Abstract
Deoxynivalenol (DON), the most commonly occurring trichothecene in nature, may affect animal and human health through causing diarrhea, vomiting, gastrointestinal inflammation, and immunomodulation. DON-3-glucoside (DON-3G) as a major plant metabolite of the mycotoxin is another “emerging” food safety issue in recent years. Humans may experience potential health risks by consuming DON-contaminated food products. Thus, it is crucial for human and animal health to study also the degradation of DON and DON-3G during thermal food processing. Baking, boiling, steaming, frying, and extrusion cooking are commonly used during thermal food processing and have promising effects on the reduction of mycotoxins in food. For DON, however, the observed effects of these methods, as reported in numerous studies, are ambiguous and do not present a clear picture with regard to reduction or transformation. This review summarized the influence of thermal processing on the stability of DON and the formation of degradation/conversion products. Besides this, also a release of DON and DON-3G from food matrix as well as the release of DON from DON-3G during processing is discussed. In addition, some conflicting findings as reported from the studies on thermal processing as well as cause-effect relationships of the different thermal procedures are explored. Finally, the potential toxic profiles of DON degradation products are discussed as well when data are available.
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References
Abbas HK, Mirocha CJ, Pawlosky RJ, Pusch DJ (1985) Effect of cleaning, milling, and baking on deoxynivalenol in wheat. Appl Environ Microbiol 50:482–486
Abbas HK, Mirocha CJ, Rosiles R, Carvajal M (1988) Decomposition of zearalenone and deoxynivalenol in the process of making tortillas from corn. Cereal Chem 65:15–19
Accerbi M, Rinaldi VEA, Ng PK (1999) Utilization of highly deoxynivalenol-contaminated wheat via extrusion processing. J Food Protect 62:1485–1487
Ali N, Blaszkewicz M, Al Nahid A, Rahman M, Degen GH (2015) Deoxynivalenol exposure assessment for pregnant women in Bangladesh. Toxins 7:3845–3857
Alizadeh A, Braber S, Akbari P, Garssen J, Fink-Gremmels J (2015) Deoxynivalenol impairs weight gain and affects markers of gut health after low-dose, short-term exposure of growing pigs. Toxins 7:2071–2095
Berthiller F, Krska R, Domig KJ, Kneifel W, Juge N, Schuhmacher R, Adam G (2011) Hydrolytic fate of deoxynivalenol-3-glucoside during digestion. Toxicol Letters 206:264–267
Berthiller F, Crews C, Dall'Asta C, De Saeger SD, Haesaert G, Karlovsky P, Oswald IP, Seefelde W, Speijers G, Stroka J (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57:165–186
Beyer M, Daenicke S, Rohweder D, Humpf H-U (2010) Determination of deoxynivalenol-sulfonate (DONS) in cereals by hydrophilic interaction chromatography coupled to tandem mass spectrometry. Mycotox Res 26:109–117
Bouaziz C, Martel C, Sharaf e d O, Abid-Essefi S, Brenner C, Lemaire C, Bacha H (2009) Fusarial toxin-induced toxicity in cultured cells and in isolated mitochondria involves PTPC dependent activation of the mitochondrial pathway of apoptosis. Toxicol Sci 110:363–375
Bretz M, Beyer M, Cramer B, Knecht A, Humpf HU (2006) Thermal degradation of the Fusarium mycotoxin deoxynivalenol. J Agric Food Chem 54:6445–6451
Cano-Sancho G, Sanchis V, Ramos AJ, Marín S (2013) Effect of food processing on exposure assessment studies with mycotoxins. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:867–875
Cazzaniga D, Basílico JC, González RJ, Torres RL, de Greef DM (2001) Mycotoxins inactivation by extrusion cooking of corn flour. Lett Appl Microbiol 33:144–147
Cenkowski S, Pronyk C, Zmidzinska D, Muir WE (2007) Decontamination of food products with superheated steam. J Food Eng 83:68–75
Cetin Y, Bullerman LB (2006) Confirmation of reduced toxicity of deoxynivalenol in extrusion-processed corn grits by the MTT bioassay. J Agric Food Chem 54:1949–1955
Cheat S, Pinton P, Cossalter AM, Cognie J, Vilariño M, Callu P, Raymond-Letron I, Oswald IP, Kolf-Clauw M (2016) The mycotoxins deoxynivalenol and nivalenol show in vivo synergism on jejunum enterocytes apoptosis. Food Chem Toxicol 87:45–54
Dänicke S, Brezina U (2013) Kinetics and metabolism of the Fusarium toxin deoxynivalenol in farm animals: consequences for diagnosis of exposure and intoxication and carry over. Food Chem Toxicol 60:58–75
Dänicke S, Beineke A, Goyarts T, Valenta H, Beyer M, Humpf H-U (2008) Effects of a Fusarium toxin-contaminated triticale, either untreated or treated with sodium metabisulphite (Na2S2O5, SBS), on weaned piglets with a special focus on liver function as determined by the 13C-methacetin breath test. Arch Anim Nutr 62:263–286
Dänicke S, Hegewald AK, Kahlert S, Kluess J, Rotköttter HJ, Breves G, Döll S (2010) Studies on the toxicity of deoxynivalenol (DON), sodium metabisulfite, DON-sulfonate (DONS) and de-epoxy-DON for porcine peripheral blood mononuclear cells and the intestinal porcine epithelial cell lines IPEC-1 and IPEC-J2, and on effects of DON and DONS on piglets. Food Chem Toxicol 48:2154–2162
Dänicke S, Meyer U, Winkler J, Ulrich S, Frahm J, Kersten S, Valenta H, Rehage J, Häussler S, Sauerwein H, Locher L (2016) Haematological and immunological adaptations of non-pregnant, non-lactating dairy cows to a high-energetic diet containing mycotoxins. Arch Anim Nutr 70:1–16
De Angelis E, Monaci L, Pascale M, Visconti A (2013) Fate of deoxynivalenol, T-2 and HT-2 toxins and their glucoside conjugates from flour to bread: an investigation by high-performance liquid chromatography high-resolution mass spectrometry. Food Addit Contam A 30:345–355
Dropa T, Hajšlová J, Lancová K, Burešová I (2014) The effect of bread-making process on contents of key trichothecene mycotoxins: deoxynivalenol, T-2, and HT-2 toxins. Czech J Food Sci 32:570–577
EFSA (European Food Safety Authority) (2013) Deoxynivalenol in food and feed: occurrence and exposure. EFSA J 11:3379
Farahany EM, Jinap S (2011) Influence of noodle processing (industrial protocol) on deoxynivalenol. Food Control 22:1765–1769
Generotti S, Cirlini M, Malachova A, Sulyok M, Berthiller F, Dall'Asta C, Suman M (2015) Deoxynivalenol & deoxynivalenol-3-glucoside mitigation through bakery production strategies: effective experimental design within industrial rusk-making technology. Toxins 7:2773–2790
Giménez I, Blesa J, Herrera M, Ariño A (2014) Effects of bread making and wheat germ addition on the natural deoxynivalenol content in bread. Toxins 6:394–401
Israel-Roming F, Avram M (2010) Deoxynivalenol stability during wheat processing. Rom Biotech Let 15:47–50
Kaushik G (2015) Effect of processing on mycotoxin content in grains. Crit Rev Food Sci Nutr 55:1672–1683
Kollarczik B, Gareis M, Hanelt M (1994) In vitro transformation of the Fusarium mycotoxins deoxynivalenol and zearalenone by the normal gut microflora of pigs. Nat Toxins 2:105–110
Kostelanska M, Dzuman Z, Malachova A, Capouchova I, Prokinova E, Skerikova A, Hajslova J (2011) Effects of milling and baking technologies on levels of deoxynivalenol and its masked form deoxynivalenol-3-glucoside. J Agric Food Chem 59:9303–9312
Lancova K, Hajslova J, Kostelanska M, Kohoutkova J, Nedelnik J, Moravcova H, Vanova M (2008) Fate of trichothecene mycotoxins during the processing: milling and baking. Food Addit Contam Part A 25:650–659
Milani J, Maleki G (2014) Effects of processing on mycotoxin stability in cereals. J Sci Food Agric 94:2372–2375
Moazami FE, Jinap S, Mousa W, Hajeb P (2014) Effect of food additives on deoxynivalenol reduction and quality attributes in steamed and fried instant noodles. Cereal Chem 91:88–94
Nagl V, Schatzmayr G (2015) Deoxynivalenol and its masked forms in food and feed. Curr Opin in Food Sci 5:43–49
Nagl V, Schwartz H, Krska R, Moll WD, Knasmüller S, Ritzmann M, Adam G, Berthiller F (2012) Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in rats. Toxicol Lett 213:367–373
Nowicki TW, Gaba DG, Dexte FE, Matsuo RR, Clear RM (1988) Retention of the fusarium mycotoxin deoxynivalenol in wheat during processing and cooking of spaghetti and noodles. J Cereal Sci 18:189–202
Numanoglu E, Gökmen V, Uygun U, Koksel H (2012) Thermal degradation of deoxynivalenol during maize bread baking. Food Addit Contam A 29:423–430
Pacin A, Bovier EC, Cano G, Taglieri D, Pezzani CH (2010) Effect of the bread making process on wheat flour contaminated by deoxynivalenol and exposure estimate. Food Control 21:492–495
Paulick M, Winkler J, Kersten S, Schatzmayr D, Schwartz-Zimmermann HE, Dänicke S (2015) Studies on the bioavailability of deoxynivalenol (DON) and DON sulfonate (DONS) 1, 2, and 3 in pigs fed with sodium sulfite-treated DON-contaminated maize. Toxins 7:4622–4644
Pestka JJ (2008) Mechanisms of deoxynivalenolinduced gene expression and apoptosis. Food Addit Contam A 25:1128–1140
Pietsch C, Katzenback BA, Garcia-Garcia E, Schulz C, Belosevic M, Burkhardt-Holm P (2015) Acute and subchronic effects on immune responses of carp (Cyprinus carpio L.) after exposure to deoxynivalenol (DON) in feed. Mycotoxin Res 31:151–164
Ragab WS, Drusch S, Schnieder F, Beyer M (2007) Fate of deoxynivalenol in contaminated wheat grain during preparation of Egyptian ‘balila’. Int J Food Sci Nutr 58:169–177
Rychlik M, Humpf HU, Marko D, Dänicke S, Mally A, Berthiller F, Klaffke H, Lorenz N (2014) Proposal of a comprehensive definition of modified and other forms of mycotoxins including “masked” mycotoxins. Mycotoxin Res 30:197–205
Samar MM, Neira MS, Resnik SL, Pacin A (2001) Effect of fermentation on naturally occurring deoxynivalenol (DON) in Argentinean bread processing technology. Food Addit Contam 18:1004–1010
Samar M, Resnik SL, González HHL, Pacin AM, Castillo MD (2007) Deoxynivalenol reduction during the frying process of turnover pie covers. Food Control 18:1295–1299
Savard C, Nogues P, Boyer A, Chorfi Y (2016) Prevention of deoxynivalenol- and zearalenone-associated oxidative stress does not restore MA-10 Leydig cell functions. Toxicology 341-343:17–27
Schmeitzl C, Warth B, Fruhmann P, Michlmayr H, Malachová A, Berthiller F, Schuhmacher R, Krska R, Adam G (2015) The metabolic fate of deoxynivalenol and its acetylated derivatives in a wheat suspension culture: identification and detection of DON-15-O-glucoside, 15-acetyl-DON-3-O-glucoside and 15-acetyl-DON-3-sulfate. Toxins 7:3112–3126
Schulz AK, Kersten S, Dänicke S, Coenen M, Vervuert I (2015) Effects of deoxynivalenol in naturally contaminated wheat on feed intake and health status of horses. Mycotoxin Res 31:209–216
Scott PM, Kanhere SR, Dexter JE, Brennan PW, Trenholm HL (1984) Distribution of the trichothecene mycotoxin deoxynivalenol (vomitoxin) during the milling of naturally contaminated hard red spring wheat and its fate in baked products. Food Addit Contam 1:313–323
Scudamore KA, Guy RC, Kelleher B, MacDonald SJ (2008a) Fate of Fusarium mycotoxins in maize flour and grits during extrusion cooking. Food Addit Contam A 25:1374–1384
Scudamore KA, Guy RCE, Kelleher B, MacDonald SJ (2008b) Fate of the fusarium mycotoxins, deoxynivalenol, nivalenol and zearalenone, during extrusion of wholemeal wheat grain. Food Addit Contam A 25:331–337
Srecec S, Štefanec J, Pleadin J, Bauman I (2013) Decreasing deoxynivalenol concentration in maize within the production chain of animal feed. Agro Food Industry Hi Tech 24:62–65
Sugita-Konishi Y, Park BJ, Kobayashi-Hattori K, Tanaka T, Chonan T, Yoshikawa K, Kumagai S (2006) Effect of cooking process on the deoxynivalenol content and its subsequent cytotoxicity in wheat products. Biosci Biotechnol Biochem 70:1764–1768
Sundstøl Eriksen G, Pettersson H, Lundh T (2004) Comparative cytotoxicity of deoxynivalenol, nivalenol, their acetylated derivatives and deepoxy metabolites. Food Chem Toxicol 42:619–624
Tang Y, Li J, Li F, Hu CA, Liao P, Tan K, Tan B, Xiong X, Liu G, Li T, Yin Y (2015) Autophagy protects intestinal epithelial cells against deoxynivalenol toxicity by alleviating oxidative stress via IKK signaling pathway. Free Radic Biol Med 89:944–951
Valle-Algarra FM Mateo EM, Medina A, Mateo F, Gimeno-Adelantado JV, Jimenez M (2009) Changes in ochratoxin A and type B trichothecenes contained in wheat flour during dough fermentation and bread-baking. Food Addit Contam A 26:896–906
Varga E, Malachova A, Schwartz H, Krska R, Berthiller F (2013) Survey of deoxynivalenol and its conjugates deoxynivalenol-3-glucoside and 3-acetyl-deoxynivalenol in 374 beer samples. Food Addit Contam A 30:137–146
Vidal A, Marín S, Morales H, Ramos AJ, Sanchis V (2014) The fate of deoxynivalenol and ochratoxin A during the breadmaking process, effects of sourdough use and bran content. Food Chem Toxicol 68:53–60
Vidal A, Sanchis V, Ramos AJ, Marín S (2015) Thermal stability and kinetics of degradation of deoxynivalenol, deoxynivalenol conjugates and ochratoxin A during baking of wheat bakery products. Food Chem 178:276–286
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 Res Int 85:182–190
Visconti A, Haidukowski EM, Pascale M, Silvestri M (2004) Reduction of deoxynivalenol during durum wheat processing and spaghetti cooking. Toxicol Lett 153:181–189
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 A 27:1694–1700
Wang Z, Wu Q, Kuca K, Dohnal V, Tian Z (2014) Deoxynivalenol: signaling pathways and human exposure risk assessment—an update. Arch Toxicol 88:1915–1928
Wolf-Hall CE, Hanna MA, Bullerman LB (1999) Stability of deoxynivalenol in heat-treated foods. J Food Protect 62:962–964
Wu L, Wang B (2015) Evaluation on levels and conversion profiles of DON, 3-ADON, and 15-ADON during bread making process. Food Chem 185:509–516
Wu Q, Lohrey L, Cramer B, Yuan Z, Humpf HU (2011) Impact of physicochemical parameters on the decomposition of deoxynivalenol during extrusion cooking of wheat grits. J Agric Food Chem 59:12480–12485
Wu Q, Dohnal V, Kuca K, Yuan Z (2013) Trichothecenes: structure-toxic activity relationships. Curr Drug Metab 14:641–660
Wu Q, Wang X, Wan D, Li J, Yuan Z (2014a) Crosstalk of JNK1-STAT3 is critical for RAW264.7 cell survival. Cell Signal 26:2951–2960
Wu QH, Wang X, Yang W, Nussler AK, Xiong LY, Kuca K, Dohnal V, Zhang XJ, Yuan ZH (2014b) Oxidative stress-mediated cytotoxicity and metabolism of T-2 toxin and deoxynivalenol in animals and humans: an update. Arch Toxicol 88:1309–1326
Wu QH, Wu GX, Wang Y, Wan D, Zhang XJ, Yuan ZH (2014c) Deoxynivalenol: metabolism and regional differences in human exposure. Mil Med Sci Lett 83:114–119
Young JC (1986) Formation of sodium bisulfite addition products with trichothecenones and alkaline hydrolysis of deoxynivalenol and its sulfonate. J Agric Food Chem 34:919–923
Young JC, Blackwell BA, Apsimon JW (1986) Alkaline degradation of the myctoxin 4-deoxynivalenol. Tetrahedron Lett 27:1019–1022
Young JC, Trenholm HL, Friend DW, Prelusky DB (1987) Detoxification of deoxynivalenol with sodium bisulfite and evaluation of the effects when pure mycotoxin or contaminated corn was treated and given to pigs. J Agric Food Chem 35:259–261
Zhang H, Wang B (2014) Fate of deoxynivalenol and deoxynivalenol-3-glucoside during wheat milling and Chinese steamed bread processing. Food Control 44:86–91
Zhang H, Wang B (2015) Fates of deoxynivalenol and deoxynivalenol-3-glucoside during bread and noodle processing. Food Control 50:754–757
Acknowledgements
This study was financially supported by Yangtze Youth Talents Fund (Yangtze University, Grant No. 2015cqr19), National Natural Science Foundation of China (Grant No. 31602114), and the project of Excellence FIM UHK.
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Wu, Q., Kuča, K., Humpf, HU. et al. Fate of deoxynivalenol and deoxynivalenol-3-glucoside during cereal-based thermal food processing: a review study. Mycotoxin Res 33, 79–91 (2017). https://doi.org/10.1007/s12550-016-0263-9
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DOI: https://doi.org/10.1007/s12550-016-0263-9