Reviews research on mycotoxins in organic food
Organic Food – The Hazard of Mycotoxins
by
Eleanor Riches
Formerly associated with the John Innes Centre, Norwich, Norfolk, UK.
Abstract
Organic food production is increasing annually. Some research has indicated that there may be an increase in the levels of mycotoxins, poisonous chemicals formed by pathogens of food crops, in organically grown produce. At present, an insufficient amount of research has been directed at safety issues of growing food organically. Toxins such as deoxynivalenol and aflatoxin are known carcinogens, which are produced by pathogens of wheat and maize, among other cereal products, and fruit such as apples, and must therefore be considered a threat to food safety. Well-funded research is required to allay fears amongst consumers who expect food to be safe and nutritious.
Introduction
Increase in demand for organically grown food has led to the conversion of some British farms to pesticide free oases. Organic principles include the growth of crops in a way that is beneficial to the environment, economical and, perhaps above all, with improved nutritional quality, being uncontaminated by dangerous chemicals, untainted by conventional inputs and safe for human consumption. Growing organically does improve the biodiversity in the soil and, according to some consumers, results in produce having a better taste. However, yield drops on conversion to organic production and opportunistic pathogens require vigilance to control, and some nutritional and disease controlling inputs in the form of manure and ‘acceptable’ fungicides are used. There are some concerns being raised about the apparently unquestionable safety of organically produced food. The reduction in the use of synthetic chemicals can be beneficial to the environment but nature is capable of forming some very powerful and dangerous chemicals of its own, and some attention to these with respect to food production and human health is required.
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Mycotoxins
Mycotoxins are poisonous chemical compounds produced by certain fungi that can occur in food have great significance in the health of humans and livestock. Since fungi produce them, mycotoxins are associated with diseased or mouldy crops; therefore, disease control is essential to eliminating this threat to food safety. The symptoms caused by ingestion of these mycotoxins can be acute, rapid illness or can have cumulative effects on health, including the induction of cancers and immune deficiency (FAO, 1997). The presence of mycotoxins in crops is not only a direct food safety problem but it threatens the competitiveness of agriculture in the world market and causes significant economic losses for many countries (FAO, 1997).
Mycotoxicoses
Mycotoxicoses are diseases resulting from the consumption of mycotoxins. The effects in domestic animals include allergic reactions, reproductive failure, loss of appetite, suppression of the immune system, decreased feed efficiency, and mortality (Khera et al., 1984; Ehling et al., 1997). Human suffering from mycotoxicoses includes ergot poisoning associated with ingestion of contaminated rye flour; cardiac beriberi associated with Penicillium moulds in rice (yellow rice toxins); and alimentary toxic aleukia associated with Fusarium moulds on overwintered wheat, millet, and barley (Kuiper-Goodman, 1994; Costantini et al., 2001). Several mycotoxins have been linked to increased incidence of cancer in humans (IARC, 1993).
Deoxynivalenol
The most common food-borne mycotoxins include: deoxynivalenol/nivalenol; zearalenone; ochratoxin; fumonisins; and aflatoxins. Deoxynivalenol and nivalenol are produced by Fusaria species and are toxic to humans and animals. The main commodities affected are cereals. Deoxynivalenol is a frequent contaminant of grains such as wheat, buckwheat, barley, oats, triticale, rye, maize, sorghum and rice (Ehling et al., 1997).
Zearalenone
Zearalenone is also produced by these species on maize and wheat and has been identified by the International Agency for Research on Cancer (IARC) as a possible human carcinogen (IARC, 1993). Another Fusarium produced toxin, fumonisin B1 is found on maize and is suspected as being a human carcinogen. Fumonisin B1 is also toxic to pigs and poultry and causes equine eucoencephalomalacia, a fatal disease of horses (Costantini et al., 2001).
Aflatoxins
Aflatoxins have been identified as potent human carcinogens that can also cause malfunctioning of the immune system. Among livestock, they are particularly toxic to chickens (FAO, 1997). Aflatoxins produced by the fungus Aspergillus flavus can infect crops, such as corn, cotton, peanuts and treenuts causing a potential food safety hazard and lowering their economic value (Smith, 2003). Contamination of tree nuts by aflatoxins produced from infection by the fungus Aspergillus flavus and A. parasiticus is a serious problem because of the stringent regulatory levels imposed for these toxins due to their potential threat to human health.
In 1993, the IARC assessed and classified naturally occurring mixtures of aflatoxins as class 1 human carcinogens (IARC, 1993). Residues of aflatoxins can occur in animal products, including milk. A derivative known as aflatoxin M has been found in human milk if the mother consumes food containing aflatoxin B1 (Costantini et al., 2001). It is clear that exposure to aflatoxins is hazardous to human health. For that reason, regulations governing the allowable concentrations of aflatoxin in food and feed are in place in several countries including Britain and the US (FSA, 2002; USFDA, 2002).
Alternaria
Alternaria sp. are important fungal contaminants of grain products secreting four classes of compounds that are toxic or carcinogenic to plants and animals and cause considerable economic losses to growers and the food-processing industry. Alternariol, alternariol methyl ether, altenuen and altertoxin are of concern as they have mutagenic activity, with 50% lethal dose values of 400, 400, 50 and 0.2 mg/kg of body weight in mice (Stack et al., 1996 a,b)
The presence of mycotoxins in grains and other staple foods and feedstuffs has serious implications for human and animal health. Many countries have enacted regulations stipulating maximum amounts of mycotoxins permissible in food and feedstuffs (USFDA, 2002). Most developed countries will not permit the import of commodities containing amounts of mycotoxins above specified limits. Mycotoxins, therefore, have implications for trade between nations. Prevention of fungal invasion of commodities is by far the most effective method of avoiding mycotoxin problems.
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Comparisons of Mycotoxin Content of Conventionally and Organically Grown Crops
Marx et al. (1995) carried out some comparative investigations on the mycotoxological status of both alternatively and conventionally grown crops. Rye and wheat were investigated for contamination by attacking pathogens. The mycotoxin deoxynivalenol was found at a mean level of 427 µg/kg in rye grown alternatively whereas the average level found in conventionally grown rye was
160 µg/kg. When the authors tested for zearalenone in wheat, an average of 6 µg and 24 µg per kg was detected in conventionally and alternatively grown crops respectively.
Although the growth of pathogens on crops prior to their use in foodstuffs is of interest, it is the health risks associated with the consumption of toxin-contaminated foods that are the most prominent concern for consumers. A study comparing organic and conventional foodstuffs in France monitored products including apples and cereals (Malmauret et al., 2002). The median levels of contamination were compared with the recommended maximum levels. Contamination of both conventional and organic wheat by deoxynivalenol was observed with a higher level in organic products (106 µg/kg compared with 55 µg/kg in conventionally grown wheat). There is a proposed maximum level of 50 µg/kg for contamination by the mycotoxin patulin in apple juice, and one of six samples of organic apple contained levels (1240 µg/kg) of patulin above this level. However, the median for organic apples was
211 µg/kg whereas the median for conventionally grown ones was 35.85 µg/kg. The design of these experiments involved only a few samples and therefore the results reveal no conclusive evidence as to whether conventional products are more or less safe than organic ones. Future studies are required to be directed towards determining toxin levels in foodstuffs that are to be available directly to the consumer, i.e. after processing and packaging. However, this study indicates that particular notice should be taken of apple/patulin and wheat/deoxynivalenol containing products.
Aflatoxins are also troublesome contaminants of the peanut. In a study of aflatoxin contamination of processed foods, the toxic contents in peanut butter from alternative and conventional shops indicated that products resulting from alternative production had higher contents of total aflatoxin and aflatoxin B1 (Gilbert and Shepherd, 1995).
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The Principles of Growing Organically
The primary aim of organic agriculture is to produce nutritious food in an environmentally beneficial manner. Organic food production is designed on the basis of using minimal external inputs, relying on natural cycles using crop rotations and nutrient recycling to provide the essential elements for the production of good crops. Soils with higher organic matter content also have higher biological activity which gives the soil greater capacity to compete with pathogens such as bacteria. Additional external inputs are viewed only as supplements to the system and would only be allowed in special circumstances. Plants themselves have protective mechanisms that can be structural, for example cuticle thickness or production of trichomes on tomato (Salisbury and Ross, 1992); and chemical, for example production of toxins like glucosinolates involved in resistance to downy mildew in brassicas (Osbourn, 1996a). In addition, microbial communities provide protection from pathogenic organisms both above and below ground through mechanisms such as competition for resources, parasitism, predation, inhibition of germination and production of antibiotics (Osbourn,1996 a,b). Furthermore, non-pathogenic micro-organisms can stimulate a plant immune response which can be reactivated rapidly when the plant comes into contact with pathogenic species. By selecting varieties with natural resistance to particular pests and diseases, the likelihood of pest and disease problems occurring and the need to control them subsequently can be significantly reduced. An increasing number of vegetable, fruit and cereal varieties with resistance to common pest and disease problems are now available.
Prevention rather than cure
The emphasis of organic farming is firmly on prevention rather than cure. Chemically synthesised pesticides are prohibited due to their disruptive effects on biological systems. However, under certain circumstances, with severe restrictions, recourse to inputs with pesticidal properties is allowed with prior justification for their use. In such circumstances organic farmers in the UK can choose from six different active ingredients, although one of these, rotenone, is currently suspended. All of these are permitted in conventional agriculture. Organic standards on pesticide use are constantly changing. The use of copper salts as fungicides is one such example. Due to evidence of their damaging effects to earthworms these compounds are scheduled to be prohibited in organic faming across Europe (Soil Association, 2001). Good management and attention to detail is critical for organic farmers and growers as they are not able to call on the curative measures available to conventional agriculture. This places a clear emphasis on preventative management with regard to pests and disease.
Inherent disease resistance is the first thing organic growers look for, knowing they cannot turn to mainstream fungicide products. There is often compromise between growing a high yielding variety and one with adequate disease resistance. According to the home-grown cereals authority (Henly, 2002) current research is aimed at growing wheat without chemical intervention, about which there is a dearth of information as research funding targeted to organic production remains scarce.
There is no doubt that further research into the functioning of natural cycles in agricultural ecosystems will help to improve the productivity and sustainability of organic farming systems.
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Organic Food Production
In one of the longest-running studies of its kind, Paul Maeder of the Research Institute of Organic Agriculture, Frick, Switzerland, and his colleagues compared plots of cropland grown according to organic and conventional methods. In each system, they grew potatoes, barley, winter wheat, beets, and grass clover. Overall, the organic systems were able to produce more with less energy and fewer resources, the researchers report. Yields were stable over time although organic farming methods produced crop yields that were, on average, 20% smaller than conventional crops. Soil fertility increased, however, and the organic soils were home to a larger and more diverse community of organisms (Maeder et al., 2002).
Although the ideals of the organic movement are attractive, concerns are being raised as to the viability of banning burgeoning technology from an industry which is required to feed a World population expected to reach 6.8 billion in the next 7 years (Geohive, 2003). According to Anthony Trewavas writing in Nature (2001), there are two features of organic farming which separate it from its conventional counterpart, these being that soluble mineral inputs are prohibited and synthetic herbicides and pesticides are rejected in favour of natural ones. An agricultural system based on these principles, however, results in a more costly product due to lower yields and inefficient land use. In addition, there are risks invoked by the higher dosages of ‘natural’ pesticides required. In a study by the Hudson Institute it was determined that First World pesticide use would increase several-fold under an organic system as these must be applied frequently and at higher rates. Sulfur, for example, is applied at nearly 35 pounds per acre, compared to 1.6 pounds per acre for synthetic fungicides. Copper sulfate, a widely used organic fungicide, is more toxic to people, small mammals, earthworms, birds and fish than its synthetic counterpart, Mancozeb™. It is also a permanent soil contaminant, like sulfur (Avery, 2001). In addition, if less effective fungicides are in use, there is a great concern over the production of food mycotoxins from contaminating fungi. Failure to use effective fungicides on organic farms has led to farms acting as repositories of disease (Eltun, 1996).
The trend in modern conventional agriculture is to use pesticides of low toxicity at levels just high enough to be effective. The alleged harmfulness of many banned agricultural chemicals to humans and the environment is a subject of scientific debate. Before the advent of modern chemical pesticides, farmers used various toxic substances such as arsenic salts. In the developing countries of humid, tropical regions, cultivation of health-giving and life saving crops of vegetables without the use of insecticides and fungicides is difficult or nearly impossible. Mycotoxins accumulate without the use of pesticides and are often much more harmful than any pesticide. Residues of pesticides applied to the young vulnerable plants decrease near harvest time, usually to undetectable levels. Mycotoxins, if fungal pathogens are allowed to become established, remain and accumulate. If an invasive micro-organism spreads into plant tissue, the plant also will make and release antimicrobial toxins, some of which may be more harmful to humans than the man-made chemicals that could have protected the plant (DeGregori, 1996). A balance may therefore be called for, between the use of conventional pesticides and organic techniques, to ensure the health of crops and prevent the proliferation of mycotoxins.
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Summary
The expansion of organic food production is beneficial for consumer choice and for farming income. Conventional wheat fetches under £60 per tonne, however, organic feed wheat has commanded a price of £175 per tonne and bread-making varieties fetched more that £200 per tonne (Henly, 2002). Some environmental benefits of organically producing food are clear in terms of the increase soil biodiversity and possible benefits to wildlife. There are, however, potential risks associated with the greater contamination of organic crops with fungal pathogens leading to the production of mycotoxins and ultimately their ingestion by humans. These risks have not been thoroughly evaluated and there is a necessity for this aspect of organic food production to be assessed with well-funded research. Consumers eat organically grown products as they are perceived to be more nutritious than conventionally grown produce, however, should their safety be called into question, the public will demand answers.
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