R.V. Bhat and J.D. Miller
Dr Ramesh V. Bhat is Assistant Director at the National Institute of Nutrition, Hyderabad, India.
Dr J. David Miller is Senior Research Scientist at the Plant Research Centre, Agriculture Canada, Ottawa, Ontario.
Historical aspects
Occurrence
Health implications
Economic Implications
Prevention and control
References
The experience of the past 25 years indicates that it is possible to maintain present food consumption levels by increasing overall food supplies in quantitative terms. However, in terms of providing food of the right quality which is nutritious and free from environmental contaminants, the task ahead is challenging, particularly in highly populated parts of the world. Among food contaminants, mycotoxins will have greater consequences in terms of both human and animal health as well as economics.
Mycotoxins are substances produced by moulds that contaminate various agricultural commodities either before harvest or under post-harvest conditions. In addition to the various moulds occurring in crops which are improperly stored, certain plant diseases are responsible for the production of mycotoxins. Different weather conditions, such as unseasonable rains at the time of flowering or cyclones and droughts during harvest and post-harvest stages; mould growth; and mycotoxin contamination can also pose serious problems.
Mycotoxins have received considerable attention especially over the last three decades. Mycotoxicology is currently a subject of international importance. The problem of mould damage and the hazard of consuming damaged grains have been recognized since historical times. In areas of the Indo-Gangetic plains, for instance, traditional farmers have practised appropriate post-harvest measures to preserve crops. Expressions like "dry the grains well and keep dry grains dry" have been passed from one generation to the next. The problem of ergotism resulting from the infestation of rye by Claviceps has been known since biblical times and is now recognized as having been an important cause of human mortality in medieval Europe. The use of wheat, which is highly susceptible to Fusarium species producing trichothecenes, increased during this period and has been linked to the plague epidemics of the time. During the first half of this century, the possibility of human diseases occurring as a result of the consumption of mould-damaged rice and wheat was raised in Japan and other Asian countries. In the USSR, there was also awareness of risks from eating overwintered millet. However, the serious worldwide concern about mycotoxins began in the early 1960s after it was discovered in the United Kingdom that Turkey "X" disease is caused by aflatoxins.
Although there are many species of toxigenic moulds, only a few mycotoxins, particularly those affecting cereals (maize, wheat, barley, oats and rice) and groundnuts, are considered to be significant for humans. The most well-known mycotoxin, the potent human hepatocarcinogen aflatoxin, is produced by Aspergillus flavus and A. parasiticus. These moulds occur in warm climates and produce aflatoxin in drought-stressed maize and groundnuts in the field. They also affect these crops and many other commodities (copra, cottonseed, pepper) which are stored under improper conditions of temperature and humidity.
There are 24 toxigenic species of Fusarium which are increasingly viewed as having an important effect on human and animal health. F. graminearum, which causes head blight and ear rot, produces a variety of potent mycotoxins including deoxynivalenol, zearalenone and fusarin C. F. sporotrichioides produces T-2 toxin and related compounds which were responsible for the large-scale human toxicosis in Eastern Europe noted above.
Epidemics of Fusarium head blight and maize ear rot are chronic in cereal-growing areas of Asia as well as parts of Africa and South America. Public health authorities in these areas report acute human toxicosis from deoxynivalenol (Bhat et al., 1989). The effect of chronic exposure to trichothecenes (which are immunosuppressors) is not known. Of great concern at the moment are the toxins of F. moniliforme, namely fusarins and fumonisins. The presence of these toxins in maize in southern Africa and parts of China may explain the high rates of oesophageal cancer in these regions. There are a number of other species of moulds, particularly Aspergillus and Penicillium, that produce mycotoxins under poor storage conditions. Ochratoxin is thought to be the most important mycotoxin in this category.
There is no information available on the precise extent of __contamination and co-occurrence of various mycotoxins in different commodities on a worldwide basis. Data from the Joint UNEP/FAO/WHO Food Contamination Monitoring Programme1 indicated that "much of the grain monitored in the United States and the Soviet Union, and to a lesser extent in Guatemala and Kenya, contained 90th percentile levels above 5-20 m g/kg, the regulatory levels for foods in most countries". Data from 185000 samples of peanuts from Brazil, Guatemala, Ireland, Mexico, Switzerland, the United Kingdom, the United States and the USSR indicated that, for all but 1 percent of the samples, the 90th percentile levels of aflatoxins were less than 20 m g/kg (Jelinek et al., 1989).
[1 The Joint UNEP/FAO/WHO Food Contamination Monitoring Programme was initiated in 1976 and is an integral part of UNEP'S Global Environment Monitoring System (GEMS). The main objectives of the programme are to collect data on levels of certain chemicals and contaminants in selected foods a to disseminate the information to countries worldwide.]
Although there is little firm evidence, the results of these surveys suggest that in certain situations as much as 50 percent of the grain may be contaminated with mycotoxins. In certain years, the deoxynivalenol content in wheat was found to be more than 500 m g/kg in some countries (ibid.).
The poorest quality grain (where it can be spared) is used for animal feed. Animal feeds with ingredients such as oilseed cakes, peanut, cottonseed and coconut cake or corn grits often contain mycotoxins. Feed conversion to animal protein is always reduced by the presence of mycotoxins. In addition, mycotoxins have a negative effect on animal health and fertility is decreased. When animals ingest the contaminated feeds, some toxins can be metabolized and remain in milk, meat and eggs. The presence of mycotoxins in animal products such as aflatoxins and ochratoxins in milk, meat and eggs has been of concern in some countries (Rodricks and Stoloff, 1977). The levels of toxins such as aflatoxin and ochratoxins present in these secondary sources are much lower than those in agricultural commodities. However, their levels in these products, in particular milk, is strictly regulated in most developed countries. The effects of this source of toxins on human health may be modest in developed countries because of feed safety regulations and pooling of milk at dairies. However, in developing countries where animals are likely to consume mycotoxin-contaminated animal feeds and are milked individually at the household level, the levels of toxins can be higher. Despite this, mycotoxin occurrence in animal products in some high-risk areas is being paid little attention.
The consumption of mycotoxin-contaminated commodities is related to several acute and chronic diseases in humans as well as in animals. While the exact cause and effect relationship has been established for only a few of the diseases, speculation about the role of mycotoxins in the aetiology of various illnesses has been based on circumstantial evidence in other cases. The acute diseases for which there is some evidence of an association with mycotoxins include: aflatoxic hepatitis in India and Kenya; enteric ergotism in India; vascular ergotism in Ethiopia; and deoxynivalenol mycotoxicosis in India and China. A common feature in all these outbreaks has been the involvement of staple foods such as corn, wheat or pearl millet, following unseasonable rains or drought during either the growing season or harvest.
Among the mycotoxins, aflatoxins have been implicated in human diseases including liver cancer, Reye's syndrome, Indian childhood cirrhosis, chronic gastritis, kwashiorkor and certain occupational respiratory diseases in various parts of the world, particularly in African and Asian countries. In China, the Philippines, Thailand, Kenya, Swaziland and Mozambique, higher levels of aflatoxins in the food supply have been correlated with aflatoxins and their derivatives in human fluids which may be associated with liver cancer (Palmgren and Hayes, 1987). Fusarium toxins have been suspected to have a role in diseases such as Kashin Beck syndrome in the USSR, China and Viet Nam; Mseleni joint disease in southern Africa; endemic familial arthritis in India; alimentary toxic aleukia in the USSR; and oesophageal cancer in southern Africa. Ochratoxins have been associated with Balkan endemic nephropathy and urinary tract tumours (Berry, 1988). However, in most of these instances, conclusive evidence for the role of mycotoxins in disease causation has been lacking.
International trade in agricultural commodities such as wheat, rice, barley, corn, sorghum, soybeans, groundnuts and oilseeds amounts to hundreds of millions of tonnes each year (FAO, 1988). Many of these commodities run a high risk of mycotoxin contamination. Regulations on mycotoxins have been set and are strictly enforced by most importing countries, thus affecting international trade. For some developing countries, where agricultural commodities account for as much as 50 percent of the total national exports, the economic importance of mycotoxins is considerable.
There is a notable length of time between the purchase of the agricultural commodity at the village market of the exporting country and its arrival at the distribution centre of the importing country. The transport chain for agricultural commodities from village to port, from the port of the exporting country to that of the importing country as well as from the port to the distribution centre can be long. Furthermore, storage conditions at the farm level as well as during transport under adverse weather conditions may not always be satisfactory. For these reasons, there is considerable opportunity for mould and mycotoxin contamination of agricultural commodities to take place throughout the food system - from production to distribution and transport - and this may lead to economic losses (Bhat, 1988).
The exact figures for world economic losses resulting from mycotoxin - contamination may never be available. Apart from the obvious losses of food and feed, there are losses caused by lower productivity; losses of valuable foreign exchange earnings; costs incurred by inspection, sampling and analysis before and after shipments; losses attributable to compensation paid in case of claims; farmer subsidies to cover production losses; research, training and extension programme costs; costs of detoxification; etc. When combined, these costs may be staggering (Coulibaly, 1989).
Several preventive measures to minimize mycotoxin contamination in agricultural commodities have been attempted. These can be divided into three broad categories:
· plant breeding;
· good agronomic practices; and
· detoxification.
The problem of ergot contamination of cereals and millets has been successfully minimized in the past by cultivating varieties of rye, wheat and pearl millet that are resistant to the disease. The periodic re-emergence of the problem can be attributed to the release of varieties which are not resistant to ergot. However, there has been little success in providing resistant varieties of corn and peanut to minimize the problem of aflatoxins. Other agronomic approaches such as avoiding water stress, minimizing insect infestation and reducing inoculum potential have been suggested and are effective when the farmers can implement such practices. Following good agricultural practices during both pre-harvest and post-harvest conditions would, minimize the problem of contamination by mycotoxins such as aflatoxins, ochratoxin and trichothecene mycotoxins. These include appropriate drying techniques, maintaining proper storage facilities and taking care not to expose the grains or oilseeds to moisture during transport and marketing. The method of segregating contaminated, mouldy, shrivelled or insect-infested seeds from sound kernels has been particularly useful in minimizing aflatoxin contamination in peanuts.
Detoxification of aflatoxins in foods and animal feeds has been attempted in the past. For instance, Senegal has been operating commercial facilities to detoxify peanut cake contaminated with aflatoxins by the ammonia process. Any detoxification procedure must be tested for safety and efficacy and invariably results in increased handling and costs. In addition, the detoxified product has been considered suitable only for animal feed purposes and not for human consumption.
Several countries have introduced legislation concerning mycotoxins. Most of this legislation pertains to aflatoxins, ergot alkaloids, deoxynivalenol and ochratoxins. Although various legislative measures have yet to be harmonized among countries, the Codex Alimentarius Commission is making efforts to establish international guideline levels for mycotoxins, and aflatoxins in particular.
Mycotoxin control measures have been implemented for agricultural commodities entering international trade or located in countries with centralized or large-scale buying and distribution systems. However, in developing countries, where local food consumption or subsistence agriculture is practised by as much as 70 percent of the population, such measures would be difficult to implement. Because of the stringent mycotoxin control measures being maintained by those countries importing food grains and oilseeds, and because of the need for exporting countries to earn foreign exchange, the best of the commodities are often sold abroad while the substandard or contaminated commodities are retained for domestic use. Such a situation exacerbates the risk to human and animal health.
Continuous surveillance of high-risk agricultural commodities for contamination by selected mycotoxins and the monitoring of human population groups for diseases attributable to mycotoxins have to be carried out throughout the world to ensure a supply of safe food which is free from naturally occurring contaminants. The financial and human investments in this endeavour would be returned in terms of better human and animal health as well as reduced economic losses.
Berry, L. 1988. The pathology of mycotoxins. J. Pathology, 154: 301-311.
Bhat, R.V. 1988, Mould deterioration of agricultural commodities during transit: problems faced by developing countries, Int. J. Food Microbiology, 7(3): 219-225.
Bhat, R.V., Sashidhar, R.B., Ramakrishna.Y. & Munshi, K.L. 1989. Outbreak of trichothecene mycotoxicosis associated with consumption of mould damaged wheat products in Kashmir Valley, India. Lancet, I: 35-37.
Coulibaly, B. 1989. The problem of aflatoxin contamination of groundnut and groundnut products as seen by the African Groundnut Council. In D. McDonald & V.K. Mehan, eds., Aflatoxin contamination of groundnuts. Proceedings of the international workshop, p, 47-55, Patancheru, India, International Crops Research Institute for the Semi-Arid Tropics.
FAO. 1988. FAO Trade Yearbook, 1987, 41: 380. Rome, FAO.
Jelinek, C.F., Pohland, A.E. & Wood, G.E. 1989. Worldwide occurrence of mycotoxins in foods and feeds (an update. J. Assoc. Off. Anal. Chem., 72: 223-230.
Palmgren, M.S. & Hayes, A.W. 1987. Aflatoxins in food. In P. Krogh, ed., Mycotoxins in food, p. 65-95, London, Academic Press.
Rodricks, J.V. & Stoloff, L. 1977. Aflatoxin residues from contaminated feed in edible tissues of food-producing animals. In J.V. Rodricks, C.W. Hesseltine & M.A. Mehlman, eds., Mycotoxins and animal health, p, 67-79, Park Forest Hills, Illinois, Pathotox Publishers Inc.
