Occurrence of mycotoxins in pastures: A systematic review

Main Article Content

João P. R. B. Aranega https://orcid.org/0000-0002-9115-478X
Carlos A. F. Oliveira

Keywords

pastures, animal feed, feed safety, mycotoxins, occurrence

Abstract

In this study, a systematic review is presented on the worldwide occurrence levels of mycotoxins in pastures reported in the scientific literature from January 1987 until December 2021. Trichothecenes and zearalenone were the most frequent mycotoxins found at high levels in pastures from countries in Europe, Oceania, and North America. Alternariol and Ergot alkaloids were also frequently detected, although at low levels. A few surveys were conducted in South American countries, and no information was available from the African and Asian continents, stressing the need for studies on the occurrence of mycotoxins in pastures from those regions, especially in tropical areas, where pastures are used as main sources for animal nutrition.

Abstract 992 | PDF Downloads 742 HTML Downloads 112 XML Downloads 25

References

Adegbeye, M.J., Reddy, P.R.K., Chilaka, C.A., Olalekan, B.B., Elgandour, M.M., Rivas-Cáceres, R.R. and Salem, A.Z., 2020. Mycotoxin toxicity and residue in animal products: prevalence, consumer exposure and reduction strategies–a review. Toxicon 177: 96–108. 10.1016/j.toxicon.2020.01.007

Baholet, D., Kolackova, I., Kalhottka, L., Skladanka, J. and Haninec, P., 2019. Effect of species, fertilization and harvest date on microbial composition and mycotoxin content in forage. Agriculture 9(5): 102. 10.3390/agriculture9050102

Bangar, S.P., Sharma, N., Bhardwaj, A. and Phimolsiripol, Y., 2022. Lactic acid bacteria: a bio-green preservative against mycotoxins for food safety and shelf-life extension. Quality Assurance and Safety of Crops & Foods 14: 13–31. 10.15586/qas.v14i2.1014

Battilani, P., Toscano, P., Van Derfels-Klerx, H.J., Moretti, A., Camardo Leggieri, M., Brera, C., Rottais, A., Goumperis, T. and Robinson, T., 2016. Aflatoxin B1 contamination in maize in Europe increases due to climate change. Scientific Reports 6: 24328. 10.1038/srep24328

Bebber, D.P., Ramotowski, M.A.T. and Gurr, S.J., 2013. Crop pests and pathogens move polewards in a warming world. Nature Climate Change 3: 985–988. 10.1038/nclimate1990

Burkin, A.A. and Kononenko, G.P., 2015. Mycotoxin contamination of meadow grasses in European Russia. Agricultural Biology 50(4): 503–512. 10.15389/agrobiology.2015.4.503eng

Buszewska-Forajta, M., 2020. Mycotoxins, invisible danger of feedstuff with toxic effect on animals. Toxicon 182: 34–53. 10.1016/j.toxicon.2020.04.101

Canty, M.J., Fogarty, U., Sheridan, M.K., Ensley, M.S., Schrunk, D.E. and More, S.J., 2014. Ergot alkaloid intoxication in perennial ryegrass (Lolium perenne): an emerging animal health concern in Ireland? Irish Veterinary Journal 67(1): 21. 10.1186/2046-0481-67-21

Cimbalo, A., Alonso-Garrido, M., Font, G. and Manyes, L., 2020. Toxicity of mycotoxins in vivo on vertebrate organisms: a review. Food and Chemical Toxicology 137: 111161. 10.1016/j.fct.2020.111161

Daou, R., Hoteit, M., Bookari, K., Al-Khalaf, M., Nahle, S., Al-Jawaldeh, A., Koubar, M., Doumiati, S. and EL Khoury, A., 2022. Aflatoxin B1 occurrence in children under the age of five’s food products and aflatoxin M1 exposure assessment and risk characterization of Arab infants through consumption of infant powdered formula: a Lebanese experience. Toxins 14: 290. 10.3390/toxins14050290

Dias-Filho, M.B., 2016. Uso de pastagens para a produção de bovinos de corte no Brasil: passado, presente e futuro. Doc. 418, Empresa Brasileira de Pesquisa Agropecuária, Belém, PR. Available at: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/1042092/1/DOCUMENTOS418.pdf (Accessed 10 Sept 2021).

Di Menna, M.E., Laure, D.R., Poole, P.R., Mortimer, P.H., Hill, R.A. and Agnew, M.P., 1987. Zearalenone in New Zealand pasture herbage and the mycotoxin-producing potential of Fusarium species from pasture. New Zealand Journal of Agricultural Research 30(4): 499–504. 10.1080/00288233.1987.10417963

European Commission, 2010. Commission Regulation (EC) Nº 165/2010 of 26 February 2010. Setting maximum levels for certain contaminants in foodstuffs as regards aflatoxins. Official Journal of the European Union L50: 8–12. Available at: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:050:0008:0012:EN:PDF (Accessed 13 Sept 2021).

European Commission, 2012. Commission Regulation (EC) Nº 154/2012 of 27 March 2012, Monitoring the presence of ergot alkaloids in animal feed and food kinds. Official Journal of the European Union L77: 20–21. Available at: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2012:077:0020:0021:EN:PDF (Accessed 12 Sept 2021).

European Commission, 2013. Commission Regulation (EC) Nº 165/2013 of 27 March 2013, Concerning the presence of T-2 and HT-2 toxins in cereals and cereal-based products. Official Journal of the European Union L91: 12–15. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32013H0165 (Accessed 13 Sept 2021).

European Commission, 2016. Commission Regulation (EC) Nº 1319/2016 of 29 July 2016, Deoxynivalenol, zearalenone and ochratoxin A in pet food. Official Journal of the European Union L208: 58–60. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32016H1319&from=EN (Acessed 13 Sept 2021).

Fallah, A.A., Barani, A. and Nasiri, Z., 2015. Aflatoxin M1 in raw milk in Qazvin Province, Iran: a seasonal study. Food Additives & Contaminants: Part B 8: 195–198. 10.1080/19393210.2015.1046193

Fallah, A.A., Pirali-Kheirabadi, E., Rahnama, M., Saei-Dehkordi, S.S. and Pirali-Kheirabadi, K., 2014. Mycoflora, aflatoxigenic strains of Aspergillus section Flavi and aflatoxins in fish feed. Quality Assurance and Safety of Crops & Foods 6: 419–424. 10.3920/QAS2012.0186

FDA (Food and Drug Administration), 2016. Annual report on mycotoxins in animal food. Report for Fiscal Year: 1–11, Available at: https://www.fda.gov/media/130526/download (Accessed 13 Sept 2021).

Franco. L.T., Ismail, A., Amjad, A. and Oliveira, C.A.F., 2021. Occurrence of toxigenic fungi and mycotoxins in workplaces and human biomonitoring of mycotoxins in exposed workers: a systematic review. Toxin Reviews 40: 576–591. 10.1080/15569543.2020.1795685

Gallo, A., Gianluca, G., Frisvad, J.C., Bertuzzi, T. and Nielsen, K.F., 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. 10.3390/toxins7083057

Gonçalves, B.L., Corassin, C.H. and Oliveira, C.A.F., 2015. Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances 10: 752–760. 10.3923/ajava.2015.752.760

Gott, P.N., Hendel, E.G., Curry, S.M. and Stam, A.M., 2019. Occurrence of mycotoxins in US forage grasses. Journal of Animal Science 97(3): 196. 10.1093/jas/skz258.404

Gott, P.N., Hendel, E.G., Smith, S., Hofstetter-Schahs, U., Robins, K. and Murugesan, G., 2018. Ergovaline and additional mycotoxins in tall fescue. Journal of Animal Science 96(3): 208–209. 10.1093/jas/skz258.404

Gott, P.N., Stam, A., Johns, A., Miller, B.G., Bell, B. and Murugesan, G.R., 2017. Mycotoxin survey of common Bermudagrass in south-central Florida. Journal of Animal Science 95(4): 19–20. 10.2527/asasann.2017.039

Heshmati, A., Khorshidi, M. and Khaneghah, A.M., 2021. The prevalence and risk assessment of aflatoxin in sesame-based products. Italian Journal of Food Science 33(SP1): 92–102. 10.15586/ijfs.v33iSP1.2065

Higgins, J.P.T. and Green, S., 2011. Cochrane handbook for systematic reviews of interventions. Cochrane Training, version 5.1.0 (updated March 2011). Available at: https://handbook-5-1.cochrane.org/ (Accessed 01 July 2021).

Jafari, K., Fathabad, A.E., Fakhri, Y., Shamsaei, M., Miri, M., Farahmandfar, R. and Khaneghah, A.M., 2021. Aflatoxin M1 in traditional and industrial pasteurized milk samples from Tiran County, Isfahan Province: a probabilistic health risk assessment. Italian Journal of Food Science 33(SP1): 103–116. 10.15586/ijfs.v33iSP1.2054

Magnoli, A.P., Poloni, V.L. and Cavaglieri, L., 2019. Impact of mycotoxin contamination in the animal feed industry. Current Opinion in Food Science 29: 99–108. 10.1016/j.cofs.2019.08.009

Medina, A., González-Jartín, J.M. and Sainz, M.J., 2017. Impact of global warming on mycotoxins. Current Opinion in Food Science 18: 76–81. 10.1016/j.cofs.2017.11.009

Mohajeri, F.A., Ghalebi, S.R., Rezaeian, M., Gheisari, H.R., Azad, H.K., Zolfaghari, A. and Fallah, A.A., 2013. Aflatoxin M1 contamination in white and Lighvan cheese marketed in Rafsanjan, Iran. Food Control 33: 525–527. 10.1016/j.foodcont.2013.04.002

Moher, D., Shamseer, L., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P., Stewart, L.A. and PRISMA-P Group, 2015. Preferred reporting items for systematic review and metaanalysis protocols (PRISMA-P) 2015 statement. Systematic Reviews 4: 1. 10.1186/2046-4053-4-1

Mokhtarian, M., Tavakolipour, H., Bagheri, F., Oliveira, C.A.F., Corassin, C.H. and Khaneghah, A.M., 2020. Aflatoxin B1 in the Iranian pistachio nut and decontamination methods: a system-atic review. Quality Assurance and Safety of Crops & Foods 12: 15–25. 10.15586/qas.v12i4.784

Moretti, A., Pascale, M. and Logrieco, A.F., 2019. Mycotoxin risks under a climate change scenario in Europe. Trends in Food Science & Technology 84: 38–40. 10.1016/j.tifs.2018.03.008

Murty, L.D., Duringer, J.M. and Craig, A.M., 2018. Co-exposure of the mycotoxins lolitrem B and ergovaline in steers fed perennial ryegrass (Lolium perenne) straw: metabolic characterization of excreta. Journal of Agricultural and Food Chemistry 66(25): 6394–6401. 10.1021/acs.jafc.8b00963

Nichea, M.J., Palacios, S.A., Chiacchiera, S.M., Sulyok, M., Krska, R., Chulze, S.N., Torres, A.M. and Ramirez, M.L., 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. 10.3390/toxins7083309

Oluwafemi, F., Badmos, A.O., Kareem, S.O., Ademuyiwa, O. and Kolapo, A.L., 2014. Survey of aflatoxin M1 in cows milk from free-grazing cows in Abeokuta, Nigeria. Mycotoxin Research 30(4): 207–211. 10.1007/s12550-014-0204-4

Orina, A.S., Gavrilova, O.P., Gagkaeva, T.Y., Burkin, A.A. and Kononenko, G.P., 2020. The contamination of Fabaceae plants with fungi and mycotoxins. Agricultural and Food Science 29(3): 265–275. 10.23986/afsci.89171

Penagos-Tabares, F., Khiaosa-Ard, R., Nagl, V., Faas, J., Jenkins, T., Sulyok, M. and 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. 10.3390/toxins13070460

Pereira, C.S., Cunha, S.C. and Fernandes, J.O., 2019. Prevalent mycotoxins in animal feed: Occurrence and analytical methods. Toxins 11(5): 290. 10.3390/toxins11050290

Pires, R.C., Portinari, M.R.P., Moraes, G.Z., Khaneghah, A.M., Gonçalves, B.L., Rosim, R.E., Oliveira, C.A.F. and Corassin, C.H., 2022. Evaluation of anti-aflatoxin M1 effects of heat-killed cells of Saccharomyces cerevisiae in Brazilian commercial yogurts. Quality Assurance and Safety of Crops & Foods 14: 75–81. 10.15586/qas.v14i1.1006

Reed, K.F.M. and Moore, D.D., 2009. A preliminary survey of zearalenone and other mycotoxins in Australian silage and pasture. Animal Production Science 49(8): 696–703. 10.1071/EA08164

Reed, K.F.M., Walsh, J.R., Mcfarlane, N.M. and Sprague, M, 2004. Zearalenone and its presence in pasture. Animal Production in Australia 25: 140–143. 10.1071/SA0401036

Rodrigues, I.A., 2014. Review on the effects of mycotoxins in dairy ruminants. Animal Production Science 54(9): 1155–1165. 10.1071/AN13492

Salvat, A.E., Balbuena, O., Ricca, A., Comerio, R.M., Rosello Brajovich, J.E., Rojas, D., Berretta, M.F., Delssin, E., Bedascarrasbure, E. and Salerno, J.C., 2013. Presencia de zearalenona en pasturas del este de Chaco. Revista de Investigaciones Agropecuarias 39(1): 31–36. Available at: http://www.scielo.org.ar/pdf/ria/v39n1/v39n1a06.pdf (Accessed 20 Sept 2021).

Skládanka, J., Adam, V., Doležal, P., Nedělník J., Kizek, R., Linduskova, H., Mejia, J. E.A. and Nawrat, A., 2013. How do grass species, season and ensiling influence mycotoxin content in forage? International Journal of Environmental Research and Public Health 10(11): 6084–6095. 10.3390/ijerph10116084

Skládanka, J., Nedělník J., Adam, V., Doležal, P., Moravcová H. and Dohna, V., 2011. Forage as a primary source of mycotoxins in animal diets. International Journal of Environmental Research and Public Health 8(1): 37–50. 10.3390/ijerph8010037

Souza, C., Khaneghah, A.M. and Oliveira, C.A.F., 2021. The occurrence of aflatoxin M1 in industrial and traditional fermented milk: a systematic review study. Italian Journal of Food Science 33(SP1): 12–23. 10.15586/ijfs.v33iSP1.1982

Štýbnarová, M., Křížová, L., Pavlok, S., Mičová, P., Látal, O. and Pozdíšek, J., 2016. Nutritive value and mycotoxin contamination of herbage in mountain locality exposed to renewed cattle grazing. Acta Universitatis Agriculturae Et Silviculturae Mendelianae Brunensis 64: 883–891. 10.11118/actaun201664030883

Vedovatto, M.G., Bento, A.L., Kiefer, C., Souza, K.M.R. and Franco, G.L., 2020. Micotoxinas na dieta de bovinos de corte: revisão. Archivos de Zootecnia 69(266): 234–244. 10.21071/az.v69i266.5119

Yang, C., Song, G. and Lim, W., 2020. Effects of mycotoxin-contaminated feed on farm animals. Journal of Hazardous Materials 389: 122087. 10.1016/j.jhazmat.2020.122087