Summary of the ACS Symposium on Public Health Perspectives of

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Summary of the ACS Symposium on Public Health Perspectives of Mycotoxins in Food ABSTRACT: A symposium entitled “Public Health Perspectives of Mycotoxins in Food” was held at the 251st American Chemical Society (ACS) Meeting in March 2016 in San Diego, CA, and was sponsored by the ACS Division of Agricultural and Food Chemistry. The purpose of the symposium was to convene the leading mycotoxin researchers throughout the world to discuss the current state of knowledge as well as research needs with respect to evaluating the toxicological properties of mycotoxins and ways to detect, control, and reduce human and animal exposure to these natural toxins. A total of 23 presentations were delivered by speakers representing academic, government, and industrial institutions from North America, Europe, Asia, and Africa. The presentations covered such diverse topics as a historical perspective on the discovery of the major fungal toxins, occurrence of mycotoxins in food and feed, toxicological properties of mycotoxins and their influence on public health, analytical methods for mycotoxins, pre- and postharvest control of mycotoxins, and regulatory aspects. This paper is intended to provide a brief summary of the presentations as well as a record of the proceedings of the symposium.

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authored by symposium presenters that cover many of the topics discussed in the symposium. The introductory session presented an overview of mycotoxin research history, occurrence of mycotoxins in food and feed, and environmental and climatic conditions that influence fungal growth and mycotoxin production. A keynote presentation, given by John Pitt (CSIRO, Australia), provided a historic perspective of mycotoxin research. In his talk, Dr. Pitt reviewed the major mycotoxins, including ergot, rice toxins (citreoviridin, citrinin, luteoskyrin, and cyclochlorotine), aflatoxins, fumonisins, deoxynivalenol, and zeararalenone, from a historical context and, more specifically, how these toxins were discovered and their effects on human and animal health. David Miller (Carleton University, Ottawa, Ontario, Canada) presented on environmental changes, such as fluctuations in the temperature and rainfall, and their potential role in the types and extent of fungal and toxin contaminations in agricultural commodities. Dojin Ryu (University of Idaho, Moscow, ID, U.S.A.) reviewed the major fungi and mycotoxins associated with cereal grain and cereal-based foods, discussed the co-occurrence of fungal toxins in grain and their possible public health significance, and concluded that there is a need for improved monitoring programs and research to establish science-based control measures and regulatory limits for mycotoxins. A final paper in this section, presented by Franz Berthiller (University of Natural Resources and Life Sciences, Vienna, Tulln, Austria) reviewed the occurrence, toxicological significance, and analysis of “emerging mycotoxins”. Included in this discussion were masked mycotoxins, chemically modified mycotoxin derivatives that are undetectable by conventional analytical techniques, changes in the distribution of mycotoxins in various regions of the world, and the “emerging mycotoxins” (culmorin, beauvericin, and enniatins), mycotoxins which are not regulated but where there is evidence that their incidence is increasing.11 The second session of the symposium was devoted to presentations on the identification and use of biomarkers to

ycotoxins are ubiquitous, toxic secondary metabolites produced by filamentous fungi, with Aspergillus, Penicillium, and Fusarium species producing the majority of the toxins of concern to human and animal health.1−3 These fungal metabolites are responsible for pre- and postharvest contamination of agricultural commodities used for human food and animal feed. While an overall incidence of mycotoxin contamination of human food is not currently known, recent surveys suggest that greater than 30% of animal feed and feed ingredients are contaminated with at least one mycotoxin.4−8 In the U.S. alone, annual losses of crops as a result of mycotoxin contamination is estimated to range from $418 million to $1.66 billion, which do not include mitigative costs and livestock losses of $466 million and $6 million, respectively.9 Mycotoxins can cause a wide range of chronic health effects in animals and humans exposed to small amounts of toxins over an extended period of time. In addition, mycotoxins can cause acute effects and be lethal if consumed in large quantities over a short time.1 Health-related effects of mycotoxins depend upon the age and nutritional status of the person or animal exposed, the extent of exposure to the mycotoxin and other toxic compounds, and the toxicological properties of the mycotoxin.1−3 The ubiquitous nature and highly toxic nature of some fungal toxins illustrate the importance of ensuring that mycotoxin contamination is minimized to reduce the risk of human and animal exposure.10 To discuss and evaluate the current status of mycotoxin research, a symposium entitled “Public Health Perspectives of Mycotoxins in Food” was held March 15−16, 2016 at the 251st American Chemical Society (ACS) National Meeting in San Diego, CA. The symposium consisted of 23 presentations delivered by recognized scientists from the U.S., Canada, Europe, Asia, and Africa and covered such diverse topics as general properties of mycotoxins found in food and feed, toxicological effects of mycotoxins and the influence that they have on public health, detection and analysis of mycotoxins in food, and approaches for control and regulation of mycotoxins. This paper is intended to provide a brief summary of the presentations as well as a record of the proceedings of the symposium. Following this overview paper are 12 papers © 2017 American Chemical Society

Special Issue: Public Health Perspectives of Mycotoxins in Food Published: July 27, 2017 7017

DOI: 10.1021/acs.jafc.7b02909 J. Agric. Food Chem. 2017, 65, 7017−7020

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Symposium Introduction

cancer and toxicity as evaluated by the toxicological end points. Investigations on the mechanisms by which OTA binds to DNA to form adducts were reviewed by Richard Manderville (University of Guelph, Guelph, Ontario, Canada). His talk also indicated that the ability of OTA to form DNA adducts may be used to develop an aptasensor for detecting OTA. The third session of the mycotoxin symposium covered approaches for preharvest control of mycotoxin formation as well as postharvest ways to bind, degrade, or detoxify toxins present in food or feed. Strategies to reduce the mycotoxin contamination in crops preharvest include (1) cultural practices that prevent or reduce crop damage and the levels of toxigenic fungi or crop damage in the field, (2) biological control through the use of microorganisms that compete with the toxigenic fungi and/or prevent their outgrowth and production of mycotoxins, and (3) enhancing host resistance through plant breeding and/genetic engineering.1,14 Charles Bacon (ARS, USDA) reviewed the use of endophytic microorganisms, particularly those that produce quorum-sensing inhibitors, as biocontrol agents for mycotoxic fungal endophytes, such as the Fusarium species. Reduction of aflatoxin contamination in harvested crops is accomplished using non-aflatoxigenic Aspergillus flavus strains that outcompete wild aflatoxigenic A. flavus strains present in the field. Hamed Abbas (ARS, USDA, Stoneville, MS, U.S.A.) reviewed improvements in aflatoxin biocontrol treatments through the use of bioplastic materials (corn starch and other biodegradable raw materials) that act as nutritive carriers of the biocontrol agents. The complex interplay of factors affecting plant resistance to fungal attack and mycotoxin production, the biochemical and chemical markers for resistance in corn to aflatoxin contamination, and the use of plant breeding and genetic engineering to confer crops with resistance to fungal infection and toxin accumulation were discussed by Deepak Bhatnagar (ARS, USDA, New Orleans, LA, U.S.A.). Approaches for postharvest control of mycotoxins include (1) practices that prevent fungal growth and toxin production during storage of agricultural commodities and food, such as controlling moisture levels, temperature, and addition of preservatives, (2) processing methods that remove mycotoxin-contaminated grain or food stream or inactivate or detoxify preformed toxin (e.g., sorting, milling, and thermal processing), (3) chemical treatments that modify and detoxify mycotoxins, and (4) binding agents that suppress or reduce absorption, promote excretion, or modify the mode of action of mycotoxins.1,14 Ken Voss (ARS, USDA, Athens, GA, U.S.A.) gave a presentation on studies that evaluated the effects of different food processing treatments on the toxicological properties of fumonisin present in corn-based foods using rodent bioassays. The studies found that extrusion processing was effective at reducing fumonisin toxicity, particularly when glucose was added to the corn prior to processing. In contrast, nixtamalization (an alkaline cooking method) effectively detoxified fumonisin-contaminated corn at lower contamination levels while reducing but not preventing toxicity at a higher contamination level. Postharvest control of mycotoxins was a subject of a review by Gerd Schatzmayr (BIOMIN Research Center, Tulln, Austria). His presentation focused on the use of clays and other agents to bind and inhibit absorption of mycotoxins present in feed. Other approaches discussed were the use of microbiological agents and enzymes to transform or degrade mycotoxins into forms of reduced toxicity.

estimate human and animal exposure to fungal toxins and the toxicological properties and public health consequences as a result of the presence of mycotoxins in food and feed. Because developing countries often lack the resources to prevent and control mycotoxin accumulation in agricultural commodities, populations in these regions of the world are at a higher risk of exposure to these natural toxins.12,13 Paul Turner (University of Maryland, College Park, MD) gave a presentation study that evaluated exposure of children living in Western Africa to aflatoxin-, deoxynivalenol-, and fumonisin-contaminated dietary staples. These studies found a possible association of consumption of mycotoxin-contaminated food with growth stunting and other health-related problems in these populations. Analice Kamala (University of Ghent, Ghent, Belgium) presented the results of a study that assessed exposure of infants from different regions of Tanzania to multiple mycotoxins (aflatoxins, deoxynivalenol, ochratoxin, zearalenone, fumonisins, T-2 toxin, and HT-2 toxin) present in corn, an important dietary staple for these populations. The results of this study indicate that exposure varied among the different agroecological regions of Tanzania and that children receiving corn-based complementary foods in Tanzania are at a high risk of exposure to multiple toxins, particularly aflatoxin and fumonisins. Two presentations in this session were given on the identification and use of biomarkers for estimating exposure to fungal toxins. The first, delivered by Michele Solfrizzo [Institute of Sciences of Food Protection, National Research Council (CNR), Bari, Italy], focused on identification and use of urinary biomarkers in humans and animals for estimating exposure to the major mycotoxins [aflatoxin B1, ochratoxin A, zearalenone, fumonisin B1 (FB1), and deoxynivalenol]. Ronald Riley [Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Athens, GA, U.S.A.] discussed the results of a study that examined the use of urinary and blood biomarkers to determine exposure to FB1 in human populations in Guatemala. The results of this study as well as other research studies reviewed by Dr. Riley indicate that urinary FB1 levels and the red blood cell sphiganine/ sphingosine ratio are correlated and that both biomarkers could be used to predict when individuals are at an increased risk for exceeding the provisional maximum tolerable daily intake (PMTDI) established by the Joint Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO) Expert Committee on Food Additives (JECFA). Another major research finding is that individuals exposed to high levels of fumonisins from the diet experienced sphingolipid metabolism changes similar to those seen when animals and cell cultures were dosed with these mycotoxins alone. Several presentations reviewed the toxicological properties of mycotoxins, focusing on their specific target organs, such as the liver, kidney, and brain. Matthias Behrens (University of Munster, Munster, Germany) discussed studies that discovered that some mycotoxins (deoxynivalenol, moniliformin, citrinin, and zearalenone) have a high permeability to the blood−brain barrier, which potentially leads to high brain exposure to these toxins, while other toxins, such as ochratoxin A (OTA), reduce the viability and integrity of the blood−brain barrier. OTA, an International Agency for Research on Cancer (IARC) Group 2B carcinogen (possibly carcinogenic to human), is a frequent contaminant of cereal grains and other agricultural commodities.14,15 Genevieve Bondy (Health Canada) reported on studies that assessed the effects of OTA on rats with kidney 7018

DOI: 10.1021/acs.jafc.7b02909 J. Agric. Food Chem. 2017, 65, 7017−7020

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Hofmann-Sellier, and Journal of Agricultural and Food Chemistry editors for the invitation to publish papers corresponding to symposium presentations and facilitating the manuscript submission and review process. We hope that the following set of papers will constitute a valuable record and resource for continuing progress in the scientifically challenging and vitally important field of mycotoxin research.

Awareness of the significant impacts of mycotoxins on animal and human health has led to the development of analytical methods for their identification and surveillance in food and feed. The wide range of crops, commodities, and agricultural systems in which mycotoxins can be found presents a challenge for effective analyses. The fourth session of the symposium focused on tradition as well as state-of-the-art methods for detection of mycotoxins. Sarah De Saeger (University of Ghent, Ghent, Belgium) provided a comprehensive review of immunochemical methods used for rapid screening for mycotoxins. These methods include traditional enzyme-linked immunosorbent assays (ELISAs) and more recently developed multiplex fluorescent immunoassays that use quantum dots rather than enzymes for detection. The improvements in immunoassay sensitivity, stability, and selectivity through the use of nanobodies were discussed by Candace Bever (University of CaliforniaDavis, Davis, CA, U.S.A.). Nanobody-based techniques differ from the traditional ELISA because the antibodies are made in bacterial cells by expression of an engineered fragment of the variable antibody region. Hong-Li Guo (Tsinghua University, Beijing, China) gave a presentation on a new planar waveguide fluorescence immunosensor for rapid detection of aflatoxin M1 and melamine in milk. A new stable isotope dilution liquid chromatography−tandem mass spectrometry (LC−MS/MS)based method for detecting at least 12 mycotoxins in a variety of human and animal food and feed products was highlighted in a presentation by Kai Zhang [United States Food and Drug Administration (U.S. FDA), College Park, MD, U.S.A.]. The benefits of such a method include sensitivity, selectivity, and ability to detect and quantify a variety of analytes in a single analysis. The final presentation in this session, given by Veronika Nagl (BIOMIN Research Center, Tulln, Austria), focused on the tools to determine the identity, occurrence, and toxicity of masked mycotoxins. Regulations relating to mycotoxins have been established in over 100 countries to protect humans and animals from exposure to these hazardous compounds.16 Factors that play a role in the decision-making process of setting limits for mycotoxins include the availability of toxicology and occurrence data, procedures for sampling and analysis, and socio-economic factors. The final two presentations of the symposium discussed regulation of mycotoxins in Canada and the U.S. Genevieve Bondy (Health Canada, Ottawa, Ontario, Canada) outlined the different federal agencies in Canada that research and regulate mycotoxins, Canadian involvement in committees responsible for international standard setting for mycotoxins and other chemical contaminants in food, surveillance and monitoring activities in Canada, the considerations involved in setting maximum levels for chemical contaminants in food, and Canadian regulations and maximum levels governing mycotoxin residues in food. Mycotoxin regulations in the U.S. were described in a presentation by Henry Kim (U.S. FDA, College Park, MD, U.S.A.). In his talk, Dr. Kim discussed the regulatory authority and role of the U.S. FDA in ensuring the safety of the U.S. food supply, factors that impact establishment of regulatory limits for chemical contaminants, such as mycotoxins, approaches for controlling mycotoxins, and regulatory limits for several of the mycotoxins of public health concern. We thank the ACS Division of Agricultural and Food Chemistry for sponsoring the symposium and the symposium speakers and attendees for their informative presentations and lively discussions. We are grateful to Thomas Hofmann, Ivonne

Lauren S. Jackson*,† Dojin Ryu‡ †

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Division of Food Processing Science and Technology, Office of Food Safety, Center for Food Safety and Applied Nutrition, United States Food and Drug Administration, 6502 South Archer Road, Bedford Park, Illinois 60501, United States ‡ School of Food Science, University of Idaho/Washington State University, 875 Perimeter Drive, MS 2312, Moscow, Idaho 83844-2312, United States

AUTHOR INFORMATION

Corresponding Author

*Telephone: 708-924-0616. Fax: 708-924-0690. E-mail: lauren. [email protected]. ORCID

Lauren S. Jackson: 0000-0001-6246-700X Dojin Ryu: 0000-0003-3424-1163 Notes

The authors declare no competing financial interest.

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REFERENCES

(1) Bhat, R.; Rai, R. V.; Karim, A. A. Mycotoxins in food and feed: Present status and future concerns. Compr. Rev. Food Sci. Food Saf. 2010, 9, 57−81. (2) Council for Agricultural Science and Technology (CAST). Mycotoxins: Economic and Health Risks; CAST: Ames, IA, 1989; Task Force Report 116. (3) Council for Agricultural Science and Technology (CAST). Mycotoxins: Risks in Plant, Animal and Human Systems; CAST: Ames, IA, 2003; Task Force Report 139. (4) Binder, E. M.; Tan, L. M.; Chin, L. J.; Handl, J.; Richard, J. Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim. Feed Sci. Technol. 2007, 137, 265−282. (5) Rodrigues, I.; Naehrer, K. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins 2012, 4, 663− 675. (6) Streit, E.; Schatzmayr, G.; Tassis, P.; Tzika, E.; Marin, D.; Taranu, I.; Tabuc, C.; Nicolau, A.; Aprodu, I.; Puel, O.; Oswald, I. P. Current situation of mycotoxin contamination and co-occurrence in animal feedFocus on Europe. Toxins 2012, 4, 788−809. (7) Streit, E.; Naehrer, K.; Rodrigues, I.; Schatzmayr, G. Mycotoxin occurrence in feed and feed raw materials worldwide: Long-term analysis with special focus on Europe and Asia. J. Sci. Food Agric. 2013, 93, 2892−2899. (8) Pinotti, L.; Ottoboni, M.; Giromini, C.; Dell’Orto, V.; Cheli, F. Mycotoxin contamination in the EU feed supply chain: A focus on cereal byproducts. Toxins 2016, 8, 45. (9) Vardon, P. J.; McLaughlin, C.; Nardinelli, C. Potential economic costs of mycotoxins in the United States. In Mycotoxins: Risks in Plant and Human Systems; Council of Agriculture, Science and Technology (CAST): Ames, IA, 2003; CAST Task Force Report 139, Chapter 10, pp 136−142. (10) Mitchell, N. J.; Bowers, E.; Hurburgh, C.; Wu, F. Potential economic losses to the US corn industry from aflatoxin contamination. Food Addit. Contam., Part A 2016, 33, 540−550. (11) Vaclavikova, M.; Malachova, A.; Veprikova, Z.; Dzuman, Z.; Zachariasova, M.; Hajslova, J. ‘Emerging’ mycotoxins in cereals

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processing chains: Changes of enniatins during beer and bread making. Food Chem. 2013, 136, 750−757. (12) Wu, F. Mycotoxin risk assessment for the purpose of setting international regulatory standards. Environ. Sci. Technol. 2004, 38, 4049−4055. (13) International Agency for Research on Cancer (IARC). Mycotoxin Control in Low- and Middle Income Countries; Wild, C. P., Miller, J. D., Groopman, J. D., Eds.; World Health Organization (WHO) Press: Geneva, Switzerland, 2015; IARC Working Group Report 9, https://www.ncbi.nlm.nih.gov/pubmed/27030861 (accessed June 19, 2017). (14) International Agency for Research on Cancer (IARC).. Practical approaches to control mycotoxins. IARC Sci. Publ. 2012, 158, 131− 146. (15) International Agency for Research on Cancer (IARC). Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins; IARC: Lyon, France, 1993; IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 56. (16) van Egmond, H. P.; Schothorst, R. C.; Jonker, M. A. Regulations relating to mycotoxins in food. Anal. Bioanal. Chem. 2007, 389, 147− 157.

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