Mycotoxin Res. 2021 Nov;37(4):297-313. doi: 10.1007/s12550-021-00442-y. Epub 2021 Sep 18.
Survey of zearalenone and type-B trichothecene mycotoxins in swine feed in the USA.
Mycotoxin research
Erica D Pack, Sarah Weiland, Rob Musser, David G Schmale
Affiliations
Affiliations
- School of Plant and Environmental Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
- Nutriquest, IA, Mason City, USA.
- School of Plant and Environmental Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA. [email protected].
PMID: 34537950
DOI: 10.1007/s12550-021-00442-y
Abstract
New information is needed regarding the types and concentrations of mycotoxins in swine feed. We hypothesized that (1) the mycotoxins deoxynivalenol (DON), 3-acetyldeoxynivalenol (3-AcDON), 15-acetyldeoxynivalenol (15-AcDON), nivalenol (NIV), and zearalenone (ZEN) vary among swine ingredient and feed types, and (2) the inclusion of specific ingredients is associated with mycotoxin contamination in complete feed. A total of 707 samples were collected from cooperators in 14 states between June 2018 and January 2020 then analyzed for DON, 3-AcDON, 15-AcDON, NIV, and ZEN contamination using gas chromatography-mass spectrometry (GC-MS). Ninety-four percent (663/707) of samples contained DON, 33% (230/707) of samples contained 3-AcDON, 57% (404/707) of samples contained 15-AcDON, 1% (6/707) of samples contained NIV, and 47% (335/707) of samples contained ZEN. Seventy-three percent (514/707) of samples contained multiple mycotoxins. Resulting DON concentrations were below the national advisory limits for all sample types, and no advisory limits are imposed for the other mycotoxins studied. Increased incorporation of distiller's dried grains with solubles (DDGS) was associated with increased DON in complete feed (R
© 2021. Society for Mycotoxin (Research Gesellschaft für Mykotoxinforschung e.V.) and Springer-Verlag GmbH Germany, part of Springer Nature.
Keywords: Distillers’ grains; Fusarium; Mycotoxin; Swine feed
References
- Abdallah MF, Girgin G, Baydar T et al (2017) 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 97:4419–4428. https://doi.org/10.1002/jsfa.8293 - PubMed
- Alassane-Kpembi I, Puel O, Oswald IP (2015) Toxicological interactions between the mycotoxins deoxynivalenol, nivalenol and their acetylated derivatives in intestinal epithelial cells. Arch Toxicol 89:1337–1346. https://doi.org/10.1007/s00204-014-1309-4 - PubMed
- Alimentarius C (1995) Codex Alimentarius international food standards, General standard for contaminants and toxins in food and feed. CXS 193-1995. Adopted in 1995. Revised in 1997, 2006, 2008, 2009. Amended in 2010, 2012, 2013, 2014, 2015, 2016, 2017. Food and Agriculture Organization of the United Nations (FAO), the World Health Organization (WHO) - PubMed
- Andretta I, Kipper M, Hauschild L et al (2016) Meta-analysis of individual and combined effects of mycotoxins on growing pigs. Sci Agric 73:328–331. https://doi.org/10.1590/0103-9016-2015-0132 - PubMed
- Averill T (2020) Quarterly hogs and pigs, executive summary. United States Department of Agriculture, National Agriculture Statistics Service. https://www.nass.usda.gov/Newsroom/Executive_Briefings/2020/03-26-2020.pdf . Accessed on 14 Sept 2021 - PubMed
- Berger G, Green A, Khatibi P, Brooks W, Rosso L, Liu S, Chao S, Griffey C, Schmale D (2014) Characterization of fusarium head blight resistance and deoxynivalenol accumulation in hulled and hulless winter barley. Plant Dis 98(5):599–606. https://doi.org/10.1094/PDIS-05-13-0479-RE - PubMed
- Binder EM, Tan LM, Chin LJ et al (2007) Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim Feed Sci Technol 137:265–282. https://doi.org/10.1016/j.anifeedsci.2007.06.005 - PubMed
- Cai Y, McLaughlin M, Zhang K (2020) Advancing the FDA/office of regulatory affairs mycotoxin program: new analytical method approaches to addressing needs and challenges. J AOAC Int 103:705–709. https://doi.org/10.1093/jaocint/qsz007 - PubMed
- Castañares E, Martínez M, Cristos D et al (2019) Fusarium species and mycotoxin contamination in maize in Buenos Aires province, Argentina. Eur J Plant Pathol 155:1265–1275. https://doi.org/10.1007/s10658-019-01853-5 - PubMed
- Demaree-Saddler H (2019) Alltech: high risk of mycotoxin in U.S. corn. In: World grain. https://www.world-grain.com/articles/13003-alltech-high-risk-of-mycotoxin-in-us-corn . Accessed 14 Jan 2021 - PubMed
- Dohlman E (2003) Mycotoxin hazards and regulations: impacts on food and animal feed crop trade. United States Department of Agriculture - PubMed
- Doran T (2020) Corn quality above five-year average. In: AgriNews. https://www.agrinews-pubs.com/business/2020/12/31/corn-quality-above-five-year-average/ . Accessed 14 Jan 2021 - PubMed
- Dzuman Z, Stranska-Zachariasova M, Vaclavikova M et al (2016) Fate of free and conjugated mycotoxins within the production of distiller’s dried grains with solubles (DDGS). J Agric Food Chem 64:5085–5092. https://doi.org/10.1021/acs.jafc.6b00304 - PubMed
- Eskola M, Altieri A, Galobart J (2018) Overview of the activities of the European Food Safety Authority on mycotoxins in food and feed. World Mycotox J 11(2):277–289. https://doi.org/10.3920/WMJ2017.2270 - PubMed
- FDA (2010) Guidance for industry and FDA: advisory levels for deoxynivalenol (DON) in finished wheat products for human consumption and grains and grain by-products used for animal feed. In: U.S. Food Drug Adm. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-and-fda-advisory-levels-deoxynivalenol-don-finished-wheat-products-human . Accessed 14 Sept 2021 - PubMed
- Gajecka M, Rybarczyk L, Jakimiuk E et al (2012) The effect of experimental long-term exposure to low-dose zearalenone on uterine histology in sexually immature gilts. Exp Toxicol Pathol 64:537–542. https://doi.org/10.1016/j.etp.2010.11.009 - PubMed
- Gajęcka M, Rybarczyk L, Zwierzchowski W et al (2011) The effect of experimental, long-term exposure to low-dose zearalenone mycotoxicosis on the histological condition of ovaries in sexually immature gilts. Theriogenology 75:1085–1094. https://doi.org/10.1016/j.theriogenology.2010.11.017 - PubMed
- Gajęcka M, Tarasiuk M, Zielonka Ł et al (2016) Risk assessment for changes in the metabolic profile and body weights of pre-pubertal gilts during long-term monotonic exposure to low doses of zearalenone (ZEN). Res Vet Sci 109:169–180. https://doi.org/10.1016/j.rvsc.2016.07.013 - PubMed
- Gale LR, Harrison SA, Ward TJ et al (2011) Nivalenol-type populations of Fusarium graminearum and F asiaticum are prevalent on wheat in southern Louisiana. Phytopathology 101:124–134. https://doi.org/10.1094/PHYTO-03-10-0067 - PubMed
- Gale LR, Ward TJ, Balmas V, Kistler HC (2007) Population subdivision of Fusarium graminearum sensu stricto in the upper midwestern united states. Phytopathology 97:1434–1439. https://doi.org/10.1094/PHYTO-97-11-1434 - PubMed
- Gerez JR, Pinton P, Callu P et al (2015) Deoxynivalenol alone or in combination with nivalenol and zearalenone induce systemic histological changes in pigs. Exp Toxicol Pathol 67:89–98. https://doi.org/10.1016/j.etp.2014.10.001 - PubMed
- Glenn AE (2007) Mycotoxigenic Fusarium species in animal feed. Anim Feed Sci Technol 137:213–240. https://doi.org/10.1016/j.anifeedsci.2007.06.003 - PubMed
- Gruber-Dorninger C, Jenkins T, Schatzmayr G (2019) Global mycotoxin occurrence in feed: a ten-year survey. Toxins 11:375. https://doi.org/10.3390/toxins11070375 - PubMed
- Gutleb AC, Caloni F, Giraud F et al (2015) Detection of multiple mycotoxin occurrences in soy animal feed by traditional mycological identification combined with molecular species identification. Toxicol Rep 2:275–279. https://doi.org/10.1016/j.toxrep.2015.01.006 - PubMed
- Hlavová K, Štěpánová H, Šťastný K et al (2020) Minimal concentrations of deoxynivalenol reduce cytokine production in individual lymphocyte populations in pigs. Toxins 12:190. https://doi.org/10.3390/toxins12030190 - PubMed
- Jennings P, Coates ME, Walsh K et al (2004) Determination of deoxynivalenol- and nivalenol-producing chemotypes of Fusarium graminearum isolated from wheat crops in Angland and Wales. Plant Pathol 53:643–652. https://doi.org/10.1111/j.0032-0862.2004.01061.x - PubMed
- Ji F, He D, Olaniran AO et al (2019) Occurrence, toxicity, production and detection of Fusarium mycotoxin: a review. Food Prod Process Nutr 1:6. https://doi.org/10.1186/s43014-019-0007-2 - PubMed
- Katzenellenbogen BS, Katzenellenbogen JA, Mordecai D (1979) Zearalenones: Characterization of the estrogenic potencies and receptor interactions of a series of fungal β-resorcylic acid lactones. Endocrinology 105:33–40. https://doi.org/10.1210/endo-105-1-33 - PubMed
- Kelly AC, Clear RM, O’Donnell K et al (2015) Diversity of Fusarium head blight populations and trichothecene toxin types reveals regional differences in pathogen composition and temporal dynamics. Fungal Genet Biol 82:22–31. https://doi.org/10.1016/j.fgb.2015.05.016 - PubMed
- Khatibi PA, Berger G, Liu S et al (2012) Resistance to Fusarium head blight and deoxynivalenol accumulation in Virginia barley. Plant Dis 96:279–284. https://doi.org/10.1094/PDIS-07-11-0551 - PubMed
- Khatibi PA, McMaster NJ, Musser R, Schmale DG (2014) Survey of mycotoxins in corn distillers’ dried grains with solubles from seventy-eight ethanol plants in Twelve states in the U.S. in 2011. Toxins 6:1155–1168. https://doi.org/10.3390/toxins6041155 - PubMed
- Khoshal AK, Novak B, Martin PGP et al (2019) Co-occurrence of DON and emerging mycotoxins in worldwide finished pig feed and their combined toxicity in intestinal cells. Toxins 11:727. https://doi.org/10.3390/toxins11120727 - PubMed
- Kongkapan J, Polapothep A, Owen H, Giorgi M (2016) A brief overview of our current understanding of nivalenol: a growing potential danger yet to be fully investigated. Israel Journal of Veterinary Medicine 71:3–9 - PubMed
- Leslie JF (1990) Fusarium spp. from corn, sorghum, and soybean fields in the central and eastern united states. Phytopathology 80:343. https://doi.org/10.1094/Phyto-80-343 - PubMed
- Liu D, Ge L, Wang Q et al (2020) Low-level contamination of deoxynivalenol: a threat from environmental toxins to porcine epidemic diarrhea virus infection. Environ Int 143:105949. https://doi.org/10.1016/j.envint.2020.105949 - PubMed
- Logrieco A, Miller J, Eskola M et al (2018) The mycotox charter: increasing awareness of, and concerted action for, minimizing mycotoxin exposure worldwide. Toxins 10:149. https://doi.org/10.3390/toxins10040149 - PubMed
- Ma R, Zhang L, Liu M et al (2018) Individual and combined occurrence of mycotoxins in feed ingredients and complete feeds in china. Toxins 10:113. https://doi.org/10.3390/toxins10030113 - PubMed
- Magnoli AP, Poloni VL, Cavaglieri L (2019) Impact of mycotoxin contamination in the animal feed industry. Curr Opin Food Sci 29:99–108. https://doi.org/10.1016/j.cofs.2019.08.009 - PubMed
- McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 3:802–814. https://doi.org/10.3390/toxins3070802 - PubMed
- McMaster N, Acharya B, Harich K et al (2019) Quantification of the mycotoxin deoxynivalenol (DON) in Sorghum using GC-MS and a stable isotope dilution assay (SIDA). Food Anal Methods 12:2334–2343. https://doi.org/10.1007/s12161-019-01588-3 - PubMed
- Medina A, Akbar A, Baazeem A et al (2017) Climate change, food security and mycotoxins: do we know enough? Fungal Biol Rev 31:143–154. https://doi.org/10.1016/j.fbr.2017.04.002 - PubMed
- Miller JD, Greenhalgh R, Wang Y, Lu M (1991) Trichothecene chemotypes of three Fusarium species. Mycologia 83:121–130. https://doi.org/10.1080/00275514.1991.12025988 - PubMed
- Neme K, Mohammed A (2017) Mycotoxin occurrence in grains and the role of postharvest management as a mitigation strategies. A Review Food Control 78:412–425. https://doi.org/10.1016/j.foodcont.2017.03.012 - PubMed
- Pack E, Stewart J, Rhoads M et al (2020) Effects of short-term moderate ZEN consumption on uterosacral ligament elasticity in pubertal gilts. Res Vet Sci 133:202–209. https://doi.org/10.1016/j.rvsc.2020.09.023 - PubMed
- Pack ED, Meyerhoff K, Schmale DG (2021) Tracking zearalenone and type-b trichothecene mycotoxins in the commercial production of beer and brewers’ spent grains. J Am Soc Brew Chem 1–10. https://doi.org/10.1080/03610470.2021.1938489 - PubMed
- Patience JF (1996) Precision in swine feeding programs: an integrated approach. Anim Feed Sci Technol 59:137–145. https://doi.org/10.1016/0377-8401(95)00894-2 - PubMed
- Payros D, Alassane-Kpembi I, Pierron A et al (2016) Toxicology of deoxynivalenol and its acetylated and modified forms. Arch Toxicol 90:2931–2957. https://doi.org/10.1007/s00204-016-1826-4 - PubMed
- Peng WX, Marchal JLM, van der Poel AFB (2018) Strategies to prevent and reduce mycotoxins for compound feed manufacturing. Anim Feed Sci Technol 237:129–153. https://doi.org/10.1016/j.anifeedsci.2018.01.017 - PubMed
- Pereira CS, Cunha SC, Fernandes JO (2019) Prevalent mycotoxins in animal feed occurrence and analytical methods. Toxins 11:290. https://doi.org/10.3390/toxins11050290 - PubMed
- Pestka J (2010) Toxicological mechanisms and potential health effects of deoxynivalenol and nivalenol. World Mycotoxin J 3:323–347. https://doi.org/10.3920/WMJ2010.1247 - PubMed
- Pinotti L, Ottoboni M, Giromini C et al (2016) Mycotoxin contamination in the EU feed supply chain: a focus on cereal byproducts. Toxins 8:45. https://doi.org/10.3390/toxins8020045 - PubMed
- Rai A, Das M, Tripathi A (2020) Occurrence and toxicity of a Fusarium mycotoxin, zearalenone. Crit Rev Food Sci Nutr 60:2710–2729. https://doi.org/10.1080/10408398.2019.1655388 - PubMed
- Schmale DG, Ross SD, Fetters TL et al (2012) Isolates of Fusarium graminearum collected 40–320 meters above ground level cause Fusarium head blight in wheat and produce trichothecene mycotoxins. Aerobiologia 28:1–11. https://doi.org/10.1007/s10453-011-9206-2 - PubMed
- Schmale DG, Wood-Jones AK, Cowger C et al (2011) Trichothecene genotypes of Gibberella zeae from winter wheat fields in the eastern USA. Plant Pathol 60:909–917. https://doi.org/10.1111/j.1365-3059.2011.02443.x - PubMed
- Singh J, Mehta A (2020) Rapid and sensitive detection of mycotoxins by advanced and emerging analytical methods: a review. Food Sci Nutr 8:2183–2204. https://doi.org/10.1002/fsn3.1474 - PubMed
- Spiehs MJ, Whitney MH, Shurson GC (2002) Nutrient database for distiller’s dried grains with soluble produced from new ethanol plants in Minnesota and south dakota. J Anim Sci 80:2639–2645. https://doi.org/10.2527/2002.80102639x - PubMed
- Stock JD, Supakorn C, Hostetler C, Stalder KJ (2017) Prolapse incidence in swine breeding herds is a cause for concern. Open J Vet Med 7:85–97. https://doi.org/10.4236/ojvm.2017.78009 - PubMed
- Tarazona A, Gómez JV, Mateo F et al (2020) Study on mycotoxin contamination of maize kernels in Spain. Food Control 118:107370. https://doi.org/10.1016/j.foodcont.2020.107370 - PubMed
- U.S. Grains Council (2020) USGC releases 2020/2021 corn harvest quality report. In: Ethanol Prod Mag. http://ethanolproducer.com/articles/17798/usgc-releases-2020-2021-corn-harvest-quality-report . Accessed 14 Jan 2021 - PubMed
- Valverde-Bogantes E, Bianchini A, Herr JR et al (2020) Recent population changes of Fusarium head blight pathogens: drivers and implications. Can J Plant Pathol 42:315–329. https://doi.org/10.1080/07060661.2019.1680442 - PubMed
- van der Lee T, Zhang H, van Diepeningen A, Waalwijk C (2015) Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Addit Contam Part A 32:453–460. https://doi.org/10.1080/19440049.2014.984244 - PubMed
- Voss KA, Snook ME (2010) Stability of the mycotoxin deoxynivalenol (DON) during the production of flour-based foods and wheat flake cereal. Food Addit Contam Part A 27:1694–1700. https://doi.org/10.1080/19440049.2010.514688 - PubMed
- Ward TJ, Clear RM, Rooney AP et al (2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol 45:473–484. https://doi.org/10.1016/j.fgb.2007.10.003 - PubMed
- Wellington MO, Bosompem MA, Petracek R et al (2020) Effect of long-term feeding of graded levels of deoxynivalenol (DON) on growth performance, nutrient utilization, and organ health in finishing pigs and DON content in biological samples. 9 - PubMed
- Whitaker TB, Johansson AS (2005) Sampling uncertainties for the detection of chemical agents in complex food matrices. J Food Prot 68:1306–1313. https://doi.org/10.4315/0362-028X-68.6.1306 - PubMed
- Whitney MH, Shurson GC (2004) Growth performance of nursery pigs fed diets containing increasing levels of corn distiller’s dried grains with solubles originating from a modern midwestern ethanol plant. J Anim Sci 82:122–128. https://doi.org/10.2527/2004.821122x - PubMed
- Wu F (2007) Measuring the economic impacts of Fusarium toxins in animal feeds. Anim Feed Sci Technol 137:363–374. https://doi.org/10.1016/j.anifeedsci.2007.06.010 - PubMed
- Wu F, Munkvold GP (2008) Mycotoxins in ethanol co-products: modeling economic impacts on the livestock industry and management strategies. J Agric Food Chem 56:3900–3911. https://doi.org/10.1021/jf072697e - PubMed
- Xu W, Han X, Li F (2019) Co-occurrence of multi-mycotoxins in wheat grains harvested in Anhui province, China. Food Control 96:180–185. https://doi.org/10.1016/j.foodcont.2018.09.006 - PubMed
- Yang C, Song G, Lim W (2020) Effects of mycotoxin-contaminated feed on farm animals. J Hazard Mater 389:122087. https://doi.org/10.1016/j.jhazmat.2020.122087 - PubMed
- Yoshizawa T, Jin Y (1995) Natural occurrence of acetylated derivatives of deoxynivalenol and nivalenol in wheat and barley in Japan. Food Addit Contam 12:689–694. https://doi.org/10.1080/02652039509374358 - PubMed
- Zhang Y, Caupert J (2012) Survey of mycotoxins in U.S. distiller’s dried grains with solubles from 2009 to 2011. J Agric Food Chem 60:539–543. https://doi.org/10.1021/jf203429f - PubMed
- Zheng W, Feng N, Wang Y et al (2019) Effects of zearalenone and its derivatives on the synthesis and secretion of mammalian sex steroid hormones: a review. Food Chem Toxicol 126:262–276. https://doi.org/10.1016/j.fct.2019.02.031 - PubMed
- Zhou H, Guog T, Dai H et al (2020) Deoxynivalenol: toxicological profiles and perspective views for future research. World Mycotoxin J 13:179–188. https://doi.org/10.3920/WMJ2019.2462 - PubMed
- Zijlstra RT, Beltranena E (2013) Swine convert co-products from food and biofuel industries into animal protein for food. Anim Front 3:48–53. https://doi.org/10.2527/af.2013-0014 - PubMed
- Zinedine A, Soriano JM, Moltó JC, Mañes J (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem Toxicol 45:1–18. https://doi.org/10.1016/j.fct.2006.07.030 - PubMed
Publication Types
Grant support