Published: 13 May 2013
CSIRO Animal, Food and Health Sciences
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Mycotoxins are toxic secondary metabolites produced by filamentous fungi that may occur in almost all food commodities but particularly in cereals, oilseeds and nuts. They are recognised as an unavoidable risk and are found in the world’s most important food and feed crops, including maize, wheat, and barley. When present in foods in sufficiently high levels, mycotoxins pose a significant food safety risk and health hazard. Besides negative health impacts, mycotoxin contamination of food and feeds has a major worldwide economic impact. Mycotoxin contamination of foods is the subject of increasing international importance due to a number of worldwide issues, including globalisation of food trade, global food security and climate change. Innovative strategies to meet the menace of mycotoxin contamination are required, and a greater understanding of the ecology of mycotoxigenic fungi and the molecular regulation of mycotoxin production may aide in the development of such strategies.
Fungi are ubiquitous in nature and are a normal part of the microflora of worldwide food supplies. They can colonise food throughout the food chain from preharvest to storage wherever favourable conditions prevail. Some of these fungi are able to produce mycotoxins; the most important mycotoxigenic fungi belong to the genera Aspergillus, Fusarium and Penicillium. Thousands of mycotoxins have been identified, but only a few are a food safety risk and have an impact on global agriculture1. Major mycotoxin classes are aflatoxins, produced by Aspergillus flavus and Aspergillus parasiticus; fumonisins, produced by Fusarium verticillioides; trichothecenes, most importantly deoxynivelanol, produced by Fusarium graminearum; and ochratoxins, produced by Aspergillus ochraceus, Aspergillus carbonarius and Penicillium verrucosum. A wide range of commodities can be contaminated by these mycotoxins (Table 1). Exposure to mycotoxins may cause diverse and powerful toxic effects leading to both acute and chronic disease, ranging from liver and kidney damage, cancer, immunosuppression and childhood stunting (Table 1). These diseases are referred to as mycotoxicoses and the symptoms are dependent upon the type of mycotoxin, the concentration and length of exposure, and characteristics of the individual exposed, such as genetics, age, health and gender. Other factors contributing to disease development include synergies with other diseases and mycotoxin co-contamination food and feed2. The main route of exposure to mycotoxins is through ingestion of plant derived contaminated foods, however exposure may also occur through carryover of mycotoxins and their metabolites in animal products such as milk, meat and eggs or through inhalation of air and dust containing toxins3,4.
The true cost of mycotoxin contamination is difficult to estimate due to the complexity of the issue and its effect throughout the food chain on numerous stakeholders. Obvious costs include health impacts, crop losses and reduced animal productivity. Aflatoxins alone may cause up to 150,000 deaths worldwide per annum from liver cancer, and many more when the synergistic effect of hepatitis B virus is taken into account5. Other costs from mycotoxin contamination are incurred through efforts by producers to improve production, storage and handling to minimise the risk of mycotoxin contamination6. With over 100 countries having regulations regarding levels of mycotoxins in the food and feed industry7, there are significant costs associated with monitoring, enforcing and analysing at-risk commodities. There are also social costs associated with the loss of consumer confidence in the safety of food products.
In developed countries, stringent food safety regulations and monitoring ensures low levels of mycotoxin exposure in the population, however this is not the case in developing countries. In developing countries, the lack of infrastructure, the prominence of subsistence farming systems, the lack of irrigation, and inadequate drying and storing facilities results in chronic exposure to mycotoxins in the diet and the risk of serious health problems. The costs of these health problems include mortality and morbidity, as well as the more intangible costs of pain, suffering, anxiety, and reduction in quality of life.
Globalisation of food trade has several potential impacts on mycotoxin contamination in food and feeds. It possibly can extend the impact of mycotoxin contamination in food supplies beyond local communities. Mycotoxin exposure in humans and other animals, previously dictated by local factors such as crop production, climatic conditions and agronomic practices, is now affected by international food trade potentially distributing mycotoxin contaminated crops globally. The use of strict mycotoxin regulations on commodities for importation by developed countries reduce exposure risks in the importing countries, however the complexity and volume of international trade, importing corporations lacking accountability, greater opportunities for intentional fraud and the lack of enforcement tools, mean that there remains a potential mycotoxin food safety risk8. These strict mycotoxin regulations also have a significant economic impact on developing countries9. For example, a World Bank study estimated that the European Union regulations on aflatoxins cost Africa $750 million each year in exports of cereals, dried fruit and nuts10. Strict international mycotoxin regulations may also inadvertently result in higher exposure in developing countries because only the best quality foods are exported, leaving poorer quality, mycotoxin contaminated commodities for local consumption11.
Mycotoxin production on a food commodity is greatly influenced by environmental factors, most importantly temperature, relative humidity, insect attack, and stress conditions of the crop12. Global climate change with warmer temperatures and more extreme rainfall and drought events are likely to increase the threat of mycotoxins to human health12–14. Climate change effects on fungal colonisation and mycotoxin production should be assessed on a case-by-case basis, as optimum temperature and relative humidity for growth and mycotoxin formation vary between fungi12. In general, however, warmer temperatures with greater extremes in rainfall and drought events will increase plant stress, predisposing crops to fungal infection and mycotoxin contamination. Additionally, warmer temperatures may increase insect activity facilitating the establishment of mycotoxigenic fungi, through altered insect population growth rates, increased insect voltinism, altered crop-pest synchrony, and altered geographical ranges of important pest species14.
The costs of mycotoxin contamination of food commodities will significantly hamper the world’s ability to address the challenge of global food security. As defined by the World Health Organization, global food security exists “when all people at all times have access to sufficient, safe, nutritious, food to maintain a healthy and active life”15. Clearly, mycotoxin contamination of food commodities will affect the provision of safe and nutritious foods. The Food and Agricultural Organization (FAO) estimates that 25% of the world’s food crops are significantly contaminated with mycotoxins and that in the range of 1 billion tonnes of food is lost worldwide due to mycotoxins16.
Mycotoxin contamination of food and feeds remains a food safety risk of worldwide significance that has major economic impacts in both developed and developing countries. Various approaches have been put forward to reduce the impact of mycotoxins in food, and have had varying degrees of success: biocontrol by competitive exclusion, plant breeding and genetics, improved agricultural practices, increased irrigation, improved sorting, drying and storage techniques, dietary interventions including specific clays and antioxidants and, specifically for aflatoxin, immunisation against hepatitis B6. A greater understanding of the interactions between mycotoxigenic fungi and their host plants, and the use of genomic and transcriptomic information may assist in improving existing intervention strategies and may also lead to other interventions. Whole-genome sequences are available for A. flavus, F. verticillioides and F. graminearum17–19, and research is at a point that allows an examination of the similarities and differences in molecular mechanisms that regulate mycotoxin biosynthesis20. These whole-genome sequences have provided reference databases for genomic, transcriptomic and proteomic analyses that have revealed complex transcriptional and epigenetic regulation of mycotoxin biosynthesis.
It is important that strategies aimed at reducing the risk of mycotoxin contamination of human food and animal feed be implemented, especially in the light of global issues such as international food trade, food security and climate change.
Nai Tran-Dinh joined CSIRO in 2002 as a postdoctoral fellow and is currently a project leader with research interests in mycotoxigenic moulds. He has expertise in microbiology and molecular biology, and has applied these skills in a variety of food safety/spoilage research areas. He has worked on and led projects investigating the physiology, ecology, taxonomy, biochemistry, mycotoxigenic potential and understanding relationships between strains of fungi from the agriculturally important fungal genera of Aspergillus, Fusarium and Alternaria. He has worked extensively in the area of Aspergillus flavus/parasiticus infection and aflatoxin contamination in peanuts and other crops. This work has included investigating infection cycles, fungal population surveys from crops and soils, mycotoxin production, biological control of aflatoxin contamination and differentiation and phylogeny of strains using molecular markers.
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