The risk of mycotoxins in foods – factors affecting production and control measures

This article is an introduction to mycotoxins, providing general information on mycotoxin potential health effects, control measures and due diligence for businesses. Mycotoxins are ubiquitous in nature. According to the Food and Agriculture Organisation of the United Nations (FAO), at least 25 per cent of the world’s food crops are contaminated with mycotoxins1.

A simple definition for mycotoxins is not straightforward as the group includes a range of different chemical compounds with different modes of action. One definition is as follows: “Low molecular weight, secondary metabolites of certain filamentous fungi that are toxic to animals and humans at low levels.” As the definition suggests, not all species of fungi produce mycotoxins and not all fungal toxins are classified as mycotoxins. For example, Penicillin that is toxic against bacteria is considered as an antibiotic.

Aspergillus spp, Fusarium spp and Penicilium spp are the three main mycotoxin–producing fungi of concern with regard to food safety but they are not the only ones. Alternaria spp, as well as Claviceps spp, are another two genera that can also infect crops and produce mycotoxins likely to be present in food commodities.

Why are mycotoxins of concern?

Mycotoxins can have a range of health effects on animals and humans. Toxicity can be acute or chronic. Acute mycotoxicoses is likely to be rare in humans in European countries. However, chronic toxicity can be of concern, as it can be induced with consumption of low quantities of mycotoxins over a long period of time. Any adverse health effects caused in this way may not be easily associated with the causal factor. The risk to the individual depends upon their age, gender and health state – for example, infants, children and immunosuppressed individuals may be more susceptible to the effects of some mycotoxins.

The likelihood of a health risk when mycotoxins in foods are consumed is assessed by consumers’ potential exposure to mycotoxins and their possible toxic effects, rather than the inherent hazard associated with the mycotoxin itself. These risk assessments are performed by international bodies such as the European Food Safety Authority (EFSA) and the Joint Expert Committee on Food Additives (JECFA) and national regulatory organisations such as the UK Food Standards Agency. Risk assessments acknowledge that ‘the dose makes the poison’ as observed by Paracelsus in the 15th century. The risk assessment takes into account available information in scientific literature, including toxicological studies, the results of national research and survey programmes, as well as epidemiological data and monitoring occurr – ence data.

In the interest of consumer protection, the European Commission set maximum legal levels2 (this regulation has been amended since it was issued) for a number of mycotoxins on the basis of their toxicity and their contribution to consumers’ diets, as well as on the ALARA principle (As Low As Reasonably Achievable).

According to the ALARA principle, maximum legal levels should be set at the lowest level that can be reasonably achieved by food producers and manufacturers using good practices. This is because elimination of mycotoxins is not possible as they are naturally occurring and climate-dependant to a great extent. Additionally, special limits exist for food commodities likely to be consumed by vulnerable population groups such as infants and toddlers.

What are the different types of mycotoxins?

The main mycotoxins of interest as regards food safety are:

Aflatoxins, produced by Aspergillus spp in warm and humid climates. Crops that are frequently affected include cereals such as maize, oilseeds including peanuts (groundnuts), various spices, figs and other dried fruit and tree nuts such as hazelnuts, almonds, pistachios and Brazil nuts. The toxin can also be found in the milk of animals that are fed contami – nated feed, in the form of aflatoxin M1. Aflatoxins, and in particular aflatoxin B1, are genotoxic and carcinogenic and they can cause liver cancer in humans.

Ochratoxin A, produced by Aspergillus spp and Penicilium spp. Contamination of food commodities including cereals and cereal products, coffee, dry vine fruits, wine and grape juice, spices and liquorice occurs worldwide. Ochratoxin A is common in warm as well as temperate climates, including the UK, where it can be formed in grain during storage. Ochratoxin A causes a number of toxic effects in animal species, the most sensitive and notable effect being kidney damage. It may also have an effect on foetal development and on the immune system.

Patulin, produced by Aspergillus spp and Penicilium spp. The toxin can be present in mouldy fruits and grains, usually found in apples and apple products. Patulin has been shown to have various toxic effects such as harm to the immune system and gastrointestinal tract.

Fusarium toxins, including deoxynivalenol (DON), zearalenone (ZON), fumonisins and T2 & HT2.

• DON is also known as vomitoxin because the main symptom associated with acute toxicity is vomiting. Diarrhoea, nausea and headaches have also been reported. It is most likely to be present in cereal grains such as wheat, barley, oats, rye and maize and cereal-based products such as bread and breakfast cereals
• Fumonisins are mainly present in maize grains and maize-based products and they have been related to oesophageal cancer in humans and to liver and kidney toxicity in animal species. The most important toxin of the group is fumonisin B1
• ZON is also produced in cereals such as wheat, maize and barley and products thereof. It is estrogenic, causing changes in the reproductive system
• T2 & HT2 can have immunological and haematological effects. Similarly to other Fusarium toxins they occur mainly in cereal grains and cereal – based products, notably oats

Maximum legal levels are set for all of the aforementioned mycotoxins (except T2 & HT2) in European legislation. However, no limits exist for other toxins such as Alternaria toxins and ergot alkaloids.

Alternaria toxins are common in fruits such as tomatoes, melons, apples, grapes and olives, oilseeds, cereals and vegetables. A recent scientific EFSA opinion has indicated that alternariol (AOH) and alternariol monomethyl ether (AME) are carcinogenic whereas AOH, AME, tenuazonic acid (TeA) and altertoxins (ATX)) are fetotoxic and teratogenic in rats. In addition, it has been suggested that in certain areas in China Alternaria toxins in grains might be responsible for oesophageal cancer.

Ergot alkaloids are produced by fungi of all species of the Claviceps genus, most notably by C. purpurea, which parasitise the seed heads of living plants (mostly cereals and grasses) at the time of flowering. The fungus replaces the developing grain or seed with a wintering body, known as ergot, ergot body or sclerotium. Ergot is ubiquitous, but is more common in seasons with heavy rainfall and wet soils. Rye and triticale are the most susceptible plant species because they have open florets.

Ergotism has been known since the Middle Ages when St Anthony’s fire disease occurred in a village in France as a result of consumption of highly contaminated grain. Typical signs of ergotism are gangrene and/or hallucinations and convulsions. At lower levels of contamination, ergot alkaloids can cause vasoconstriction and reproductive effects. Ergotism is not reported in humans nowadays but it is occasionally reported in animals.

What factors affect the production of mycotoxins and how can the levels be reduced?

Fungi present in the soil colonise plants before harvest and under favourable climatic conditions, mycotoxins are produced. Different fungal species may have different environmental requirements for growth. The requirements might be different even for species belonging to the same genera. For example, Fusarium poae has been associated with dry and warm conditions, F. graminareum with warm and humid con – ditions and F. avenaceum and F. culmorum with cool and humid conditions3. F. culmorum and F. graminareum are the most commonly found fungi species in UK cereal crops4. The different growth requirements result in a different geographical distribution of fungi species across the globe. Scientists have recently started looking into the effects that climate change can have in this distribution.

In the UK, heavy rainfall during flowering helps the fungus spread its spores and infect crops. Once infection has occurred, warm and wet climatic conditions enhance fungal germination and growth. Rainfall at the crop ripening stage allows for further fungal growth and mycotoxins production to occur5.

Several scenarios for climate change exist for the UK, one of which is that the weather will become warmer with wetter winters and drier summers3. It is unclear at the moment how this climate change can affect the production of mycotoxins by Fusarium spp. One of the possible implications is that the inter-crop period will become drier increasing the survival of the fungi in the soil due to lack of competition by saprotrophic fungi and thus increasing subsequent crop infection3. Nevertheless, weather is not the only factor affecting the production of mycotoxins in the field. Other factors include the host plant species and varieties, agronomic practices such as crop rotation, the use of fungicides (recent scientific evidence suggests that the use of fungicides or other pesticides may actually increase the levels of mycotoxins as it imposes stress onto the plant making more vulnerable to fungal infections), tillage and lodging and the time of harvest, as well as the presence of weeds and insects.

Crop rotation is important because the crop debris remaining in the field may contain the fungi inoculum that will contaminate the crops. In the case of Fusarium spp, wheat and maize as a preceding crop can increase the extent of crop infection and subsequently the levels of mycotoxin production.

In addition to the above, the quality of the soil and the presence of insects can affect the physiological state of the crop allowing or preventing fungal infection, i.e. if the host plant is stressed, infection becomes easier.

Fungi may also infect the food product during storage mainly when previous crop debris remains in the storage facilities. Regardless of the stage at which fungal infection takes place, mycotoxins can occur during storage throughout the food chain. In order to avoid mycotoxin production during storage, crops need to be dried as soon as possible after harvest so that the water activity within the product is reduced adequately and it is not available to the fungus in such quantities that would allow its growth and the production of mycotoxins. Additionally, the air circulation within the storage facilities should be adequate to prevent a temperature increase in stored (especially wet) grain that would favour fungal growth. Storage facilities and transport containers need to be clean dry, well aerated and pest-proof.

Knowledge of how different factors affect the production of mycotoxins allows the agricultural industry to adapt agronomic practices to reduce levels of mycotoxins in foods. Codes of practice (COP) on the prevention and reduction of the mycotoxins risk in food products have been produced by Codex5 and the European Commission. The Food Standards Agency has also produced a COP for the prevention and reduction of Fusarium toxins in cereals and OTA in stored cereals6,7.

How are mycotoxins in foods detected?

Mycotoxins cannot be detected by sight, odour or taste. Absence of visible mould does not mean that mycotoxins are not present, although, in the case of ergot contamination the presence of sclerotia (ergot bodies) in grain is visible, clearly indicating the presence of ergot alkaloids. Moreover, mycotoxins are quite stable compounds and once formed they remain in the product throughout its life (some food processes may result in chemical structure changes and formation of hydrolysed and bound forms of mycotoxins).

For these reasons, it is very important for all food business operators (FBOs) to take all necessary measures to prevent or reduce the presence of mycotoxins in food. Complete elimination of mycotoxins is not possible because, as previously explained, they are naturally occurring and climate-dependant to a great extent. Therefore, there is an onus upon FBOs to sample and test their products for mycotoxins in order to satisfy themselves that they are compliant with legislation. This testing can also be used as due diligence evidence in case contamination is found when the product is on the market. A lot of progress has already been done within the UK industry to understand and reduce the levels of mycotoxins in food.

Testing for mycotoxins involves sampling and analysis with the former being a crucial step. This is because distribution of mycotoxins in food is heterogeneous and it can be concentrated in a few ‘hot spots’ rather than spread evenly throughout the food. In order to get a representative sample, indicative of the actual product contamination, a number of small samples (incremental) should be taken from throughout the batch, which will then be mixed together to form the aggregate sample that will be sent to the analytical laboratory for testing. The analytical method to be used should comply with the performance parameters specified in legislation where applicable8. The full analytical procedure, including the sample preparation should be accredited with the United Kingdom Accreditation Service (UKAS).

The analytical result corrected for recovery and minus the measurement of uncertainty associated with the analytical result is used to check compliance for official control purposes (Figure 1).

For enforcement purposes, the sampling procedures also specified in legislation8 are used and the samples taken (official control samples) are sent to an Official Control Laboratory for analysis. Each official control sample is then split into three portions: the enforcement sample (used for enforcement purposes), the defence sample (analysed if the food business operator disputes the result of the first test) and the reference sample which is analysed in case the two previous results are conflicting and overrules all previous results.

Rapid test kits exist for many mycotoxins and can be used by the FBOs to assess the levels of mycotoxins in foods.

Conclusion

In conclusion, mycotoxins are natural contaminants that can be found in a wide range of food commodities. Due to their natural presence in the food as well as to their dependence on weather conditions, they cannot be completely eliminated. However, they can be controlled with good agricultural and manufacturing practices. Maximum legal levels exist to protect consumers from the adverse health effects associated with mycotoxins.

References

1. FAO (2012). Mycotoxins. Available at: http://www.fao.org/food/foodsafety- quality/food-safetyquality/ topical-issues/mycotoxins/en / [Accessed 27 Feb 2012]

2. Anonymous (2006a). Regulation (EC) 1881/2006

3. West J.S., Holgate S., et al (2011). Impacts of changing climate and agronomic factors on fusarium ear blight of wheat in the UK. Fungal ecology, in press, DOI: 10.1016/j.funeco.2011.03.003

4. HGCA (2012). Cereal Disease Encyclopedia – Fusarium. Available at: http://www.hgca.com/ minisite_manager.output/3613/3613 /Cereal%20 Disease%20Encyclopedia/Diseases/ Fusarium%20(Foot%20Rot, %20Seedling%20Blight,%20Ear%20 (Head)%20Blight).mspx?minisiteId= 26 [Accessed 28 Feb 2012]

5. Codex (2003). Code of practice for the prevention and reduction of mycotoxin contamination in cereal, including annexes on ochratoxin A, zearalenone, fumonisins and trichothecenes

6. FSA (2007a). The UK code of good agricultural practice to reduce Fusarium mycotoxins in cereals. Available at [http://www.food.gov.uk/ multimedia/pdfs/fusariumcop.pdf [Accessed 27 Feb 2012]

7. FSA (2007b). The UK code of good storage practice to reduce ochratoxin A in cereals. Available at: http://www.food.gov.uk/multimedia /pdfs/ochratoxinacop.pdf [Accessed 28 Feb 2012)

8. Anonymous (2006b). Regulation (EC) 401/2006

9. EMAN (2012). Mycotoxins basic factsheets. Available at: http://www.mycotoxins.org/ [Accessed 27 Feb 2012]

10. Anonymous (2006c). Commission Recommenda tion on prevention and reduction of Fusarium toxins in cereals and cereal products. L 234/35