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Strategies to Prevent Mycotoxin Contamination of Food and Animal Feed: a Review

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Strategies to Prevent Mycotoxin Contamination of Food and Animal Feed: a Review Critical Reviews in Food Science and Nutrition, 46:593–619 (2006) Copyright C Taylor and Francis Group, LLC ISSN: 1040-8398 DOI: 10.1080/10408390500436185 Strategies to Prevent Mycotoxin Contamination of Food and Animal Feed: A Review BULENT KABAK Department of Food Engineering, Agricultural Faculty, University of Cukurova, TR-01330 Adana, Turkey ALAN D. W. DOBSON Microbiology Department and Environmental Research Institute, University College Cork, National University of Ireland, Cork, Ireland IS¸IL˙ VAR Department of Food Engineering, Agricultural Faculty, University of Cukurova, TR-01330 Adana, Turkey Mycotoxins are fungal secondary metabolites that have been associated with severe toxic effects to vertebrates produced by many important phytopathogenic and food spoilage fungi including Aspergillus, Penicillium, Fusarium, and Alternaria species. The contamination of foods and animal feeds with mycotoxins is a worldwide problem. We reviewed various control strategies to prevent the growth of mycotoxigenic fungi as well as to inhibit mycotoxin biosynthesis including pre-harvest (resistance varieties, field management and the use of biological and chemical agents), harvest management, and post-harvest (improving of drying and storage conditions, the use of natural and chemical agents, and irradiation) applications. While much work in this area has been performed on the most economically important mycotoxins, aflatoxin B1 and ochratoxin A much less information is available on other mycotoxins such as trichothecenes, fumonisin B1, zearalenone, citrinin, and patulin. In addition, physical, chemical, and biological detoxification methods used to prevent exposure to the toxic and carcinogenic effect of mycotoxins are discussed. Finally, dietary strategies, which are one of the most recent approaches to counteract the mycotoxin problem with special emphasis on in vivo and in vitro efficacy of several of binding agents (activated carbons, hydrated sodium calcium aluminosilicate, bentonite, zeolites, and lactic acid bacteria) have also been reviewed. Keywords Mycotoxin, detoxification, prevention INTRODUCTION Mycotoxins primarily occur in the mycelium of the toxi- genic moulds and may also be found in the spores of these Mycotoxins are secondary metabolites which are produced organisms13 and cause a toxic response, termed a mycotoxi- by several fungi mainly belonging to the genera: Aspergillus, cosis, when ingested by higher vertebrates and other animals.14 Penicillium, Fusarium, and Alternaria.1,2,3,4 While Aspergillus These secondary metabolites are synthesized during the end of and Penicillium species are generally found as contami- the exponential phase of growth and appear to have no biolog- nants in food during drying and storage, Fusarium and Al- ical significance with respect to mould growth/development or , − ternaria spp. can produce mycotoxins before or immediately competitiveness.13 15 17 All moulds are not toxigenic and while after harvesting.5 Up until now, approximately 400 secondary some mycotoxins are produced by only a limited number of metabolites with toxigenic potential produced by more than species, others may be produced by a relatively large range from , 100 moulds, have been reported, with the Food and Agricul- several genera.13 16 ture Organization (FAO) estimating that as much as 25% of The toxic effect of mycotoxin ingestion in both humans the world’s agricultural commodities are contaminated with and animals depends on a number of factors including in- mycotoxins,6−11 leading to significant economic losses.12 take levels, duration of exposure, toxin species, mechanisms of action, metabolism, and defense mechanisms.10,17 Consump- Address correspondence to Bulent Kabak, Department of Food Engineering, Agricultural Faculty, University of Cukurova, TR-01330 Adana,Turkey. E-mail: tion of mycotoxin-contaminated food or feed does however [email protected] lead to the induction of teratogenic, cancerogenic, oestrogenic, 593 594 B. KABAK ET AL. neurotoxic, and immunosuppresive effect in humans and/or Prevention Strategies of Mycotoxins in Cereals animals.11,18 The mycotoxins of most significance from both The main mycotoxin hazards associated with wheat pre- a public health and agronomic perspective include the aflatox- harvest in Europe are the toxins that are produced by fungi ins, trichothecenes, fumonisins, ochratoxin A (OTA), patulin, belonging to the genus Fusarium in the growing crop. Mycotox- tremorgenic toxins, and ergot alkoloids.10,11,17,19 ins produced by these fungi include zearalenone (ZEN) as well Because of the detrimental effects of these mycotoxins, as trichothecenes and include nivalenol (NIV), deoxynivalenol a number of strategies have been developed to help prevent (DON) and T-2 toxin. Fusarium species are also responsible for the growth of mycotoxigenic fungi as well as to decontami- a serious disease called Fusarium Head Blight (FHB), which nate and/or detoxify mycotoxin contaminated foods and animal can result in significant losses in both crop yield and quality. It feeds. 20,21 These strategies include: is important to note that although Fusarium infection is gener- • The prevention of mycotoxin contamination, ally considered to be a pre-harvest problem, it is possible for • Detoxification of mycotoxins present in food and feed, poor drying practices to lead to an increased susceptibility for 29 • Inhibition of mycotoxin absorption in the gastrointestinal in storage mycotoxin contamination. tract. Resistance Varieties. There are inherent differences in the susceptibility of various cereal species to FHB, which are re- flected in differences in the degree of mycotoxin contamination PREVENTION OF MYCOTOXIN CONTAMINATION to which each species is susceptible. The differences between crop species appear to differ between countries. This is proba- Mycotoxin contamination may occur in the field before har- bly due to differences in the genetic pool within each country’s vest, during harvesting, or during storage and processing,1,22,23 breeding program and the different environmental and agro- thus methods for the prevention of mycotoxin contamination nomic conditions in which crops are cultivated.30 Tekauz31 has can conveniently be divided into pre-harvest, harvesting and shown that DON levels in wheat, barley, and oats were similar post-harvest strategies.24 Whereas certain treatments have been when grown under the same field conditions in Western Canada found to reduce specific mycotoxin formation in different com- in 2001. However, Langesth and Rudberget32 have shown that modities, the complete elimination of mycotoxin contaminated oats had higher levels of DON contamination than barley and commodities is currently not realistically achievable. wheat in Norway from 1996 to 1999. It has also been reported Several codes of practice have been developed by Codex Al- that in wheat; tall plants without awns, and plants with lax ears imentarius for the prevention and reduction of mycotoxins in tend to have lower rates of natural infection than plants that are cereals, peanuts, apple products, and raw materials. The elabo- short, awned, or which have a high spikelet density.33 ration and acceptance of a General Code of Practice by Codex Only seed varieties recommended for use in a particular area will provide uniform guidance for all countries to consider in of a country should be planted in that particular area.25 In recent attempting to control and manage contamination by various my- work by Mesterhazy,34 wheat varieties most resistant to FHB cotoxins. In order for this practice to be effective, it will be were shown to reduce DON production to near zero. In fact, re- necessary for the producers in each country to consider the gen- sistance seemed to depend to a great extent on inhibition of toxin eral principles given in the Code, taking into account their local production directly, since the most aggressive disease-causing crops, climate, and agronomic practices, before attempting to fungal strains were also those producing the highest levels of implement provisions in the Code. The recommendations for the DON. This author suggested that an increased availability of re- reduction of various mycotoxins in cereals are divided into two sistant varieties, coupled with the use of appropriate fungicides, parts: recommended practices based on Good Agricultural Prac- was the key in an integrated approach to mycotoxin control asso- tice (GAP) and Good Manufacturing Practice (GMP); a com- ciated with Fusarium. Similarly, in another field test, resistance plementary management system to consider in the future is the to both FHB and DON contamination in different wheat varieties use of Hazard Analysis Critical Control Point (HACCP).25 has also been reported.35 Obtaining high levels of native genetic resistance in various Pre-Harvest Control Strategies crop types to toxigenic fungi has proven difficult to achieve. Problems in this regard have centered primarily on the lack of It is well established that mycotoxin contamination of agri- resistant control genotypes and on the lack of involvement of cultural product can occur in the field as well as during single major genes.36 Some resistance to Gibberella ear rot has storage.23,26,27,28 Since phytopathogenic fungi such as Fusar- however been reported in the past.37,38 A resistant gene has been ium and Alternaria spp can produce mycotoxins before or im- identified in Giberella39and maize hybrids produced which dis- mediately post harvesting several strategies have been developed
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