Potential Health Risk Associated with Mycotoxins in Oat Grains Consumed in Spain
Abstract
:1. Introduction
2. Results
2.1. Method Validation
2.2. Analysis of Oat Grain Samples
2.2.1. Zearalenone
2.2.2. Deoxynivalenol (DON) and 3-Acetyl-Deoxynivalenol (3-ADON)
2.2.3. T-2 Toxin (T2) and HT-2 Toxin (HT2)
2.2.4. Fumonisins
2.2.5. Aflatoxins
2.2.6. Ochratoxin A
2.3. Co-Occurrence of Mycotoxins
3. Discussion
4. Conclusions
5. Materials and Methods
5.1. Samples
5.2. Standards and Reagents
5.3. Determination of Mycotoxins
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Chen, J.; Raymond, K. Beta-glucans in the treatment of diabetes and associated cardiovascular risks. Vasc. Health Risk Manag. 2008, 4, 1265–1272. [Google Scholar] [CrossRef] [PubMed]
- Hou, Q.; Li, Y.; Li, L.; Cheng, G.; Sun, X.; Li, S.; Tian, H. The metabolic effects of oats intake in patients with type 2 diabetes: A systematic review and meta-analysis. Nutrients 2015, 7, 10369–10387. [Google Scholar] [CrossRef]
- Rasane, P.; Jha, A.; Sabikhi, L.; Kumar, A.; Unnikrishnan, V.S. Nutritional advantages of oats and opportunities for its processing as value added foods—A review. J. Food Sci. Technol. 2015, 52, 662–675. [Google Scholar] [CrossRef] [PubMed]
- FAO. Countries by Commodity, Ranking. FAOSTAT. Available online: http://www.fao.org/faostat/en/#rankings/countries_by_commodity (accessed on 3 March 2021).
- Luke, Grain Production Volumes. Available online: https://www.luke.fi/ruokafakta/en/field-crops/grain-production-volumes/ (accessed on 3 March 2021).
- OEC. The Observatory of Economic Complexity. Available online: https://oec.world/es/profile/hs92/oats (accessed on 4 March 2021).
- Perrone, G.; Gallo, A. Aspergillus species and their associated mycotoxins. In Mycotoxigenic Fungi: Methods and Protocols, Methods in Molecular Biology; Moretti, A., Susca, A., Eds.; Springer Science + Business Media LLC: New York, NY, USA, 2017; Volume 1542, pp. 33–49. [Google Scholar]
- Munkvold, G.P. Fusarium species and their associated mycotoxins. In Mycotoxigenic Fungi: Methods and Protocols, Methods in Molecular Biology; Moretti, A., Susca, A., Eds.; Springer Science + Business Media LLC: New York, NY, USA, 2017; Volume 1542, pp. 51–106. [Google Scholar]
- Hofgaard, I.S.; Aamot, H.U.; Torp, T.; Jestoi, M.; Lattanzio, V.M.T.; Klemsdal, S.S.; Waalwijk, C.; Van der Lee, T.; Brodal, G. Associations between Fusarium species and mycotoxins in oats and spring wheat from farmers’ fields in Norway over a six-year period. World Mycotoxin J. 2016, 9, 365–378. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Hietaniemi, V.; Ramo, S.; Yli-Mattila, T.; Jestoi, M.; Peltonen, S.; Kartio, M.; Sievilainen, E.; Koivisto, T.; Parikka, P. Updated survey of Fusarium species and toxins in Finnish cereal grains. Food Addit. Contam. Part A 2016, 33, 831–848. [Google Scholar] [CrossRef]
- Edwards, S.G. Fusarium mycotoxin content of UK organic and conventional oats. Food Addit. Contam. 2009, 26, 1063–1069. [Google Scholar] [CrossRef] [PubMed]
- De Colli, L.; De Ruyck, K.; Abdallah, M.F.; Finnan, J.; Mullins, E.; Kildea, S.; Spink, J.; Elliott, C.; Danaher, M. Natural co-occurrence of multiple mycotoxins in unprocessed oats grown in Ireland with various production systems. Toxins 2021, 13, 188. [Google Scholar] [CrossRef] [PubMed]
- Gottschalk, C.; Barthel, J.; Engelhardt, G.; Bauer, J.; Meyer, K. Occurrence of type A trichothecenes in conventionally and organically produced oats and oat products. Mol. Nutr. Food Res. 2007, 51, 1547–1553. [Google Scholar] [CrossRef]
- Schöneberg, T.; Jenny, E.; Wettstein, F.E.; Bucheli, T.D.; Mascher, F.; Bertossa, M.; Musa, T.; Seifert, K.; Gräfenhan, T.; Keller, B.; et al. Occurrence of Fusarium species and mycotoxins in Swiss oats—Impact of cropping factors. Eur. J. Agron. 2018, 92, 123–132. [Google Scholar] [CrossRef]
- Rasmussen, P.H.; Nielsen, K.F.; Ghorbani, F.N.; Spliid, H.; Nielsen, G.C.; Jørgensen, L.N. Occurrence of different trichothecenes and deoxynivalenol-3-β-D-glucoside in naturally and artificially contaminated Danish cereal grains and whole maize plants. Mycotoxin Res. 2012, 28, 181–190. [Google Scholar] [CrossRef]
- Bernhoft, A.; Clasen, P.E.; Kristoffersen, A.B.; Torp, M. Less Fusarium infestation and mycotoxin contamination in organic than in conventional cereals. Food Addit. Contam. 2010, 27, 842–852. [Google Scholar] [CrossRef]
- Edwards, S.G.; Imathiu, S.M.; Ray, R.V.; Back, M.; Hare, M.C. Molecular studies to identify the Fusarium species responsible for HT-2 and T-2 mycotoxins in UK oats. Int. J. Food Microbiol. 2012, 156, 168–175. [Google Scholar] [CrossRef]
- Opoku, N.; Back, M.; Edwards, S.G. Development of Fusarium langsethiae in commercial cereal production. Eur. J. Plant Pathol. 2013, 136, 159–170. [Google Scholar] [CrossRef]
- European Commission. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union 2006, 364, 5–24. [Google Scholar]
- European CommissionEuropean Commission. Commission recommendation on the presence of T-2 and HT-2 toxin in cereals and cereal products. Off. J. Eur. Union 2013, 91, 12–15. [Google Scholar]
- Lee, H.J.; Ryu, D. Worldwide occurrence of mycotoxins in cereals and cereal-derived food products: Public health perspectives of their co-occurrence. J. Agric. Food Chem. 2017, 65, 7034–7051. [Google Scholar] [CrossRef]
- Luo, S.; Du, H.; Kebede, H.; Liu, Y.; Xing, F. Contamination status of major mycotoxins in agricultural product and food stuff in Europe. Food Control 2021, 127, 108120. [Google Scholar] [CrossRef]
- Eskola, M.; Kos, G.; Elliott, C.T.; Hajšlová, J.; Mayar, S.; Krska, R. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit. Rev. Food Sci. Nutr. 2020, 60, 2773–2789. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef]
- Grenier, B.; Oswald, I. Mycotoxin co-contamination of food and feed: Meta-analysis of publications describing toxicological interactions. World Mycotoxin J. 2011, 4, 285–313. [Google Scholar] [CrossRef]
- Malachová, A.; Stránská, M.; Václavík, M.; Elliott, C.T.; Black, C.; Meneely, J.; Hajšlová, J.; Ezekiel, C.N.; Schuhmacher, R.; Krska, R. Advanced LC–MS-based methods to study the co-occurrence and metabolization of multiple mycotoxins in cereals and cereal-based food. Anal. Bioanal. Chem. 2018, 410, 801–825. [Google Scholar] [CrossRef] [PubMed]
- Romera, D.; Mateo, E.M.; Mateo-Castro, R.; Gómez, J.V.; Gimeno-Adelantado, J.V.; Jiménez, M. Determination of multiple mycotoxins in feedstuffs by combined use of UPLC–MS/MS and UPLC–QTOF–MS. Food Chem. 2018, 267, 140–148. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.H.; Hong, S.Y.; Kang, J.W.; Cho, S.M.; Lee, K.R.; An, T.K.; Lee, C.; Chung, S.H. Simultaneous determination of multi-mycotoxins in cereal grains collected from South Korea by LC/MS/MS. Toxins 2017, 9, 106. [Google Scholar] [CrossRef] [PubMed]
- Vidal, A.; Marín, S.; Ramos, A.J.; Cano-Sancho, G.; Sanchis, V. Determination of aflatoxins, deoxynivalenol, ochratoxin A and zearalenone in wheat and oat based bran supplements sold in the Spanish market. Food Chem. Toxicol. 2013, 53, 133–138. [Google Scholar] [CrossRef] [PubMed]
- Tarazona, A.; Gómez, J.V.; Mateo, F.; Jiménez, M.; Romera, D.; Mateo, E.M. Study on mycotoxin contamination of maize kernels in Spain. Food Control 2020, 118, 107370. [Google Scholar] [CrossRef]
- SANTE. European Commission Directorate General for Health and Food Safety. Guidance Document on Analytical Quality Control and Method Validation Procedures for Pesticide Residues and Analysis in Food and Feed. SANTE/11813/2017, 21–22, November, 2017, rev.0. Available online: https://pdf4pro.com/fullscreen/analytical-quality-control-european-commission-5b920d.html (accessed on 15 April 2020).
- Agriopoulou, S.; Stamatelopoulou, E.; Varzakas, T. Advances in occurrence, importance, and mycotoxin control strategies: Prevention and detoxification in foods. Foods 2020, 9, 137. [Google Scholar] [CrossRef]
- Rai, A.; Dixit, S.; Pratap Singh, S.; Kumar Gautam, N.; Das, M.; Tripathi, A. Presence of zearalenone in cereal grains and its exposure risk assessment in Indian population. J. Food Sci. 2018, 83, 3126–3133. [Google Scholar] [CrossRef] [PubMed]
- Van Der Fels-Klerx, H.J.; Klemsdal, S.; Hietaniemi, V.; Lindblad, M.; Ioannou-Kakouri, E.; Van Asselt, E.D. Mycotoxin contamination of cereal grain commodities in relation to climate in North West Europe. Food Addit. Contam. Part A 2012, 29, 1581–1592. [Google Scholar] [CrossRef]
- Lorenz, N.; Dänicke, S.; Edler, L.; Gottschalk, C.; Lassek, E.; Marko, D.; Rychlik, M.; Mally, A. A critical evaluation of health risk assessment of modified mycotoxins with a special focus on zearalenone. Mycotoxin Res. 2019, 35, 27–46. [Google Scholar] [CrossRef]
- EFSA—European Food Safety Authority. Scientific opinion on the risks for public health related to the presence of zearalenone in food. EFSA J. 2011, 9, 2197. [Google Scholar] [CrossRef]
- Edwards, S.G. Impact of agronomic and climatic factors on the mycotoxin content of harvested oats in the United Kingdom. Food Addit. Contam. Part A 2017, 34, 2230–2241. [Google Scholar] [CrossRef] [PubMed]
- Gruber-Dorninger, C.; Jenkins, T.; Schatzmayr, G. Global mycotoxin occurrence in feed: A ten-year survey. Toxins 2019, 11, 375. [Google Scholar] [CrossRef] [PubMed]
- Šliková, S.; Gavurníková, S.; Hašana, R.; Mináriková, M.; Gregová, E. Deoxynivalenol in grains of oats and wheat produced in Slovakia. Agric. For. 2016, 62, 343–348. [Google Scholar]
- Mishra, S.; Srivastava, S.; Dewangan, J.; Divakar, A.; Rath, S.K. Global occurrence of deoxynivalenol in food commodities and exposure risk assessment in humans in the last decade: A survey. Crit. Rev. Food Sci. Nutr. 2020, 60, 1346–1374. [Google Scholar] [CrossRef]
- Grafenhan, T.; Patrick, S.K.; Roscoe, M.; Trelka, R.; Gaba, D.; Chan, J.M.; McKendry, T.; Clear, R.M.; Tittlemier, S.A. Fusarium damage in cereal grains from Western Canada. 1. Phylogenetic analysis of moniliformin-producing Fusarium species and their natural occurrence in mycotoxin-contaminated wheat, oats, and rye. J. Agric. Food Chem. 2013, 61, 5425–5437. [Google Scholar] [CrossRef]
- Pettersson, H.; Brown, C.; Hauk, J.; Hoth, S.; Meyer, J.; Wessels, D. Survey of T-2 and HT-2 toxins by LC-MS/MS in oats and oat products from European oat mills in 2005–2009. Food Addit. Contam. Part B 2011, 4, 110–115. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef]
- Kuzdraliński, A.; Solarska, E.; Mazurkiewicz, J. Mycotoxin content of organic and conventional oats from southeastern Poland. Food Control 2013, 33, 68–72. [Google Scholar] [CrossRef]
- Pleadin, J.; Vasilj, V.; Kudumija, N.; Petrović, D.; Vilušić, M.; Škrivanko, M. Survey of T-2/HT-2 toxins in unprocessed cereals, food and feed coming from Croatia and Bosnia & Herzegovina. Food Chem. 2017, 224, 153–159. [Google Scholar]
- Tittlemier, S.A.; Blagden, R.; Chan, J.; Roscoe, M.; Pleskach, K. A multi-year survey of mycotoxins and ergosterol in Canadian oats. Mycotoxin Res. 2020, 36, 103–114. [Google Scholar] [CrossRef]
- Palumbo, R.; Crisci, A.; Venâncio, A.; Cortiñas Abrahantes, J.; Dorne, J.L.; Battilani, P.; Toscano, P. Occurrence and co-occurrence of mycotoxins in cereal-based feed and food. Microorganisms 2020, 8, 74. [Google Scholar] [CrossRef]
- Polišenská, I.; Jirsa, O.; Vaculová, K.; Pospíchalová, M.; Wawroszova, S.; Frydrych, J. Fusarium mycotoxins in two hulless oat and barley cultivars used for food purposes. Foods 2020, 9, 1037. [Google Scholar] [CrossRef]
- Soleimany, F.; Jinap, S.; Abas, F. Determination of mycotoxins in cereals by liquid chromatography tandem mass spectrometry. Food Chem. 2012, 130, 1055–1060. [Google Scholar] [CrossRef]
- Kos, J.J.; Škrinjar, M.M.; Mandić, A.I.; Mišan, A.Č.; Bursić, V.P.; Šarić, B.M.; Janić-Hajnal, E.P. Presence of aflatoxins in cereals from Serbia. Food Feed Res. 2014, 41, 31–38. [Google Scholar] [CrossRef]
- Li, R.; Wang, X.; Zhou, T.; Yang, D.; Wang, Q.; Zhou, Y. Occurrence of four mycotoxins in cereal and oil products in Yangtze Delta region of China and their food safety risks. Food Control 2014, 35, 117–122. [Google Scholar] [CrossRef]
- Kolakowski, B.; O’Rourke, S.M.; Bietlot, H.P.; Kurz, K.; Aweryn, B. Ochratoxin A concentrations in a variety of grain-based and non–grain-based foods on the Canadian retail market from 2009 to 2014. J. Food Prot. 2016, 79, 2143–2159. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Ibáñez-Vea, M.; Lizarraga, E.; González-Peñas, E.; López de Cerain, A. Co-occurrence of type-A and type-B trichothecenes in barley from a northern region of Spain. Food Control 2012, 25, 81–88. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Madalena, M.; Sobral, C.; Faria, M.A.; Cunha, S.C.; Ferreira, I.M.P.L.V.O. Toxicological interactions between mycotoxins from ubiquitous fungi: Impact on hepatic and intestinal human epithelial cells. Chemosphere 2018, 202, 538–548. [Google Scholar]
- Yang, Y.; Yu, S.; Tan, Y.; Liu, N.; Wu, A. Individual and combined cytotoxic effects of co-occurring deoxynivalenol family mycotoxins on human gastric epithelial cells. Toxins 2017, 9, 96. [Google Scholar] [CrossRef]
- European Commission. Commission Regulation (EC) No 401/2006 of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Off. J. Eur. Union 2006, 70, 12–34. [Google Scholar]
- De Santis, B.; Debegnach, F.; Gregori, E.; Russo, S.; Marchegiani, F.; Moracci, G.; Brera, C. Development of a LC-MS/MS method for the multi-mycotoxin determination in composite cereal-based samples. Toxins 2017, 9, 169. [Google Scholar] [CrossRef] [PubMed]
Mycotoxin 1 | Mean tr (min) | LOD (ng/g) | LOQ (ng/g) | Mean Recovery (%) | Mean RSDr (%) |
---|---|---|---|---|---|
FB1 | 7.66 | 20 | 60 | 90.2 | 5.6 |
FB2 | 9.10 | 14 | 41 | 92.6 | 4.7 |
DON | 2.82 | 6.0 | 18 | 85.3 | 8.1 |
3-ADON | 4.53 | 3.0 | 9 | 86.9 | 5.7 |
ZEA | 8.28 | 9.3 | 28 | 95.8 | 5.9 |
AFB1 | 5.93 | 0.3 | 0.9 | 98.2 | 6.6 |
AFB2 | 5.70 | 0.2 | 0.6 | 100.4 | 5.5 |
AFG1 | 5.35 | 0.7 | 2.1 | 94.6 | 7.3 |
AFG2 | 5.07 | 1.0 | 3.0 | 98.0 | 6.5 |
T2 | 7.72 | 4.0 | 12 | 95.8 | 8.5 |
HT2 | 7.04 | 1.5 | 4.6 | 97.4 | 4.7 |
OTA | 8.46 | 0.6 | 1.8 | 99.5 | 4.8 |
Mycotoxin | No of Samples with Levels <LOD | No of Samples with Levels between LOD and LOQ | No of Samples with Levels ≥LOQ | Range of Levels ≥LOQ (ng/g) | Mean/Median 2 (ng/g) | EU ML (No of Samples Exceeding the EU ML) 3 |
---|---|---|---|---|---|---|
ZEA | 34 | 29 | 37 | 28.1–153 | 39.1/32.6 | 100 (1) |
DON | 66 | 12 | 22 | 19.1–736 | 81.4/30.5 | 1750 (0) |
3-ADON 4 | 96 | 1 | 3 | 9.2–42.6 | 29.9/37.8 | – |
T2 | 74 | 14 | 12 | 12.3–321 | 49.9/16.3 | – |
HT2 | 53 | 11 | 36 | 4.98–439 | 37.1/25.55 | – |
T2 + HT2 | – | – | – | 4.98–760 | 51.8/29.8 | 1000 (0) |
FB1 | 71 | 23 | 6 | 63.2–217.4 | 157.5/194 | – |
FB2 | 89 | 8 | 3 | 42.5–64.0 | 50.6/45.2 | – |
FB1 + FB2 | – | – | – | 70.0–251.4 | 182.8/209.0 | – |
AFB1 | 86 | 9 | 5 | 1.06–1.70 | 1.34/1.28 | 2 (0) |
AFB2 | 86 | 13 | 1 | 0.61 | 0.61/0.61 | – |
AFG1 | 100 | – | – | – | – | – |
AFG2 | 89 | 9 | 2 | 4.5–4.7 | 4.6/4.6 | – |
Sum of AF | – | – | – | 0.61–4.7 | 2.3/1.70 | 4 (2) |
OTA | 96 | 3 | 1 | 2.24 | 2.24/2.24 | 5 (0) |
Year | |||||
---|---|---|---|---|---|
2015 (N 1 = 10) | 2016 (N = 33) | 2017 (N = 31) | 2018 (N = 16) | 2019 (N = 10) | |
Mycotoxin | n 2/Mean/Range 3 | n/Mean/Range | n/Mean/Range | n/Mean/Range | n/Mean/Range |
ZEA | 8/31.6/29.1–34.9 | 13/31.8/28.9–34.8 | 9/58.8/28.1–153 | 4/33.8/31.9–35.5 | 3/39.0/32.8–45.5 |
DON | 1/48.9 | 4/32.2/24.9–48.9 | 12/123.8/19.1–736 | 3/26.6/24.8–29.5 | 2/23.5/21.2–25.8 |
3-ADON | – | – | 3/29.9/9.24–42.65 | – | – |
T2 | – | 3/13.85/12.3–16.3 | 4/103/13.6–321 | 3/15.5/12.9–18.7 | 2/15.4/12.4–18.3 |
HT2 | 1/13.5 | 9/23.3/10.5–34.8 | 11/74.0/5.15–439 | 8/26.1/5.45–40.8 | 7/14.8/4.98–29.3 |
T2 + HT2 | 1/13.5 | 9/26.5/10.5–42.3 | 11/111/5.15–760 | 8/31.9/5.45–59.45 | 7/19.2/4.98–43.4 |
FB1 | 1/217.4 | 2/203.6/200.7–206.4 | 2/128.7/70–187.4 | 1/63.2 | – |
FB2 | – | 1/45.2 | 1/64.0 | 1/42.5 | – |
FB1 + FB2 | 1/217.4 | 2/226.2/200.7–251.6 | 2/160.7/70–251.4 | 1/105.7 | – |
AFB1 | – | – | 2/1.49/1.28–1.70 | 2/1.30/1.06–1.54 | 1/1.12 |
AFB2 | – | – | 1/0.61 | – | – |
AFG2 | – | – | 2/4.6/4.50–4.7 | – | – |
Sum of AF | – | – | 5/2.64/0.61–4.7 | 2/1.30/1.06–1.54 | 1/1.12 |
OTA | – | – | 1/2.24 | – | – |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tarazona, A.; Gómez, J.V.; Mateo, F.; Jiménez, M.; Mateo, E.M. Potential Health Risk Associated with Mycotoxins in Oat Grains Consumed in Spain. Toxins 2021, 13, 421. https://doi.org/10.3390/toxins13060421
Tarazona A, Gómez JV, Mateo F, Jiménez M, Mateo EM. Potential Health Risk Associated with Mycotoxins in Oat Grains Consumed in Spain. Toxins. 2021; 13(6):421. https://doi.org/10.3390/toxins13060421
Chicago/Turabian StyleTarazona, Andrea, José Vicente Gómez, Fernando Mateo, Misericordia Jiménez, and Eva María Mateo. 2021. "Potential Health Risk Associated with Mycotoxins in Oat Grains Consumed in Spain" Toxins 13, no. 6: 421. https://doi.org/10.3390/toxins13060421