxins in various barley cultivars and their transfer into malt. J Sci Food Agric. 90(14):2495–2505. doi:10.1002/jsfa.4112
  • Manni K, Rämö S, Franco M, Rinne M, Huuskonen A. 2022. Occurrence of mycotoxins in grass and whole-crop cereal silages—a farm survey. Agriculture. 12(3):398. doi:10.3390/agriculture12030398
  • Marczuk J, Obremski K, Lutnicki K, Gajecka M, Gajecki M. 2012. Zearalenone and deoxynivalenol mycotoxicosis in dairy cattle herds. Pol J Vet Sci. 15(2):365–372. doi:10.2478/v10181-012-0055-x
  • Martin O, Scholze M, Ermler S, McPhie J, Bopp SK, Kienzler A, Parissis N, Kortenkamp A. 2021. Ten years of research on synergisms and antagonisms in chemical mixtures: a systematic review and quantitative reappraisal of mixture studies. Environ Int. 146:106206. doi:10.1016/j.envint.2020.106206
  • Mattsson JL. 2007. Mixtures in the real world: the importance of plant self-defense toxicants, mycotoxins, and the human diet. Toxicol Appl Pharmacol. 223(2):125–132. doi:10.1016/j.taap.2006.12.024
  • McLean MS, Hollaway GJ. 2019. Control of net form of net blotch in barley from seed-and foliar-applied fungicides. Crop Pasture Sci. 70(1):55–60. doi:10.1071/CP18142
  • Miethbauer S, Gaube F, Möllmann U, Dahse HM, Schmidtke M, Gareis M, Pickhardt M, Liebermann B. 2009. Antimicrobial, antiproliferative, cytotoxic, and tau inhibitory activity of rubellins and caeruleoramularin produced by the phytopathogenic fungus Ramularia collo-cygni. Planta Med. 75(14):1523–1525. doi:10.1055/s-0029-1185835
  • Mishra P, Sharma A, Sharma D. 2014. A study on harmful effects of pesticide residue in vegetables. Int J Recent Res Rev. 7(1):45–48.
  • Mussatto SI. 2014. Brewer’s spent grain: a valuable feedstock for industrial applications. J Sci Food Agric. 94(7):1264–1275. doi:10.1002/jsfa.6486
  • Navarro S, Perez G, Navarro G, Vela N. 2007. Decline of pesticide residues from barley to malt. Food Addit Contam. 24(8):851–859. doi:10.1080/02652030701245189
  • Nesic K, Ivanovic S, Nesic V. 2014. Fusarial toxins: secondary metabolites of Fusarium fungi. Rev Environ Contam Toxicol. 228:101–120. doi:10.1007/978-3-319-01619-1_5
  • Nichea MJ, Palacios SA, Chiacchiera SM, Sulyok M, Krska R, Chulze SN, Torres AM, Ramirez ML. 2015. Presence of multiple mycotoxins and other fungal metabolites in native grasses from a wetland ecosystem in Argentina intended for grazing cattle. Toxins 7(8):3309–3329. doi:10.3390/toxins7083309
  • Nielsen KF, Sumarah MW, Frisvad JC, Miller JD. 2006. Production of metabolites from the Penicillium roqueforti complex. J Agric Food Chem. 54(10):3756–3763. doi:10.1021/jf060114f
  • O’Brien M, Nielsen KF, O’Kiely P, Forristal PD, Fuller HT, Frisvad JC. 2006. Mycotoxins and other secondary metabolites produced in vitro by Penicillium paneum Frisvad and Penicillium roqueforti Thom isolated from baled grass silage in Ireland. J Agric Food Chem. 54(24):9268–9276. doi:10.1021/jf0621018
  • Oh SY, Fisher RE, Swamy HVLN, Boermans HJ, Yiannikouris A, Karrow NA. 2015. Silage Penicillium mycotoxins: hidden modulators of the immune system. In: Rios C, editor. Mycotoxins: occurrence, toxicology and management strategies. New York (NY): Nova Science Publishers Inc.; p. 1–40.
  • Oh SY, Boermans HJ, Swamy HVLN, Sharma BS, Karrow NA. 2012. Immunotoxicity of Penicillium mycotoxins on viability and proliferation of bovine macrophage cell line (BOMACs). TOMYCJ. 6(1):11–16. doi:10.2174/1874437001206010011
  • Opalski KS, Tresch S, Kogel KH, Grossmann K, Köhle H, Hückelhoven R. 2006. Metrafenone: studies on the mode of action of a novel cereal powdery mildew fungicide. Pest Manag Sci. 62(5):393–401. doi:10.1002/ps.1176
  • Pack ED, Meyerhoff K, Schmale DG. III 2021. Tracking zearalenone and type-b trichothecene mycotoxins in the commercial production of beer and brewers’ spent grains. J Am Soc Brew Chem. 80(2):180–189. doi:10.1080/03610470.2021.1938489
  • Palladino C, Puigvert F, Muela A, Taborda B, Pérez CA, Pérez-Parada A, Pareja L. 2021. Evaluation of Fusarium mycotoxins and fungicide residues in barley grain produced in Uruguay. J Agric Food Res. 3:100092. doi:10.1016/j.jafr.2020.100092
  • Palmer GH. 2018. Barley and malt. In: Stewart GG, Anstruther A, Russell I, editors. Handbook of brewing. 3rd ed. Boca Raton (FL): CRC Press; p. 107–128.
  • [PAN] Pesticide Action Network. 2021. PAN international list of highly hazardous pesticides (PAN List of HHPs). [accessed 2022 June 11]. https://pan-international.org/wp-content/uploads/PAN_HHP_List.pdf.
  • Panico SC, van Gestel CA, Verweij RA, Rault M, Bertrand C, Barriga CAM, Coeurdassier M, Fritsch C, Gimbert F, Pelosi C. 2022. Field mixtures of currently used pesticides in agricultural soil pose a risk to soil invertebrates. Environ Pollut. 305:119290. doi:10.1016/j.envpol.2022.119290
  • Park SH, Stierle A, Strobel GA. 1993. Metabolism of maculosin, a host-specific phytotoxin produced by Alternaria alternata on spotted knapweed (Centaurea maculosa). Phytochemistry. 35(1):101–106. doi:10.1016/S0031-9422(00)90516-8
  • Pascari X, Ramos AJ, Marín S, Sanchís V. 2018. Mycotoxins and beer. Impact of beer production process on mycotoxin contamination. A review. Food Res Int. 103:121–129. doi:10.1016/j.foodres.2017.07.038
  • Paudel B, Maharjan R, Rajbhandari P, Aryal N, Aziz S, Bhattarai K, Baral B, Malla R, Bhattarai HD. 2021. Maculosin, a non-toxic antioxidant compound isolated from Streptomyces sp. KTM18. Pharm Biol. 59(1):933–936.
  • Penagos-Tabares F, Khiaosa-Ard R, Schmidt M, Pacífico C, Faas J, Jenkins T, Nagl V, Sulyok M, Labuda R, Zebeli Q. 2022. Fungal species and mycotoxins in mouldy spots of grass and maize silages in Austria. Mycotoxin Res. 38(2):117–136. doi:10.1007/s12550-022-00453-3
  • Penagos-Tabares FK, Khiaosa-Ard R, Nagl V, Faas J, Jenkins T, Sulyok M, Zebeli Q. 2021. Mycotoxins, phytoestrogens, and other secondary metabolites in Austrian pastures: occurrences, contamination levels, and implications of geo-climatic factors. Toxins. 13(7):460. doi:10.3390/toxins13070460
  • Pereyra ML, Rosa CAR, Dalcero AM, Cavaglieri LR. 2011. Mycobiota and mycotoxins in malted barley and brewer’s spent grain from Argentinean breweries. Lett Appl Microbiol. 53(6):649–655. doi:10.1111/j.1472-765X.2011.03157.x
  • Petit G, Korbel E, Jury V, Aider M, Rousselière S, Audebrand LK, Turgeon SL, Mikhaylin S. 2020. Environmental evaluation of new brewer’s spent grain preservation pathways for further valorization in human nutrition. ACS Sustainable Chem Eng. 8(47):17335–17344. doi:10.1021/acssuschemeng.0c04236
  • Piacentini KC, Běláková S, Benešová K, Pernica M, Savi GD, Rocha LO, Hartman I, Čáslavský J, Corrêa B. 2019. Fusarium mycotoxins stability during the malting and brewing processes. Toxins. 11(5):257. doi:10.3390/toxins11050257
  • Pires NA, Gonçalves De Oliveira ML, Gonçalves JA, Faria AF. 2021. Multiclass analytical method for pesticide and mycotoxin analysis in malt, brewers’ spent grain, and beer: development, validation, and application. J Agric Food Chem. 69(15):4533–4541. doi:10.1021/acs.jafc.0c07004
  • Qian SY, Yang CL, Khan A, Chen RX, Wu MS, Tuo L, Wang Q, Liu JG, Cheng GG. 2019. New pyrazinoquinazoline alkaloids Isolated from a culture of Stenotrophomonas maltophilia QB-77. Nat Prod Res. 33(9):1387–1391. doi:10.1080/14786419.2018.1475381
  • Rahman A, Siddiqui SA, Rahman MO, Kang SC. 2020. Cyclo (L-Pro-L-Tyr) from Streptomyces sp. 150: exploiting in vitro potential in controlling foodborne pathogens and phytopathogens. Anti-Infect Agents. 18(2):169–177. doi:10.2174/2211352517666190716155147
  • Rathod PH, Shah PG, Parmar KD, Kalasariya RL. 2022. The fate of fluopyram in the soil–water–plant ecosystem: a review. Rev Environ Contam Toxicol. 260(1):1–19.
  • Reed KFM. 2016. Fertility of herbivores consuming phytoestrogen-containing Medicago and Trifolium species. Agriculture. 6(3):35. doi:10.3390/agriculture6030035
  • Reisinger N, Schurer-Waldheim S, Mayer E, Debevere S, Antonissen G, Sulyok M, Nagl V. 2019. Mycotoxin occurrence in maize silage-a neglected risk for bovine gut health? Toxins. 11(10):577. doi:10.3390/toxins11100577
  • Rivera-Becerril F, van Tuinen D, Chatagnier O, Rouard N, Béguet J, Kuszala C, Soulas G, Gianinazzi-Pearson V, Martin-Laurent F. 2017. Impact of a pesticide cocktail (fenhexamid, folpel, deltamethrin) on the abundance of Glomeromycota in two agricultural soils. Sci Total Environ. 577:84–93. doi:10.1016/j.scitotenv.2016.10.098
  • Rizzati V, Briand O, Guillou H, Gamet-Payrastre L. 2016. Effects of pesticide mixtures in human and animal models: an update of the recent literature. Chem Biol Interact. 254:231–246. doi:10.1016/j.cbi.2016.06.003
  • Rodrigues ET, Lopes I, Pardal MÂ. 2013. Occurrence, fate and effects of azoxystrobin in aquatic ecosystems: a review. Environ Int. 53:18–28. doi:10.1016/j.envint.2012.12.005
  • Romero CM, Castellanos MRT, Mendoza RM, Reyes RA, García AR. 1997. Oestrogenic syndrome in dairy cows by alfalfa consumption with large amount of coumestrol. Vet Mex. 28(1):25–30.
  • Rumbos CI, Dutton AC, Athanassiou CG. 2016. Insecticidal efficacy of two pirimiphos-methyl formulations for the control of three stored-product beetle species: effect of commodity. Crop Prot. 80:94–100. doi:10.1016/j.cropro.2015.10.002
  • Schwarz PB, Hill NS, Rottinghaus GE. 2007. Fate of ergot (Claviceps purpurea) alkaloids during malting and brewing. J Am Soc Brew Chem. 65(1):1–8. doi:10.1094/ASBCJ-2007-0116-01
  • Schwarz PB. 2017. Fusarium head blight and deoxynivalenol in malting and brewing: successes and future challenges. Trop Plant Pathol. 42(3):153–164. doi:10.1007/s40858-017-0146-4
  • Shevach EM. 1985. The effects of cyclosporin A on the immune system. Annu Rev Immunol. 3:397–423. doi:10.1146/annurev.iy.03.040185.002145
  • Shimshoni JA, Cuneah O, Sulyok M, Krska R, Galon N, Sharir B, Shlosberg A. 2013. Mycotoxins in corn and wheat silage in Israel. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 30(9):1614–1625. doi:10.1080/19440049.2013.802840
  • Smith MC, Madec S, Coton E, Hymery N. 2016. Natural co-occurrence of mycotoxins in foods and feeds and their in vitro combined toxicological effects. Toxins 8(4):94. doi:10.3390/toxins8040094.
  • Sooväli P, Koppel M. 2010. Efficacy of fungicide tebuconazole in barley varieties with different resistance level. Agric Food Sci. 19(1):34–42. doi:10.2137/145960610791015069
  • Souza LC, Zambom MA, Pozza MSdS, Neres MA, Radis AC, Borsatti L, Castagnara DD, Gundt S. 2012. Development of microorganisms during storage of wet brewery waste under aerobic and anaerobic conditions. R Bras Zootec. 41(1):188–193. doi:10.1590/S1516-35982012000100027
  • Stähelin H. 1996. The history of cyclosporin A (Sandimmune®) revisited: another point of view. Experientia. 52(1):5–13. doi:10.1007/BF01922409
  • Starkey DE, Ward TJ, Aoki T, Gale LR, Kistler HC, Geiser DM, Suga H, Tóth B, Varga J, O’Donnell K. 2007. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet Biol. 44(11):1191–1204. doi:10.1016/j.fgb.2007.03.001
  • Steiner D, Malachová A, Sulyok M, Krska R. 2021. Challenges and future directions in LC-MS-based multiclass method development for the quantification of food contaminants. Anal Bioanal Chem. 413(1):25–34. doi:10.1007/s00216-020-03015-7
  • Steiner D, Sulyok M, Malachová A, Mueller A, Krska R. 2020. Realizing the simultaneous liquid chromatography-tandem mass spectrometry based quantification of >1200 biotoxins, pesticides and veterinary drugs in complex feed. J Chromatogr A. 1629:461502. doi:10.1016/j.chroma.2020.461502
  • Stojceska V, Ainsworth P. 2008. The effect of different enzymes on the quality of high-fibre enriched brewer’s spent grain breads. Food Chem. 110(4):865–872. doi:10.1016/j.foodchem.2008.02.074
  • Sulyok M, Stadler D, Steiner D, Krska R. 2020. Validation of an LC-MS/MS-based dilute-and-shoot approach for the quantification of> 500 mycotoxins and other secondary metabolites in food crops: challenges and solutions. Anal Bioanal Chem. 412(11):2607–2620. doi:10.1007/s00216-020-02489-9
  • Sy-Cordero AA, Pearce CJ, Oberlies NH. 2012. Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination and biological activities. J Antibiot. 65(11):541–549. doi:10.1038/ja.2012.71
  • Szulc J, Okrasa M, Dybka-Stępień K, Sulyok M, Nowak A, Otlewska A, Szponar B, Majchrzycka K. 2019. Assessment of microbiological indoor air quality in cattle breeding farms. Aerosol Air Qual Res. 20(5):1–10.
  • Thrane U, Adler A, Clasen P-E, Galvano F, Langseth W, Lew H, Logrieco A, Nielsen KF, Ritieni A. 2004. Diversity in metabolite production by Fusarium langsethiae, Fusarium poae, and Fusarium sporotrichioides. Int J Food Microbiol. 95(3):257–266. doi:10.1016/j.ijfoodmicro.2003.12.005
  • Uchida R, Shiomi K, Inokoshi J, Sunazuka T, Tanaka H, Iwai Y, Takayanagi H, Omura S. 1996. Andrastins AC, new protein farnesyltransferase inhibitors produced by Penicillium sp. FO-3929 II. structure elucidation and biosynthesis. J Antibiot. 49(5):418–424. doi:10.7164/antibiotics.49.418
  • Urquhart AS, Hu J, Chooi YH, Idnurm A. 2019. The fungal gene cluster for biosynthesis of the antibacterial agent viriditoxin. Fungal Biol Biotechnol. 6:2. doi:10.1186/s40694-019-0072-y
  • [US EPA]. United States Environmental Protection Agency. 2017. Isopyrazam fact sheet. [accessed 2022 June 11]. https://www3.epa.gov/pesticides/chem_search/reg_actions/pending/fs_PC-129222_05-Oct-11.pdf.
  • Vaclavikova M, Malachova A, Veprikova Z, Dzuman Z, Zachariasova M, Hajslova J. 2013. Emerging’mycotoxins in cereals processing chains: changes of enniatins during beer and bread making. Food Chem. 136(2):750–757. doi:10.1016/j.foodchem.2012.08.031
  • Vanbergen AJ. 2021. A cocktail of pesticides, parasites and hunger leaves bees down and out. Nature. 596(7872):351–352. doi:10.1038/d41586-021-02079-4
  • Vejdovszky K, Hahn K, Braun D, Warth B, Marko D. 2017a. Synergistic estrogenic effects of Fusarium and Alternaria mycotoxins in vitro. Arch Toxicol. 91(3):1447–1460. doi:10.1007/s00204-016-1795-7
  • Vejdovszky K, Schmidt V, Warth B, Marko D. 2017b. Combinatory estrogenic effects between the isoflavone genistein and the mycotoxins zearalenone and alternariol in vitro. Mol Nutr Food Res. 61(3):1600526. doi:10.1002/mnfr.201600526
  • Violino S, Figorilli S, Costa C, Pallottino F. 2020. Internet of beer: a review on smart technologies from mash to pint. Foods. 9(7):950. doi:10.3390/foods9070950
  • Walters DR, Havis ND, Oxley SJ. 2008. Ramularia collo-cygni: the biology of an emerging pathogen of barley. FEMS Microbiol Lett. 279(1):1–7. doi:10.1111/j.1574-6968.2007.00986.x
  • Warne MSJ, Hawker DW. 1995. The number of components in a mixture determines whether synergistic and antagonistic or additive toxicity predominate: the funnel hypothesis. Ecotoxicol Environ Saf. 31(1):23–28. doi:10.1006/eesa.1995.1039
  • Weaver AC, Adams N, Yiannikouris A. 2020. Invited Review: Use of technology to assess and monitor multimycotoxin and emerging mycotoxin challenges in feedstuffs. Appl Anim Sci.  36(1):19–25. doi:10.15232/aas.2019-01898.
  • Westendorf ML, Wohlt JE. 2002. Brewing by-products: their use as animal feeds. Vet Clin North Am Food Anim Pract. 18(2):233–252. doi:10.1016/s0749-0720(02)00016-6
  • [WHO] World Health Organization. 2020. The WHO recommended classification of pesticides by hazard and guidelines to classification 2019. Geneva, Switzerland: World Health Organization. [accessed 2022 June 11]. https://apps.who.int/iris/bitstream/handle/10665/332193/9789240005662-eng.pdf?ua=1.
  • Wocławek-Potocka I, Korzekwa A, Skarzyński DJ. 2008. Czy nieodżywcze składniki pasz – fitoestrogeny stanowią zagrożenie w rozrodzie krów? [Can phytoestrogens pose a danger in the reproduction of cows?]. Med Weter. 64(4 B):515–519.
  • Wocławek-Potocka I, Mannelli C, Boruszewska D, Kowalczyk-Zieba I, Waśniewski T, Skarżyński DJ. 2013. Diverse effects of phytoestrogens on the reproductive performance: cow as a model. Int J Endocrinol. 2013:650984. doi:10.1155/2013/650984
  • Xi X, Yan J, Quan G, Cui L. 2014. Removal of the pesticide pymetrozine from aqueous solution by biochar produced from brewer’s spent grain at different pyrolytic temperatures. BioRes. 9(4):7696–7709.
  • Xu Q, Zhang K, Fu Y, Ma H, Zhu F. 2020. Toxic action and baseline sensitivity of boscalid against Penicillium digitatum. Crop Prot. 137:105272. doi:10.1016/j.cropro.2020.105272
  • Yao H, Xu X, Zhou Y, Xu C. 2018. Impacts of isopyrazam exposure on the development of early-life zebrafish (Danio rerio). Environ Sci Pollut Res Int. 25(24):23799–23808. doi:10.1007/s11356-018-2449-5
  • Yao X, Qiao Z, Zhang F, Liu X, Du Q, Zhang J, Li X, Jiang X. 2021. Effects of a novel fungicide benzovindiflupyr in Eisenia fetida: evaluation through different levels of biological organization. Environ Pollut. 271:116336. doi:10.1016/j.envpol.2020.116336
  • Zin NM, Al-Shaibani MM, Jalil J, Sukri A, Al-Maleki AR, Sidik NM. 2020. Profiling of gene expression in methicillin-resistant Staphylococcus aureus in response to cyclo-(l-Val-l-Pro) and chloramphenicol isolated from Streptomyces sp., SUK 25 reveals gene downregulation in multiple biological targets. Arch Microbiol. 202(8):2083–2092. doi:10.1007/s00203-020-01896-x
  • Zubrod JP, Bundschuh M, Feckler A, Englert D, Schulz R. 2011. Ecotoxicological impact of the fungicide tebuconazole on an aquatic decomposer-detritivore system. Environ Toxicol Chem. 30(12):2718–2724. doi:10.1002/etc.679