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Fusarium Species Infection in Wheat: Impact on Quality and Mycotoxin Accumulation

  • Sofía Noemí ChulzeEmail author
  • Juan Manuel Palazzini
  • Valerie Lullien-Pellerin
  • María Laura Ramirez
  • Martha Cuniberti
  • Naresh Magan
Chapter
  • 32 Downloads

Abstract

Wheat is the most consumed cereal worldwide and can be processed to different products for human consumption. This crop can be infected by Fusarium species, among them those within the Fusarium graminearum complex causing Fusarium head blight (FHB. The disease can severely reduce grain yield and quality under conditions of high humidity and warm temperatures during anthesis. Moreover the grains can be contaminated with mycotoxin such as trichothecenes, among them deoxynivalenol and their acetyl derivates 3-ADON, 15-ADON and DON-3-glucoside. Some years, depending on the environmental conditions Fusarium proliferatum can also infect the grain and fumonisin contamination can be observed. To understand the way of grain infection by Fusarium species will help to undertake strategies to reduce the problem both at pre-harvest and during processing to select adequate procedures to manage mycotoxin production. Different strategies at different stages of the wheat chain have been proposed to reduce the impact of FHB and mycotoxin accumulation.

Keywords

Fusarium head blight Mycotoxins Wheat Preharvest Posharvest Processing.milling Debranning 

References

  1. Abedi-Tizaki M, Zafari DM (2015) Natural occurrence of deoxynivalenol and its acetylated derivatives in wheat in north of Iran. Journal of Plant Pathology 97: 431–437.Google Scholar
  2. Alizadeh A, Braber S, Akbari P, Kraneveld A, Garssen J, Fink-Gremmels J (2016) Deoxynivalenol and its modified forms: are there major differences? Toxins 8: 334.CrossRefGoogle Scholar
  3. Aziz NH, Attia ES, Farag SA (1997) Effect of gamma-irradiation on the natural occurrence of Fusarium mycotoxins in wheat, flour and bread. Nahrung 41: 34–37.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aziz NH, Souzan RM, Azza AS (2006) Effect of gamma-irradiation on the occurrence of pathogenic microorganisms and nutritive value of four principal cereal grains. Applied Radiation and Isotopes 64: 1555–1562.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bahrami N, Bayliss D, Chope G, Penson S, Perehinec T, Fisk ID (2016) Cold plasma: A new technology to modify wheat flour functionality. Food Chemistry 202: 247–253.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bashir K, Swer TL, Prakash KS, Aggarwal M (2017) Physico-chemical and functional properties of gamma irradiated whole wheat flour and starch. LWT - Food Science and Technology 76: 131–139,CrossRefGoogle Scholar
  7. Battilani P, Toscano P, Van der Fels-Klerx HJ, Moretti A, Camardo Leggieri M, Brera C et al. (2016) Aflatoxin B1 contamination in maize in Europe increases due to climate change. Scientific Reports 6: 24328.Google Scholar
  8. Bhat NA, Wani IA, Hamdani AM, Gani A, Masoodi FA (2016) Physicochemical properties of whole wheat flour as affected by gamma irradiation. LWT - Food Science Technology 71: 175–183.CrossRefGoogle Scholar
  9. Brera C, Peduto A, Debegnach F, Pannunzi E, Prantera E, Gregori E et al. (2013) Study of the influence of the milling process on the distribution of deoxynivalenol content from the caryopsis to cooked pasta. Food Control 32: 309–312.CrossRefGoogle Scholar
  10. Bryła M, Ksieniewicz-Woźniak E, Waśkiewicz A, Szymczyk K, Jędrzejczak R (2018) Natural occurrence of nivalenol, deoxynivalenol, and deoxynivalenol-3-glucoside in Polish winter wheat. Toxins, 10: 81.CrossRefGoogle Scholar
  11. Buerstmayr H, Ban T, Anderson JA (2009) QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breeding 128: 1–26.CrossRefGoogle Scholar
  12. Burlakoti RR, Tamburic-Ilincic L, Limay-Rios V, Burlakoti P (2017) Comparative population structure and trichothecene mycotoxin profiling of Fusarium graminearum from corn and wheat in Ontario, central Canada. Plant Pathology 66: 14–27.CrossRefGoogle Scholar
  13. Calado T, Venancio A, Abrunhosa L (2014) Irradiation of mold and mycotoxin control: a review. Comprehensive Reviews in Food Science and Food Safety 13: 1049–1061.Google Scholar
  14. Calori-Domingues MA, Bernardi, CMG, Nardin MS, de Souza GV, dos Santos FGR, Stein M de A et al. (2016). Co-occurrence and distribution of deoxynivalenol, nivalenol and zearalenone in wheat from Brazil. Food Additives and Contaminants Part B, 9: 142–151.CrossRefGoogle Scholar
  15. Camardo Leggieri M, Van Der Fels-Klerx HJ, Battilani P (2013) Cross-validation of predictive models for occurrence of deoxynivalenol in wheat at harvest. World Mycotoxin Journal 6: 389–397.CrossRefGoogle Scholar
  16. Cerón-Bustamante M, Ward, TJ, Kelly A, Vaughan MM, McCormick SP, Cowger C, Leyva-Mir SG et al. (2018). Regional differences in the composition of Fusarium Head Blight pathogens and mycotoxins associated with wheat in Mexico. International Journal of Food Microbiology 273: 11–19.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cheli F, Pinotti L, Rossi L, Dell’Orto V (2013) Effect of milling procedures on mycotoxin distribution in wheat fractions: A review. LWT Food Science and Technology 54: 307–314.CrossRefGoogle Scholar
  18. Chittrakorn S, Earls D, Mac Ritchie F (2014) Ozonation as an alternative to chlorination for soft wheat flours. Journal of Cereal Science 60: 217–221.CrossRefGoogle Scholar
  19. Chulze SN, Palazzini JM, Torres AM, Barros G, Ponsone ML, Geisen R et al. (2015). Biological control as a strategy to reduce the impact of mycotoxins in peanuts, grapes and cereals in Argentina. Food Additives and Contaminants Part A 32: 471–479.CrossRefGoogle Scholar
  20. Cuniberti MB (2001). Fusarium y su efecto en la calidad de trigo. Información para Extensión INTA-EEA Marcos Juárez, Córdoba, Argentina.Google Scholar
  21. Cuniberti MB (2013) Incidencia del Fusarium en la calidad comercial, molinera e industrial del trigo. Campaña 2012/13. INTA-EEA Marcos Juárez, Córdoba, Argentina.Google Scholar
  22. Darsanaki RK, Issazadeh K, Aliabadi MA, Chakoosari MMD (2015) Occurrence of deoxynivalenol (DON) in wheat flours in Guilan Province, northern Iran. Annals of Agricultural and Environmental Medicine 22: 35–37.CrossRefGoogle Scholar
  23. De Nijs M, van den Top H, de Stoppelaar J, Lopez P, Mol H (2016) Fate of enniatins and deoxynivalenol during pasta cooking. Food Chemistry 213: 763–767.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Del Favero G, Woelflingseder L, Braun D, Puntscher H, Kütt M-L, Dellafiora L et al. (2018) Response of intestinal HT-29 cells to the trichothecene mycotoxin deoxynivalenol and its sulfated conjugates. Toxicology Letters 295: 424–437.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Del Ponte, EM, Spolti P, Ward TJ, Gomes LB, Nicolli CP, Kuhnem PR et al. (2014). Regional and field-specific factors affect the composition of Fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology 105: 246–254.CrossRefGoogle Scholar
  26. Delwiche SR, Pearson TC, Brabec DL (2005) High-speed optical sorting of soft wheat for reduction of deoxynivalenol. Plant Disese 89: 1214–1219.CrossRefGoogle Scholar
  27. Desvignes C, Chaurand M, Dubois M, Sadoudi A, Abecassis J, Lullien-Pellerin V (2008) Changes in common wheat grain milling behaviour and tissue mechanical properties following ozone treatment. Journal of Cereal Science 47: 245–251.CrossRefGoogle Scholar
  28. Dexter JE, Clear RM, Preston KR (1996) Fusarium Head Blight: effect on the milling and baking of some Canadian wheats. Cereal Chemistry 73: 695–701.Google Scholar
  29. Dong F, Qiu J, Xu, J, Yu M, Wang, S, Sun Y, Zhang Z, Shi J (2016) Effect of environmental factors on Fusarium population and associated trichothecenes in wheat grain grown in Jiangsu province, China. International Journal of Food Microbiology 230, 58–63.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dubois M, Coste C, Despres AG, Efstathiou T, Nio C, Dumont E, Parent-Massin D (2006) Safety of Oxygreen, an ozone treatment on wheat grains. Part 2. Is there a substantial equivalence between Oxygreen-treated wheat grains and untreated wheat grains? Food Additives and Contaminants 23: 1–15.Google Scholar
  31. Duffeck MR, Tibola CS, Guarienti EM, Del Ponte EM (2017) Survey of mycotoxins in Southern Brazilian wheat and evaluation of immunoassay methods. Scientia Agricola, 74: 343–348.CrossRefGoogle Scholar
  32. European Commission Commission Regulation (EC) (2006) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official. Journal of. European. Communities L364, 5–24.Google Scholar
  33. European Commission EU Directive 2009/128/EC (2009) Sustainable use of pesticides Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2 009 establishing a framework for Community action to achieve the sustainable use of pesticides, OJ L 309, 24.11.2009, p. 71–86.Google Scholar
  34. FDA-United States Food and Drug Administration (2001) Secondary direct food additives permitted in food for human consumption. Federal Register 66: 33829–33830.Google Scholar
  35. Freire L, Sant’Ana A (2018) Modified mycotoxins: An updated review on their formation, detection, occurrence, and toxic effects. Food Chemical Toxicology 111: 189–205.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gaou I, Dubois M, Pfohl-Leszkowicz A, Coste C, De Jouffrey S, Parent-Massin D (2015) Safety of Oxygreen®, an ozone treatment on wheat grains. Part 1- A four week toxicity study in rats by dietary administration of treated wheat. Food Additives and Contaminants 22: 1113–1119.CrossRefGoogle Scholar
  38. Garcia-Cela E, Kiaitsi E, Medina A, Sulyok M, Krska R, Magan N (2018a) Interacting environmental stress factors affects targeted metabolomic profiles in stored natural wheat and that inoculated with F. graminearum. Toxins 10: 56.CrossRefGoogle Scholar
  39. Garcia-Cela E, Kiaitsi E, Sulyok M, Medina A, Magan N (2018b) Fusarium graminearum in stored wheat: use of CO2 production to quantify dry matter losses and relate these to relative risks of Zearalenone contamination under different interacting environmental conditions. Toxins 10, 86.CrossRefGoogle Scholar
  40. Gärtner BH, Munich M, Kleijer G, Mascher F (2008) Characterization of kernel resistance against Fusarium infection in spring wheat by baking quality and mycotoxin assessments. European Journal of Plant Pathology, 120: 61–68.CrossRefGoogle Scholar
  41. Gerenotti S, Cirlini M, Sarkanj B, Sulyok M, Berthiller F, Dall’Asta C, Suman M (2017) Formulation and processing factors affecting trichothecene mycotoxins within industrial biscuit-making. Food Chemistry 229: 597–603.CrossRefGoogle Scholar
  42. Giménez I, Herrera M, Escobar J, Ferruz E, Lorán S, Herrera A, Ariño A (2013) Distribution of deoxynivalenol and zearalenone in milled germ during wheat milling and analysis of toxin levels in wheat germ and wheat germ oil. Food Control 34: 268–273.CrossRefGoogle Scholar
  43. Giroux ME, Bourgeois G, Dion Y, Rioux S, Pageau D, Zoghlami S et al. (2016) Evaluation of forecasting models for fusarium head blight of wheat under growing conditions of Quebec, Canada. Plant Disease 100: 1192–1201.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Gorczyca A, Oleksy A, Gala-Czekaj D, Urbaniak M, Laskowska M, Waśkiewicz A, Stępień Ł (2017) Fusarium head blight incidence and mycotoxin accumulation in three durum wheat cultivars in relation to sowing date and density. The Science of Nature, 105: 1–2.Google Scholar
  45. Goze P, Rhazi L, Lakhal L, Jacolot P, Pauss A, Aussenac T (2017) Effects of ozone treatment on the molecular properties of wheat grain proteins. Journal of Cereal Science 75: 243–251.CrossRefGoogle Scholar
  46. Goze P, Rhazi L, Pauss A, Aussenac T (2016) Starch characterization after ozone treatment of wheat grains. Journal of Cereal Science 70: 207–213.CrossRefGoogle Scholar
  47. Graham DM (1997) Use of ozone for food processing. Food Technology 51: 72–75.Google Scholar
  48. Hofgaard IS, Aamot HU, Torp T, Jestoi M, Lattanzio VMT, Klemsdal SS et al. (2016) Associations between Fusarium species and mycotoxins in oats and spring wheat from farmers’ fields in Norway over a six-year period. World Mycotoxin Journal 9: 365–378.CrossRefGoogle Scholar
  49. Hojnik N, Cvelbar U, Tavcar-Kalcher G, Walsh JL, Krizaj I (2017) Mycotoxin Decontamination of Food: Cold Atmospheric Pressure Plasma versus “Classic” Decontamination. Toxins 9: 151.CrossRefGoogle Scholar
  50. Hollingsworth CR, Motteberg CD, Wiersma JV, Atkinson LM (2008) Agronomic and economic responses of spring wheat to management of Fusarium head blight. Plant Disease 92: 1339–1348.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hope R and Magan N (2003) Two dimensional environmental profiles of growth, deoxynivalenol and nivalenol production by Fusarium culmorum on a wheat-based substrate. Letters Applied Microbiology. 37: 70–74.CrossRefGoogle Scholar
  52. Hope R, Aldred D, Magan N (2005) Comparison of the effect of environmental factors on deoxynivalenol production by F. culmorum and F. graminearum on wheat grain. Letters Applied Microbiology 40: 295–300.Google Scholar
  53. Hu Y, Wang L, Hong Z, Li Z (2017a) Superheated steam treatment improved flour qualities of wheat in suitable conditions. Journal of Food Processing and Preservation 41: e13238.CrossRefGoogle Scholar
  54. Hu Y, Wang L, Hong Z, Li Z (2017b) Modification of protein structure and dough rheological properties of wheat flour through superheated steam treatment Journal of Cereal Science 76: 222–228.CrossRefGoogle Scholar
  55. Jaillais B, Roumet P, Pinson-Gadais L, Bertrand D (2015) Detection of Fusarium head blight contamination in wheat kernels by multivariate imaging. Food Control 54: 250–258.CrossRefGoogle Scholar
  56. Janaviciene S, Mankeviciene A, Suproniene S, Kochiieru Y, Keriene I (2018) The prevalence of deoxynivalenol and its derivatives in the spring wheat grain from different agricultural production systems in Lithuania. Food Additives and Contaminants Part A, 35: 1179–1188.CrossRefGoogle Scholar
  57. Juan C, Covarelli L, Beccari G, Colasante V, Mañes J (2016) Simultaneous analysis of twenty-six mycotoxins in durum wheat grain from Italy. Food Control, 62: 322–329.CrossRefGoogle Scholar
  58. Kamimura H, Nishijima M, Saito K, Yasuda K, Ibe A, Nagyama T, Ushiyama H, Naoi Y (1979) The decomposition of trichothecene mycotoxins during food processing. Studies on mycotoxins in foods. XII. Journal of the Food Hygienic Society of Japan 20: 352–357.CrossRefGoogle Scholar
  59. Khaneghah AM, Fakhri Y, Sant’Ana A (2018) Impact of unit operations during processing of cereal-based products on the levels of deoxynivalenol, total aflatoxin, ochratoxin A and zearalenone: A systematic review and meta-analysis. Food Chemistry 268: 611–624.CrossRefGoogle Scholar
  60. Kirinčič S, Škrjanc B, Kos N, Kozolc B, Pirnat N, Tavčar-Kalcher G (2015) Mycotoxins in cereals and cereal products in Slovenia – Official control of foods in the years 2008–2012. Food Control, 50: 157–165.CrossRefGoogle Scholar
  61. Kostelanska M, Dzuman Z, Malachova A, Capouchova I, Prokinova E, Skerikova A et al. (2011) Effects of milling and baking technologies on levels of deoxynivalenol and its masked form deoxynivalenol-3-glucoside. Journal of Agricultural Food Chemistry 59: 9303–9312.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Laca A, Mousia Z, Diaz M, Webb C, Pandiella SS (2006) Distribution of microbial contamination within cereal grain Journal of Food Engineering 72: 332–338.CrossRefGoogle Scholar
  63. Lacko-Bartošová M, Remža J, Lacko-Bartošová L (2017) Fusarium mycotoxin contamination and co-occurrence in Slovak winter wheat grains. Zemdirbyste- Agriculture 104: 173–178.CrossRefGoogle Scholar
  64. Lamacchia C, Landriscina L, D’Agnello P (2016) Changes in wheat kernel proteins induced by microwave treatment. Food Chemistry 197: 634–640.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Li M, Peng J, Zhu K-X, Guo X-N, Zhang M, Peng W, Zhou H-M (2013) Delineating the microbial and physical–chemical changes during storage of ozone treated wheat flour. Innovative Food Science & Emerging Technologies 20: 223–229.CrossRefGoogle Scholar
  66. Li MM, Guan EQ, Bian K (2015a) Effect of ozone treatment on deoxynivalenol and quality evaluation of ozonised wheat. Food Addititives and Contaminants: Part A 32: 544–553.CrossRefGoogle Scholar
  67. Li X, Shin S, Heinen S, Dill-Macky R, Berthiller F, Nersesian N et al. (2015b) Transgenic wheat expressing a barley UDP-glucosyltransferase detoxifies deoxynivalenol and provides high levels of resistance to Fusarium graminearum. Molecular Plant-Microbe Interactions 28: 1237–1246.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Los A, Ziuzina D, Bourke P (2018) Current and future technologies for microbiological decontamination of cereal grains. Journal of Food Science 83: 1484–1493.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Lullien-Pellerin V (2012) Ozone in grain processing. In O’Donnell C, Tiwari B K, Cullen P J, Rice R G (ed) Ozone in Food Processing. Wiley-Blackwell, p 81–102.Google Scholar
  70. Madgewick J, West JS, White R, Semenov M, Townsend JA, Turner JA et al. (2011). Future threat: direct impact of climate change on wheat Fusarium ear blight in the UK. European Journal of Plant Pathology 130: 117–131.CrossRefGoogle Scholar
  71. Machado LV, Mallmann CA, Mallmann AO, Coelho RD, Copetti, MV (2017). Deoxynivalenol in wheat and wheat products from a harvest affected by Fusarium head blight. Food Science and Technology 37: 8–12.CrossRefGoogle Scholar
  72. Magan N. and Medina A (2016) Integrating gene expression, ecology and mycotoxin production by Fusarium and Aspergillus species in relation to interacting environmental factors. World Mycotoxin Journal 9: 863–874.CrossRefGoogle Scholar
  73. Magan N, Aldred D, Baxter ES (2014) Mycotoxin Reduction in Grain Chains. Leslie, J. F. and Logrieco, A.F (Eds) John Wiley & Sons, Ltd, Chichester, UK pp. 258–267.Google Scholar
  74. Magan N, Aldred D, Mylona K, Lambert RJW (2010) Limiting mycotoxins in stored wheat. Food Additives and Contaminants Part A 27: 644–650.CrossRefGoogle Scholar
  75. Mallmann CA, Dilkin P, Mallmann AO, Oliveira MS, Adaniya ZNC, Tonini C (2017) Prevalence and levels of deoxynivalenol and zearalenone in commercial barley and wheat grain produced in Southern Brazil: an eight-year (2008 to 2015) summary. Tropical Plant Pathology 42: 146–152.CrossRefGoogle Scholar
  76. Martinez M, Castañares E, Dinolfo MI, Pacheco W, Moreno MV and Stenglein SA (2014) Presencia de Fusarium graminearum en muestras de trigo destinado al consumo humano. Revista Argentina de Microbiologia 46: 41–44.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Mayer-Laigle C, Barakat A, Barron C, Delenne J-Y, Frank X, Mabille F, Rouau X et al. (2018) DRY biorefineries: Multiscale modeling studies and innovative processing. Innovative Food Science and Emerging Technology 46: 131–139.CrossRefGoogle Scholar
  78. McMullen M, Bergstrom G, De Wolf E, Dill-Macky R, Hershman D, Shaner G et al. (2012) a unified effort to fight an enemy of wheat and barley: Fusarium Head Blight. Plant Disease 96: 1712–1728.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Medina A, Akbar A, Baazeem A, Rodriguez A, Magan N (2017) Climate change, food security and mycotoxins: do we know enough? Fungal Biology Reviews 31: 143–154.CrossRefGoogle Scholar
  80. Medina A, Rodríguez A, Magan N (2015) Climate change and mycotoxigenic fungi: Impacts on mycotoxin production. Current Opinion in Food Science 5: 99–104.CrossRefGoogle Scholar
  81. Mei J, Liu G, Huang X, Ding W (2016) Effects of ozone treatment on medium hard wheat (Triticum aestivum L.) flour quality and performance in steamed bread making. CyTA Journal of Food 14: 449–456.Google Scholar
  82. Mesterházy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breeding 114: 377–386.CrossRefGoogle Scholar
  83. Mesterházy Á, Tóth B, Varga M, Bartók T, Szabó-Hevér Á, Farády L, Lehoczki-Krsjak S (2011). Role of fungicides, application of nozzle types, and the resistance level of wheat varieties in the control of Fusarium head blight and deoxynivalenol. Toxins 3: 1453–1483.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Moschini RC, Fortugno C (1996) Predicting wheat head blight incidence using models based on meteorological factors in Pergamino, Argentina. European Journal of Plant Pathology 102: 211–218.CrossRefGoogle Scholar
  85. Moschini RC, Martínez MI, Sepulcri MG (2013) Alconada Magliano, TM and Chulze, SN (Eds.). Fusarium head blight in Latin America. Springer Netherlands, The Netherlands pp. 205–227.Google Scholar
  86. Mylona K, Sulyok M, Magan N (2012). Fusarium graminearum and Fusarium verticillioides colonisation of wheat and maize, environmental factors, dry matter losses and mycotoxin production relevant to the EU legislative limits. Food Additives and Contaminants 29: 1118–1128.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Neira MS, Pacin AM, Martinez EJ, Molto G, Resnik SL (1997) The effects of bakery processing on natural deoxynivalenol contamination. International Journal of Food Microbiology 37: 21–25.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Nowicki TW, Gaba DG, Dexter JE, Matsuo RR, Clear RM (1988) Retention of Fusarium mycotoxin deoxynivalenol in wheat during processing and cooking of spaghetti and noodles. Journal of Cereal Science 8: 189–202.CrossRefGoogle Scholar
  89. Obadi M, Zhu K-X, Peng W, Sulieman AA, Mohammed K, Zhou H-M (2018) Effects of ozone treatment on the physicochemical and functional properties of whole grain flour. Journal of Cereal Science 81: 127–132.CrossRefGoogle Scholar
  90. Ostry V, Malir F, Toman J, Grosse Y (2017) Mycotoxins as human carcinogens-the IARC Monographs classification. Mycotoxin Research 33: 65–73.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Palacios SA, Erazo JG, Ciasca B, Lattanzio VMT, Reynoso MM, Farnochi MC et al. (2017). Occurrence of deoxynivalenol and deoxynivalenol-3-glucoside in durum wheat from Argentina. Food Chemistry 230: 728–734.CrossRefPubMedPubMedCentralGoogle Scholar
  92. Palazzini J, Fumero V, Yerkovich N, Barros G, Cuniberti M, Chulze S (2015) Correlation between Fusarium graminearum and deoxynivalenol during the 2012/13 wheat Fusarium Head Blight outbreak in Argentina. Cereal Research Communication 43: 627–637.CrossRefGoogle Scholar
  93. Palazzini J, Roncallo P, Cantoro R, Chiotta M, Yerkovich N, Palacios S, Echenique V, Torres A, Ramirez M, Karlovsky P, Chulze S (2018) Biocontrol of Fusarium graminearum sensu stricto, reduction of deoxynivalenol accumulation and phytohormone induction by two selected antagonists. Toxins 10, 88.CrossRefGoogle Scholar
  94. Palazzini JM, Alberione E, Torres A, Donat C, Kohl J, Chulze S (2016). Biological control of Fusarium gramienarum sensu stricto causal agent of Fusarium head blight of wheat, using formualted antagonists under field conditions in Argentina. Biological Control 94: 56–61.CrossRefGoogle Scholar
  95. Palazzini JM, Groenenboom-de Haas BH, Torres AM, Köhl J, Chulze SN (2013) Biocontrol and population dynamics of Fusarium spp. on wheat stubble in Argentina. Plant Pathology 62: 859–866.CrossRefGoogle Scholar
  96. Palazzini JM., Ramirez ML, Torres AM, Chulze SN (2007) Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat. Crop Protection 26: 1702–1710.CrossRefGoogle Scholar
  97. Pascale M, Haidukowski M, Lattanzio VMT, Silvestri M, Ranieri R, Visconti A (2011) Distribution of T-2 and HT-2 toxins in milling fractions of durum wheat. Journal of Food Protection 74: 1700–1707.CrossRefPubMedPubMedCentralGoogle Scholar
  98. Paul PA, Lipps PE, Hershman DE, McMullen MP, Draper MA, Madden LV (2008) Efficacy of triazole-based fungicides for fusarium head blight and deoxynivalenol control in wheat: a multivariate meta-analysis. Phytopathology 98: 999–1011.CrossRefPubMedPubMedCentralGoogle Scholar
  99. Peyron S, Abecassis J, Autran J-C, Rouau X (2002) Influence of UV exposure on phenolic acid content, mechanical properties of bran, and milling behavior of durum wheat (Triticum durum Desf.). Cereal Chemistry 79: 726–731.CrossRefGoogle Scholar
  100. Pleadin J, Staver MM, Markov K, Frece J, Zadravec M, Jaki V et al. (2017) Mycotoxins in organic and conventional cereals and cereal products grown and marketed in Croatia. Mycotoxin Research 33: 219–227.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Popovic V, Fairbanks N, Pierscianowski J, Biancaniello M, Zhou T, Koutchma T (2018) Feasibility of 3D UV-C treatment to reduce fungal growth and mycotoxin loads on maize and wheat kernels. Mycotoxin Research 34: 211–221.CrossRefPubMedPubMedCentralGoogle Scholar
  102. Prandini A, Sigolo S, Filippi L, Battilani P, Piva G (2009) Review of predictive models for Fusarium head blight and related mycotoxin contamination in wheat. Food and Chemistry Toxicology 47: 927–931.CrossRefGoogle Scholar
  103. Prange A, Birzele B, Krämer J, Meier, A, Modrow H, Köhler P (2005) Fusarium-inoculated wheat: deoxynivalenol contents and baking Quality in relation to infection time. Food Control, 16: 739–745.CrossRefGoogle Scholar
  104. Prat N, Gilbert C, Prah U, Wachter E, Steiner B, Langin T et al. (2017) QTL mapping of Fusarium Head blight resistance in three related durum wheat populations. Theoretical and applied genetics, 130: 13–27.CrossRefPubMedPubMedCentralGoogle Scholar
  105. Preston KR, Kilborn RH, Black HC (1982) The GRL Pilot Mill. II. Physical dough and baking properties of flour streams milled from Canadian red spring wheats. Canadian Institute of Food Science and Technology Journal 15: 29.CrossRefGoogle Scholar
  106. Pronyk C, Cenkowski S, Abramson D (2006) Superheated steam reduction of deoxynivalenol in naturally contaminated wheat kernels. Food Control 17: 789–796.CrossRefGoogle Scholar
  107. Purahong W, Nipoti P, Pisi A, Lemmens M, Prodi A (2014) Aggressiveness of different Fusarium graminearum chemotypes within a population from Northern-Central Italy. Mycoscience 55: 63–69.CrossRefGoogle Scholar
  108. Ramirez ML, Reynoso MM, Farnochi, Sofia MC, Chulze S (2006) Vegetative compatibility and mycotoxin chemotypes among Fusarium graminearum (Gibberella zeae) isolates from wheat in Argentina European Journal of Plant Pathology 115: 139–148.Google Scholar
  109. Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, Ando K et al. (2016) Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nature Genetics 48: 1576–1580.CrossRefPubMedPubMedCentralGoogle Scholar
  110. Rios G, Pinson-Gadais L, Abecassis J, Zakhia-Rozis N, Lullien-Pellerin V (2009a) Assessment of dehulling efficiency to reduce deoxynivalenol and Fusarium level in durum wheat grains. Journal of Cereal Science 49: 387–392.CrossRefGoogle Scholar
  111. Rios G, Zakhia N, Abecassis J, Chaurand M, Samson M-F, Richard-Forget F, Lullien-Pellerin V (2007) Impact des opérations de transformation sur la répartition du DON dans les produits de fractionnement du blé dur. In Colloque Scientifique « Mycotoxines Fusariennes des Céréales », Arcachon, FRA, (2007-09-11 - 2007-09-13).Google Scholar
  112. Rios G, Zakhia-Rozis N, Chaurand M, Richard-Forget F, Samson MF, Abecassis J, Lullien-Pellerin V (2009b) Impact of durum wheat milling on deoxynivalenol distribution in the outcoming fractions. Food Additives & Contaminants Part A, 26: 487–495CrossRefGoogle Scholar
  113. Rossi V, Caffi T, Salinari F (2012) Helping farmers face the increasing complexity of decision-making for crop protection. Phytopathologia Mediterranea 51: 457–479.Google Scholar
  114. Rossi V, Giosuè S, Pattori E, Spanna F, Del Vecchio AA (2003). A model estimating the risk of Fusarium head blight on wheat. EPPO Bulletin 33: 421–425.Google Scholar
  115. Sadhasivam S, Britzi M, Zakin V, Kostyukovsky M, Trostanetsky A, Quinn E, Sionov E (2017) Rapid detection and identification of mycotoxigenic fungi and mycotoxins in stored wheat grain. Toxins 9, 302.CrossRefGoogle Scholar
  116. Sandhu HPS, Manthey FA, Simsek S (2011) Quality of bread made from ozonated wheat (Triticum aestivum L.) flour. Journal of the Science of Food and Agriculture 91: 1576–1584.CrossRefPubMedPubMedCentralGoogle Scholar
  117. Sarrocco S, Vannacci G (2018) Preharvest application of beneficial fungi as a strategy to prevent postharvest mycotoxin contamination: A review. Crop Protection 110: 160–170.CrossRefGoogle Scholar
  118. Sarver BAJ, Ward TJ, Gale LR, Broz K, Kistler HC, Aoki T, Nicholson P et al. (2011). Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genetic Biology 48: 1096–1107.CrossRefGoogle Scholar
  119. Schaafsma AW, Hooker DC (2005) Validation of the Doncast prediction tool in wheat across France and Uruguay. In: Canty, S.M., Boring, T., Wardwell, J., Siler, L. and Ward, R.W (Eds.), Proceedings of the National Fusarium Head Blight Forum. December 11-13, 2005. Milwaukee, Wisconsin: Michigan State University, pp. 148.Google Scholar
  120. Schaarschmidt S, Fauhl-Hassek C (2018) The fate of mycotoxins during the processing of wheat for human consumption. Comprehensive Reviews on Food Science and Food Safety 17: 556–593.CrossRefGoogle Scholar
  121. Schisler DA, Khan NI, Boehm MJ, Lipps PE, Slininger PJ, Zhang S (2006) Selection and evaluation of the potential of choline-metabolizing microbial strains to reduce Fusarium head blight. Biological Control 39: 497–506.CrossRefGoogle Scholar
  122. Schmale DG, Wood-Jones AK, Cowger C, Bergstrom GC, Arellano C (2011) Trichothecene genotypes of Gibberella zeae from winter wheat fields in the eastern USA. Plant Pathology 60: 909–917.CrossRefGoogle Scholar
  123. Scudamore KA, Banks J, MacDonald SJ (2003) Fate of ochratoxin A in the processing of whole wheat grains during milling and bread production. Food Additives & Contaminants 20: 1153–1163.CrossRefGoogle Scholar
  124. Serrano AB, Font G, Manes J, Ferrer E (2016) Development a mitigation strategy of enniatins in pasta under home-cooking conditions. LWT Food Science and Technology 65: 1017–1024.CrossRefGoogle Scholar
  125. Serranti S, Cesare D, Bonifazi G (2013) The development of a hyperspectral imaging method for the detection of Fusarium-damaged, yellow berry and vitreous Italian durum wheat kernels. Biosystems Engineering 115: 20–30.CrossRefGoogle Scholar
  126. Shala-Mayrhofer V, Marjakaj R, Varga E, Berthiller F, Musolli A, Lemmens M (2015) Occurrence of Fusarium head blight and mycotoxins as well as morphological identification o Fusarium species in winter wheat in Kosovo. Cereal Research Communication 43: 438–448.CrossRefGoogle Scholar
  127. Sovrani V, Blandino M, Scarpino V, Reyneri A, Coïsson JD, Travaglia F et al. (2012) Bioactive compound content, antioxidant activity, deoxynivalenol and heavy metal contamination of pearled wheat fractions. Food Chemistry 135: 39–46.CrossRefGoogle Scholar
  128. Stanciu O, Juan C, Miere D, Dumitrescu A, Bodoki E, Loghin F, Mañes J (2017) Climatic conditions influence emerging mycotoxin presence in wheat grown in Romania – A 2-year survey. Crop Protection 100: 124–133.CrossRefGoogle Scholar
  129. Suga H, Karugia GW, Ward T, Gale LR, Tomimura K, Nakajima T et al. (2008). Molecular Characterization of the Fusarium graminearum Species Complex in Japan. Phytopathology 98, 159–166.CrossRefPubMedPubMedCentralGoogle Scholar
  130. Sugita-Konishi Y, Park BJ, Kobayashi-Hattori K, Tanaka T, Chonan T, Yoshikawas K, Kumagai S, (2006) Effect of cooking process on the deoxynivalenol content and its subsequent cytotoxicity in wheat products. Bioscience, Biotechnology, and Biochemistry 70: 1764–1768.CrossRefPubMedPubMedCentralGoogle Scholar
  131. Sumíková T, Chrpová J, Džuman Z, Salava J, Štěrbová L, Palicová J, Slavíková P et al. (2017) Mycotoxins content and its association with changing patterns of Fusarium pathogens in wheat in the Czech Republic. World Mycotoxin Journal 10: 143–151.CrossRefGoogle Scholar
  132. Tibola CS, Fernandes JMC, Guarienti EM (2016) Effect of cleaning, sorting and milling processes in wheat mycotoxin content. Food Control 60: 174–179.CrossRefGoogle Scholar
  133. Tima H, Berkics, A, Hannig Z, Ittzés A, Kecskésné Nagy E, Mohácsi-Farkas C, Kiskó G (2017) Deoxynivalenol in wheat, maize, wheat flour and pasta: surveys in Hungary in 2008–2015. Food Additives and Contaminants Part B, 11: 37–42.CrossRefGoogle Scholar
  134. Tiwari BK, Brennan CS, Curran T, Gallagher E, Cullen PJ, O’Donnell CP (2010) Application of ozone in grain processing. Journal of Cereal Science. 51: 248–255.CrossRefGoogle Scholar
  135. Tkachuk R, Dexter JE, Tipples KH, Nowicki TW (1991) Removal by specific gravity table of tombstone kernels and associated trichothecenes from wheat infected with Fusarium Head Blight. Cereal Chemistry 68: 428–431.Google Scholar
  136. Tralamazza SM, Bemvenuti RH, Zorzete P, de Souza Garcia F, Corrêa B (2016) Fungal diversity and natural occurrence of deoxynivalenol and zearalenone in freshly harvested wheat grains from Brazil. Food Chemistry 196: 445–450.CrossRefPubMedPubMedCentralGoogle Scholar
  137. Trenholm HL, Charmley LL, Prelusky DB, Warner RM (1991) Two physical methods for the decontamination of four cereals contaminated with deoxynivalenol and zearalenone. Journal of Agricultural and Food Chemistry 39: 356–360.CrossRefGoogle Scholar
  138. Trombete F, Barros A, Vieira M, Saldanha T, Venâncio A, Fraga M, (2016a) Simultaneous determination of deoxynivalenol, deoxynivalenol-3-glucoside and nivalenol in wheat grains by HPLC-PDA with immunoaffinity column cleanup. Food Analytical Methods 9: 2579–2586.Google Scholar
  139. Trombete F, Minguita A, Porto Y, Freitas-Silva O, Freitas-Sa D et al. (2016b) Chemical, Technological, and sensory properties of wheat grains (Triticum aestivum L) as affected by gaseous ozonation. International Journal of Food Properties 19: 2739–2749.CrossRefGoogle Scholar
  140. Umpiérrez-Failache M, Garmendia G, Pereyra S, Rodríguez-Haralambides A, Ward TJ, Vero S (2013). Regional differences in species composition and toxigenic potential among Fusarium head blight isolates from Uruguay indicate a risk of nivalenol contamination in new wheat production areas. International Journal of Food Microbiology 166: 135–140.CrossRefPubMedPubMedCentralGoogle Scholar
  141. 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 Chemistry 136: 750–757.CrossRefPubMedPubMedCentralGoogle Scholar
  142. Valle-Algarra FM, Mateo EM, Medina A, Mateo F, Gimeno-Adelantado JV, Jimenez M (2009) Changes in ochratoxin A and type B trichotecenes contained in wheat flour during dough fermentation and bread-baking. Food Additives and Contaminants Part A 26: 896–906.CrossRefGoogle Scholar
  143. Van der Fels-Klerx HJ, Liu C, Battilani P (2016) Modelling climate change impacts on mycotoxin contamination. World Mycotoxin Journal 9: 717–726.CrossRefGoogle Scholar
  144. Van der Lee T, Zhang H, van Diepeningen A. Waalwijk C (2015) Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Additives and Contaminants Part A 32: 453–460.CrossRefGoogle Scholar
  145. Váry Z, Mullins E, Mcelwain JC, Doohan FM (2015) The severity of wheat diseases increases when plants and pathogens are acclimatized to elevated carbon dioxide. Global Change Biology 21: 2661–2669.CrossRefPubMedPubMedCentralGoogle Scholar
  146. Vidal A, Bendicho J, Sanchis V, Ramos AJ, Marín S (2016) Stability and kinetics of leaching of deoxynivalenol, deoxynivalenol-3-glucoside and ochratoxin A during boiling of wheat spaghettis. Food Research International 85: 182–190CrossRefPubMedPubMedCentralGoogle Scholar
  147. Violleau F, Pernot AG, Surel O (2012) Effect of Oxygreen wheat ozonation process on bread dough quality and protein solubility. Journal of Cereal Science 55: 115–124.CrossRefGoogle Scholar
  148. Visconti A, Haidukowski EM, Pascale M, Silvestri M (2004) Reduction of deoxynivalenol during durum wheat processing and spaghetti cooking. Toxicology Letters 153: 181–189.CrossRefPubMedPubMedCentralGoogle Scholar
  149. Vogelgsang S, Musa T, Bänziger I, Kägi A, Bucheli TD, Wettstein FE et al. (2017). Fusarium mycotoxins in Swiss wheat: a survey of growers’ samples between 2007 and 2014 shows strong year and minor geographic effects. Toxins 9: 246.CrossRefGoogle Scholar
  150. Wang J, Yu Y (2009) Effect of gamma-ray irradiation on the physicochemical properties of flour and starch granule structure for wheat. International Journal of Food Science and Technology 44: 674–680.CrossRefGoogle Scholar
  151. Wang L, Luo Y, Luo X, Wang R, Li Y, Li Y et al. (2016b) Effect of deoxynivalenol detoxification by ozone treatment in wheat grains. Food Control 66: 137–144.CrossRefGoogle Scholar
  152. Wang L, Shao, H, Luo X, Wang R, Li Y, Li Y, Luo Y, Chen Z (2016a). Effect of ozone treatment on deoxynivalenol and wheat quality. Plos One 11, e0147613.CrossRefPubMedPubMedCentralGoogle Scholar
  153. Wang L, Wang Y, Shao HL, Luo XH, Wang, R, Li YF, Li YN et al. (2017) In vivo toxicity assessment of deoxynivalenol-contaminated wheat after ozone degradation. Food Additives and Contaminants Part A 34: 103–112.CrossRefGoogle Scholar
  154. Ward TJ, Clear RM, Rooney A, O’Donnell K, Gaba D, Patrick S 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 Genetic Biology 45: 473–484.CrossRefGoogle Scholar
  155. Wegulo SN, Baenziger PS, Hernandez J, Bockus WW, Hallen-Adams H (2015) Management of Fusarium head blight of wheat and barley. Crop Protection 73: 100–107.CrossRefGoogle Scholar
  156. West JS, Holdgate S, Townsend JA, Edwards SG, Jennings P, Fitt BDL (2012) Impacts of changing climate and agronomic factors on Fusarium ear blight in the UK. Fungal Ecology 5: 53–61.CrossRefGoogle Scholar
  157. Whitney K (2018) Fate of deoxynivalenol and deoxynivalenol-3-b-d-glucopyranoside during wheat processing. 4th ICC Latin American Cereals Conference -LACC4- and International Gluten Wheat Seminary -IGW-, pp. 68. 11–14 March, Mexico City, Mexico.Google Scholar
  158. Wu J, Doan H, Cuenca MA (2006) Investigation of gaseous ozone as an anti-fungal fumigant for stored wheat. Journal of Chemical Technology and Biotechnology 81: 1288–1293.CrossRefGoogle Scholar
  159. Xue AG, Chen Y, Voldeng HD, Fedak G, Savard ME, Längle T et al. (2014) Concentration and cultivar effects on efficacy of CLO-1 biofungicide in controlling Fusarium Head Blight of wheat. Biological Control 73: 2–7.CrossRefGoogle Scholar
  160. Yerkovich N, Palazzini JM, Sulyok M, Chulze SN (2017) Trichothecene genotypes, chemotypes and zearalenone production by Fusarium graminearum species complex strains causing Fusarium head blight in Argentina during an epidemic and non-epidemic season. Tropical Plant Pathology 42: 190–196.CrossRefGoogle Scholar
  161. Yoshinari T, Suzuki Y, Sugita-Konishi Y, Ohnishi T, Terajima J (2016) 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 Additives and Contaminants Part A, 33: 1620–1626.CrossRefGoogle Scholar
  162. Zachariasova M, Vaclavikova M, Lacina O, Vaclavik L, Hajslova J (2012) Deoxynivalenol oligoglycosides: new “masked” Fusarium toxins occurring in malt, beer, and breadstuff. Journal of Agricultural and Food Chemistry 60: 9280–9291.CrossRefPubMedPubMedCentralGoogle Scholar
  163. Zhang H, Van der Lee T, Waalwijk C, Chen W, Xu J, Xu J et al. (2012). Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PloS one 7: e31722.CrossRefPubMedPubMedCentralGoogle Scholar
  164. Zhao X, Wei Y, Wang Z, Zhang B, Chen F, Zhang P (2011) Mechanochemistry in thermomechanical processing of foods: kinetic aspects. Journal of Food Science 76: R134-R142.CrossRefPubMedPubMedCentralGoogle Scholar
  165. Zhao Y, Guan X, Zong Y, Hua X, Xing F, Wang Y et al. (2018). Deoxynivalenol in wheat from the Northwestern region in China. Food Additives and Contaminants Part B, 1–5.Google Scholar
  166. Zhu F (2018) Effect of ozone treatment on the quality of grain products. Food Chemistry 264: 358–366.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Sofía Noemí Chulze
    • 1
    Email author
  • Juan Manuel Palazzini
    • 1
  • Valerie Lullien-Pellerin
    • 2
  • María Laura Ramirez
    • 1
  • Martha Cuniberti
    • 3
  • Naresh Magan
    • 4
  1. 1.Research Institute on Mycology and Mycotoxicology (IMICO)The National Scientific and Technical Research Council (CONICET)-National University of Río Cuarto (UNRC)CórdobaArgentina
  2. 2.IATE, CIRAD, INRAE, Montpellier SupAgro, University MontpellierMontpellierFrance
  3. 3.Wheat and Soybean Quality LabNational Institute of Agricultural Research, INTACórdobaArgentina
  4. 4.Cranfield UniversityCranfieldUK

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