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Symposium Introduction
Summary of the ACS symposium "Public Health Perspectives of Mycotoxins in Food" Lauren S. Jackson, and Dojin Ryu J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b02909 • Publication Date (Web): 27 Jul 2017 Downloaded from http://pubs.acs.org on July 31, 2017
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Journal of Agricultural and Food Chemistry
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Summary of the ACS Symposium
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Public Health Perspectives of Mycotoxins in Food
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Lauren S. Jackson*† and Dojin Ryu‡
4 †
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U.S. Food and Drug Administration
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Center for Food Safety & Applied Nutrition
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Office of Food Safety
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Division of Food Processing Science & Technology
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6502 South Archer Road, Bedford Park, IL 60501
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(708) 924-0616 (Phone)
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(708) 924-0690 (Fax)
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[email protected] 13 14
‡
University of Idaho/Washington State University
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School of Food Science
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875 Perimeter Drive MS 2312
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Moscow, ID 83844-2312
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(208) 885-0166 (Phone)
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(208) 885-2567 (Fax)
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[email protected] 21
*Corresponding Author
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KEYWORDS: Mycotoxins, Toxicity, Public Health, Control, Occurrence, Detection
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Abstract
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A symposium entitled “Public Health Perspectives of Mycotoxins in Food” was held at the 251st
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American Chemical Society Meeting in March 2016 in San Diego, CA and was sponsored by the
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ACS Division of Agricultural and Food Chemistry. The purpose of the symposium was to
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convene the leading mycotoxin researchers throughout the world to discuss the current state of
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knowledge as well as research needs with respect to evaluating the toxicological properties of
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mycotoxins, and ways to detect, control and reduce human and animal exposure to these natural
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toxins.
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government and industrial institutions from North America, Europe, Asia and Africa. The
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presentations covered such diverse topics as a historical perspective on the discovery of the
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major fungal toxins, occurrence of mycotoxins in food and feed, toxicological properties of
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mycotoxins and their influence on public health, analytical methods for mycotoxins, pre- and
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post-harvest control of mycotoxins, and regulatory aspects. This article is intended to provide a
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brief summary of the presentations as well as a record of the proceedings of the symposium.
Twenty-three presentations were delivered by speakers representing academic,
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Mycotoxins are ubiquitous, toxic secondary metabolites produced by filamentous fungi, with
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Aspergillus, Penicillium, and Fusarium species producing the majority of the toxins of concern
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to human and animal health.1-3 These fungal metabolites are responsible for pre- and post-
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harvest contamination of agricultural commodities used for human food and animal feed. While
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an overall incidence of mycotoxin contamination of human food is not currently known, recent
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surveys suggest that greater than 30% of animal feed and feed ingredients are contaminated with
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at least one mycotoxin.4-8
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contamination is estimated to range from $418 million to $1.66 billion, which do not include
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mitigative costs and livestock losses of $466 million and $6 million, respectively.9
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Mycotoxins can cause a wide range of chronic health effects in animals and humans exposed to
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small amounts of toxins over an extended period of time. In addition, mycotoxins can cause
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acute effects and be lethal if consumed in large quantities over a short time.1 Health-related
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effects of mycotoxins depend the age and nutritional status of person or animal exposed, the
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extent of exposure to the mycotoxin and other toxic compounds, and the toxicological properties
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of the mycotoxin.1-3 The ubiquitous nature and highly toxic nature of some fungal toxins
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illustrate the importance of ensuring that mycotoxin contamination is minimized to reduce the
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risk of human and animal exposure.10
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To discuss and evaluate the current status of mycotoxin research, a symposium entitled “Public
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Health Perspectives of Mycotoxins in Food” was held March 15-16, 2016 at the 251st ACS
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National Meeting in San Diego, CA. The symposium consisted of 23 presentations delivered by
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recognized scientists from the U.S., Canada, Europe, Asia and Africa, and covered such diverse
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topics as general properties of mycotoxins found in food and feed, toxicological effects of
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mycotoxins and the influence they have on public health, detection and analysis of mycotoxins in
In the U.S. alone, annual losses of crops due to mycotoxin
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food, and approaches for control and regulation of mycotoxins. This article is intended to
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provide a brief summary of the presentations as well as a record of the proceedings of the
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symposium.
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presenters which cover many of the topics discussed in the symposium.
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The introductory session provided an overview of mycotoxin research history, occurrence of
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mycotoxins in food and feed, and environmental and climatic conditions that influence fungal
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growth and mycotoxin production.
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Australia), provided a historic perspective of mycotoxin research. In his talk, Dr. Pitt reviewed
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the major mycotoxins including ergot, rice toxins (citreoviridin, citrinin, luteoskyrin and
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cyclochlorotine) aflatoxins, fumonisins, deoxynivalenol and zeararalenone, from a historical
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context, and more specifically how these toxins were discovered and their effects on human and
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animal health.
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environmental changes such as fluctuations in temperature and rainfall, and their potential role in
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the types and extent of fungal and toxin contamination in agricultural commodities. Dojin Ryu
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(University of Idaho, Moscow, ID) reviewed the major fungi and mycotoxins associated with
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cereal grain and cereal-based foods, discussed co-occurrence of fungal toxins in grain and its
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possible public health significance, and concluded that there is a need for improved monitoring
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programs and research to establish science-based control measures and regulatory limits for
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mycotoxins. A final paper in this section, presented by Franz Berthiller (University of Natural
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Resources and Life Sciences Vienna, Tulln, Austria) reviewed the occurrence, toxicological
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significance and analysis of “emerging mycotoxins”. Included in this discussion were masked
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mycotoxins, chemically-modified mycotoxin derivatives that are undetectable by conventional
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analytical techniques, changes in distribution of mycotoxins in various regions of the world, and
Following this overview article are twelve papers authored by symposium
A keynote presentation, given by John Pitt (CSIRO,
David Miller (Carleton University, Ottawa, Ontario, Canada) presented on
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the “emerging mycotoxins” (culmorin, beauvericin and enniatins), mycotoxins which are not
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regulated, but where there is evidence that their incidence is increasing.11
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The second session of the symposium was devoted to presentations on identification and use of
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biomarkers to estimate human and animal exposure to fungal toxins, and the toxicological
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properties and public health consequences due to the presence of mycotoxins in food and feed.
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As developing countries often lack the resources to prevent and control mycotoxin accumulation
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in agricultural commodities, populations in these regions of the world are at a higher risk of
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exposure to these natural toxins.12,13 Paul Turner (University of Maryland, College Park, MD)
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gave a presentation studies that evaluated exposure of children living in Western Africa to
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aflatoxin-, deoxynivalenol- and fumonisin-contaminated dietary staples. These studies found a
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possible association of consumption of mycotoxin-contaminated food with growth stunting and
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other health-related problems in these populations.
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Ghent, Belgium) presented the results of a study that assessed exposure of infants from different
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regions of Tanzania to multiple mycotoxins (aflatoxins, deoxynivalenol, ochratoxin, zearalenone,
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fumonisins, T-2 toxin, HT-2 toxin) present in corn, an important dietary staple for these
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populations.
Analice Kamala (University of Ghent,
The results of this study indicate that exposure varied among the different agro-
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ecological regions of Tanzania, and that children receiving corn-based complementary foods in
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Tanzania are at a high risk of exposure to multiple toxins, particularly aflatoxin and fumonisins.
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Two presentations in this session were given on identification and use of biomarkers for
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estimating exposure to fungal toxins. The first, delivered by Michele Solfrizzo (CNR, Institute
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of Sciences of Food Protection, Bari, Italy), focused on identification and use of urinary
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biomarkers in humans and animals for estimating exposure to the major mycotoxins (aflatoxin
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B1, ochratoxin A, zearalenone, fumonisin B1 (FB1), and deoxynivalenol).
Ronald Riley 5
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(USDA/ARS, Athens, GA) discussed the results of a study that examined the use of urinary and
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blood biomarkers to determine exposure to FB1 in human populations in Guatemala. The results
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of this study as well as other research studies reviewed by Dr. Riley indicate that urinary FB1
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levels and red blood cell sphiganine/sphingosine ratio are correlated, and that both biomarkers
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could be used to predict when individuals are at increased risk for exceeding the Provisional
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Maximum Tolerable Daily Intake (PMTDI) established by the Joint FAO/WHO Expert
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Committee on Food Additives (JECFA). Another major research finding is that individuals
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exposed to high levels of fumonisins from the diet experienced sphingolipid metabolism changes
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similar to those seen when animals and cell cultures were dosed with these mycotoxins alone.
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Several presentations reviewed the toxicological properties of mycotoxins, focusing on their
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specific target organs such as the liver, kidney and the brain. Matthias Behrens (University of
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Munster, Munster, Germany) discussed studies that discovered that some mycotoxins
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(deoxynivalenol, moniliformin, citrinin, zearalenone) have a high permeability to the blood-brain
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barrier which potentially leads to high brain exposure to these toxins, while other toxins such as
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ochratoxin A (OTA) reduce the viability and integrity of the blood-brain barrier. OTA, an
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International Agency for Research on Cancer (IARC) Group 2B carcinogen (possibly
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carcinogenic to human), is a frequent contaminant of cereal grains and other agricultural
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commodities.14 Genevieve Bondy (Health Canada) reported on studies that assessed the effects
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of OTA on rats with kidney cancer and toxicity as evaluated the toxicological endpoints.
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Investigations on the mechanisms by which OTA binds to DNA to form adducts were reviewed
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by Richard Manderville (University of Guelph, Guelph, Ontario, Canada).
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indicated that ability of OTA to form DNA adducts may be used to develop an aptasensor for
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detecting OTA.
His talk also
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The third session of the mycotoxin symposium covered approaches for pre-harvest control of
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mycotoxin formation, as well as ways to post-harvest ways to bind, degrade or detoxify toxins
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present in food or feed.
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include: (1) cultural practices that prevent or reduce crop damage and the levels of toxigenic
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fungi or crop damage in the field, (2) biological control through the use of microorganisms that
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compete with the toxigenic fungi and/or prevent their outgrowth and production of mycotoxins,
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and (3) enhancing host resistance through plant breeding and/genetic engineering.1,14 Charles
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Bacon (USDA/ARS) reviewed the use of endophytic microorganisms, particularly those that
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produce quorum sensing inhibitors, as biocontrol agents for mycotoxic fungal endophytes, such
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as the Fusarium species.
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accomplished by using nonaflatoxigenic Aspergillus flavus strains that out-compete wild
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aflatoxigenic A. flavus strains present in the field. Hamed Abbas (USDA-ARS, Stoneville,
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Mississippi) reviewed improvements in aflatoxin biocontrol treatments through the use of
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bioplastic materials (corn starch and other biodegradable raw materials) that act as nutritive
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carriers of the biocontrol agents. The complex interplay of factors affecting plant resistance to
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fungal attack and mycotoxin production, biochemical and chemical markers for resistance in
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corn to aflatoxin contamination, and the use of plant breeding and genetic engineering to confer
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crops with resistance to fungal infection and toxin accumulation were discussed by Deepak
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Bhatnagar (USDA/ARS, New Orleans, LA).
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Approaches for post-harvest control of mycotoxins include: (1) practices that prevent fungal
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growth and toxin production during storage of agricultural commodities and food, such as
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controlling moisture levels, temperature and addition of preservatives, (2) processing methods
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that remove mycotoxin-contaminated grain or food stream or inactivate or detoxify preformed
Strategies to reduce mycotoxin contamination in crops pre-harvest
Reduction of aflatoxin contamination in harvested crops is
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toxin (e.g. sorting, milling, thermal processing), (3) chemical treatments that modify and
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detoxify mycotoxins, and (4) binding agents that suppress or reduce absorption, promote
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excretion, or modify the mode of action of mycotoxins.1,14 Ken Voss (USDA/ARS, Athens, GA)
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gave a presentation on studies that evaluated the effects of different food processing treatments
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on the toxicological properties of fumonisin present in corn-based foods using rodent bioassays.
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The studies found that extrusion processing was effective at reducing fumonisin toxicity,
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particularly when glucose was added to the corn prior to processing. In contrast, nixtamalization
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(an alkaline cooking method) effectively detoxified fumonisin-contaminated corn at lower
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contamination levels while reducing, but not preventing, toxicity at a higher contamination level.
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Post-harvest control of mycotoxins was a subject of a review by Gerd Schatzmayr (BIOMIN
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Research Center, Tulln, Austria). His presentation focused on the use of clays and other agents
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to bind and inhibit absorption of mycotoxins present in feed. Other approaches discussed were
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the use of microbiological agents and enzymes which can be used to biotransform or degrade
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mycotoxins into forms of reduced toxicity.
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Awareness of the significant impacts of mycotoxins on animal and human health has led to the
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development of analytical methods for their identification and surveillance in food and feed. The
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wide range of crops, commodities and agricultural systems in which mycotoxins can be found,
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presents a challenge for effective analyses. The fourth session of the symposium focused on
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tradition as well as state-of-the art methods for detection of mycotoxins. Sarah De Saeger
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(University of Ghent, Ghent, Belgium) provided a comprehensive review of immunochemical
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methods used for rapid screening for mycotoxins. These methods include traditional ELISA
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assays and more recently developed multiplex fluorescent immunoassays that use quantum dots
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rather than enzymes for detection. The improvements in immunoassay sensitivity, stability and 8 ACS Paragon Plus Environment
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selectivity through the use of nanobodies were discussed by Candace Bever (University of
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California-Davis, Davis, CA). Nanobody-based techniques differ from the traditional ELISA as
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the antibodies are made in bacterial cells by expression of engineered fragment of the variable
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antibody region.
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Hong-Li Guo (Tsinghua University, Beijing, China) gave a presentation on a new planar
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waveguide fluorescence immunosensor for rapid detection of aflatoxin M1 and melamine in
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milk.
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mycotoxins in a variety of human and animal food and feed products was highlighted in a
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presentation by Kai Zhang (U.S. FDA, College Park, MD). The benefits of such a method
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include sensitivity, selectivity, and the ability to detect and quantify a variety of analytes in a
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single analysis.
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Research Center, Tulln, Austria), focused on the tools to determine the identity, occurrence and
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toxicity of masked mycotoxins.
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Regulations relating to mycotoxins have been established in over 100 countries to protect
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humans and animals from exposure to these hazardous compounds.16 Factors which play a role
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in the decision-making process of setting limits for mycotoxins including the availability of
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toxicology and occurrence data, procedures for sampling and analysis, and socio-economic
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factors. The final two presentations of the symposium discussed regulation of mycotoxins in
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Canada and the U.S. Genevieve Bondy (Health Canada, Ottawa, Canada) outlined the different
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federal agencies in Canada that research and regulate mycotoxins, Canadian involvement in
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committees responsible for international standard-setting for mycotoxins and other chemical
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contaminants in food, surveillance and monitoring activities in Canada, the considerations
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involved in setting maximum levels for chemical contaminants in food, and Canadian regulations
A new stable isotope dilution LC-MS/MS-based method for detecting at least 12
The final presentation in this session, given by Veronika Nagl (BIOMIN
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and maximum levels governing mycotoxin residues in food. Mycotoxin regulations in the U.S.
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were described in a presentation by Henry Kim (U.S. FDA, College Park, MD). In his talk, Dr.
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Kim discussed FDA’s regulatory authority and role in ensuring the safety of the U.S. food
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supply, factors that impact establishment of regulatory limits for chemical contaminants such as
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mycotoxins, approaches for controlling mycotoxins, and regulatory limits for several of the
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mycotoxins of public health concern.
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We thank the ACS Division of Agricultural and Food Chemistry for sponsoring the symposium,
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and the symposium speakers and attendees for their informative presentations and lively
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discussions. We are grateful to Thomas Hofmann, Ivonne Hofmann-Sellier and Journal of
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Agricultural and Food Chemistry editors for the invitation to publish papers corresponding to
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symposium presentations and for facilitating the manuscript submission and review process. We
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hope that the following set of articles will constitute a valuable record and resource for
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continuing progress in the scientifically challenging and vitally important field of mycotoxin
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research.
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Lauren S. Jackson
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U.S. Food and Drug Administration
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Center for Food Safety and Applied Nutrition
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Office of Food Safety
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Division of Food Processing Science & Technology
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6502 S. Archer Rd.
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Bedford Park, IL 60501
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Dojin Ryu
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School of Food Science
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University of Idaho/Washington State University
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875 Perimeter Drive MS 2312
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Moscow, ID 83844-2312
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Funding :
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No funding was received to support the publication of this article.
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References:
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1. Bhat, R. ; Rai, R.V. ; Karim, A.A. Mycotoxins in food and feed: Present status and future
232
concerns. Comp. Rev. Food Sci. Food Safety 2010, 9, 57-81.
233
2. CAST (Council for Agricultural Science and Technology). Mycotoxins: Economic and Health
234
Risks. Task Force Report No. 116, 1989, Council for Agricultural Science and Technology,
235
Ames, IA.
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236
3. CAST (Council for Agricultural Science and Technology). Mycotoxins: Risks in Plant,
237
Animal and Human Systems. Task Force Report No. 139, 2003, Council for Agricultural Science
238
and Technology, Ames, IA.
239
4.
240
mycotoxins in commodities, feeds and feed ingredients. Anim. Feed Sci. Technol. 2007, 137,
241
265-282.
242
5. Rodrigues, I.; Naehrer, K. A three-year survey on the worldwide occurrence of mycotoxins
243
in feedstuffs and feed. Toxins 2012, 4, 663-675.
244
6. Streit, E.; Schatzmayr, G.; Tassis, P.; Tzika, E.; Marin, D.; Taranu, I.; Tabuc, C.; Nicolau, A.;
245
Aprodu, I.; Puel, O. Current situation of mycotoxin contamination and co-occurrence in animal
246
feed- Focus on Europe. Toxins 2012, 4, 788-809.
247
7. Streit, E.; Naehrer, K.; Rodrigues, I.; Schatzmayr, G. Mycotoxin occurrence in feed and feed
248
raw materials worldwide: Long-term analysis with special focus on Europe and Asia. J. Sci.
249
Food Agric. 2013, 93, 2892-2899.
250
8. Pinotti, L.; Ottoboni, M.; Giromini, C.; Dell’Orto, V.; Cheli, F. Mycotoxin contamination in
251
the EU feed supply chain: A focus on cereal byproducts. Toxins 2016, 8, 45
252
9. Vardon, P.J.; McLaughlin, C.; Nardinelli, C. Potential economic costs of mycotoxins in the
253
United States. In Mycotoxins: Risks in Plant and Human Systems, Chapter 10. CAST (Council
254
of Agriculture, Science and Technology) Task Force Report No. 139, 2003, pp. 136-142. Ames,
255
IA.
Binder, E.M.; Tan, L.M.; Chin, L.J.; Handl, J.; Richard, J.
Worldwide occurrence of
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256
10. Mitchell, N.J.; Bowers, E.; Hurburgh, C.; Wu, F. Potential economic losses to the US corn
257
industry from aflatoxin contamination. Food Addit. Contam. 2016, 33, 540-550.
258
11. Vaclavikova, M.; Malachova, A.; Veprikova, Z.; Dzuman, Z.; Zachariasova, M.; Hajslova, J.
259
‘Emerging’ mycotoxins in cereals processing chains: changes of enniatins during beer and bread
260
making. Food Chem. 2013, 136, 750−757.
261
12. Wu, F. Mycotoxin risk assessment for the purpose of setting international regulatory
262
standards. Environ. Sci. & Technol. 2004, 38, 4049-4055.
263
13. International Agency for Research on Cancer (IARC). Mycotoxin Control in Low- and
264
Middle Income Countries. IARC Working Group Report No. 9, Wild, C.P., Miller, J.D., and
265
Groopman, J.D. (Eds), WHO Press, World Health Organization, 2015, Geneva, Switzerland.
266
Available at https://www.ncbi.nlm.nih.gov/pubmed/27030861 Accessed 6/19/2017.
267
14. International Agency for Research on Cancer (IARC). Practical approaches to control
268
mycotoxins. IARC Sci. Publ. 2012, 158,131-46.
269
15.
270
Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins.
271
IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 1993, Volume 56
272
IARC; Lyon, France.
273
16. van Egmond, H.P.; Schothorst, R.C.; Jonker, M.A. Regulations relating to mycotoxins in
274
food. Anal. Bioanal. Chem. 2007, 389,147–157.
International Agency for Research on Cancer (IARC) Some Naturally Occurring
275
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Table of Content Graphic
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