Most important parent mycotoxins for cereal products, their occurrence, primary fungus producer and mode of action
1. Introduction
Mycotoxins are secondary metabolites produced by a wide variety of filamentous fungi, including species from the genera
Occurrence of mycotoxin contamination in foods is more prevalent in the tropical and subtropical countries resulting in acute and chronic mycotoxicoses in humans and animals. Wild [3] reported that many West African countries, over 98% of the tested people were positive to aflatoxin-DNA adducts indicating aflatoxin exposure in the population. The importance of this situation is highlighted with an outbreak of aflatoxicosis as 2004 in Kenya [4] and a report on impaired child growth in Benin caused by post weaning exposure to aflatoxins [5]. Many of the developed countries have regulations for mycotoxins in grains and its products, because at least 60% of the food produced and consumed in the world originates from cereal crops such as rice, wheat, corn, barley,rye, sorghum and oats. However, the risk of mycotoxin exposures continues in the developing countries due to lack of food security, poverty and malnutrition [5, 6].
Mycotoxin | Commodity | Genus | Species | Disease/mode of action | |
Ergot alkaloids | Ergotamine, ergometrine | Cereals | Necrose of limbs – St. Anthony‘s fire | ||
Ergosine, ergocristine | Pearl millet | Vasoconstrictive properties | |||
Ergocryptine, ergocornine | Gangrenous and colvulsive ergotism | ||||
Aflatoxin | B1, B2 | Cereals, nuts | Carcinogenic | ||
(AFT) | G1, G2 | Spices, figs | Liver cancer | ||
(AFM) | M1, M2 | Milk | Immune suppressive | ||
Ochratoxin (OTA) | A | Cereals | Neurotoxic | ||
B | Wine | Nephrotoxic | |||
Coffee | Kidney damage and cancer | ||||
Spices | Immune suppressive | ||||
Type B trichothecenes | DON (Vomitoxin) | Cereals | ATA (alimentary toxic leukopenia) | ||
ADON, NIV | Immunotoxic | ||||
ANIV | Acute toxicity | ||||
Type A trichothecenes | T-2 | Small grains | Acute toxicity linked to ATA | ||
HT-2 | Cereals | Immunotoxic | |||
Immune system and hematological disorders | |||||
Zearalenone (ZEA) | Cereals | Estrogenic effects | |||
Reproductive disorders | |||||
Effects endocrine system | |||||
Fumonisin (FUM) | FB1 | Corn | Esophageal cancer | ||
FB2 | Cereals | Sphingolipid methabolism disruption | |||
Multiple crops | Immune suppression | ||||
Several approaches have been developed for decontamination of mycotoxins in foods [7, 8]. Principally, there are three possibilities to avoid the harmful effect of contamination of food and feed caused by mycotoxins:
prevention of contamination;
decontamination of mycotoxin-containing food and feed; and
inhibition or absorption of mycotoxin content of consumed food into the digestive tract.
The most obvious measure as to prevent mycotoxin production is in general to reduce the moisture content of the commodity to the equivalent of less than 0.65 water activity (e.g. for cereals <14.5% moisture by weight) direct after harvest. To minimize mycotoxin contamination can also be achieved as to limit bird and insect damage. Create also anaerobic conditions by storage and promote crop rotation to minimize the carry-over of moulds from one year to the next. Many of these recommendations can be found in documents of the Codex Alimentarius (CODEX STAN 193). Other useful documents are the codes of practice for the prevention and reduction of mycotoxin contamination in cereals, including annexes on OTA, ZEA, FUM and trichothecenes. Together with a suitable Hazard Analysis Critical Control Points (HACCP) and reliability procedures and following properly reporting systems such as RASFF (Rapid Alert System for Food and Feed) in Europe and RFR (Reportable Food Registry) in the US, health and safety measures in food and feed are optimum served by preventing and controlling the formation of mycotoxin.
The approach of prevention is doubtless also to breed cereals and other food and feed plants for resistance to mould infection and consequently exclude mycotoxin production. Particularly in breeding wheat and corn, significant improvement of resistance has been achieved. The slow-moving research however in the breeding field to culture resistant crops even through marker-assisted breeding (MAS),seems to be an endless task since up until now moulds have been a step ahead of breeders. The identification of microbial species (and genes coding enzymes degrading mycotoxins) allows transfer of these genes into plants and production of such enzymes by transgenic plants. In this way, the safety problems connected with the use of live microorganisms may be avoided. Another practical approach to prevention of mycotoxin contamination is the inhibition of the growth of molds and their production of mycotoxins. First, optimal harvesting, storage and processing methods, and conditions may be successful in prevention of mold growth. Although the primary goal is the prevention of mycotoxin contamination, mycotoxin formation appears to be unavoidable under certain adverse conditions. Treatment of grains by some chemicals to prevent mycotoxin formation is also possible but not desirable in view of a.o. the chemophobia of Europeans and the far-reaching legislation in the EU to restrict herbicides and pesticides with ‘REACH’ (REACH = Registration, Evaluation, Authorisation and restriction of Chemicals), effective as of 1 June 2007.
Most of these compounds work by inhibiting fungal growth. For example, approximately one hundred compounds have been found to inhibit aflatoxin production. Two extensively studied inhibitors of aflatoxin synthesis are dichlorvos (an organophosphate insecticide) and caffeine. As reported in reference [8] some surfactants have been found to suppress the growth of
the mycotoxin must be inactivated or destroyed by transformation to non-toxic compounds;
fungal spores and mycelia should be destroyed, so that new toxins are not formed;
the food or feed material should retain its nutritive value and remain palatable;
the physical properties of raw material should not change significantly; and it must be economically feasible / the cost of decontamination should be less than the value of contaminated commodity.
Mycotoxin decontamination by physical and chemical methods has been reviewed extensively in several papers [7, 9, 10]. Partial removal of mycotoxin may be achieved by dry cleaning of the grain and in the milling process, as well. Milling led to a fractionation, with increased level of mycotoxin in bran and decreased level in flour. The majority of mycotoxins are heat-stable so heat treatment, usually applied in food technology, does not have significant effect on the mycotoxin level. Efforts were made in several countries to find an economically acceptable way of destruction of mycotoxins into non-toxic products using different chemicals such as alkali and oxidative agents. Although such treatment reduces nearly completely the mycotoxin concentration, these chemicals also cause losses of some nutrients and such treatment is too drastic for e.g. grain destined for food uses. Many physical adsorbents have been studied and are available as commercial preparations as animal feed additives. However, many of these adsorbents can bind to only a small group of toxins while showing very little or no binding to others [9]. Although the different methods used at present have been to some extent successful, most methods have major disadvantages, starting with limited efficacy to losses of important nutrients and generally with high costs. Because the EU does not allow chemical treatment methods anyway, manoeuvrability is limited.
More recently, biological decontamination and biodegradation of mycotoxins with microorganisms or enzymes have been used [11, 12]. Many species of bacteria and fungi have been shown to enzymatically degrade mycotoxins [13-19]. In this case no harmful chemicals were used, so no significant losses in nutritive value and palatability of decontaminated food and feed occurred. Today, ruminants appear to be a promising potential source of microbes or enzymes for use in the biotransformation of fungi and/or there mycotoxins they create. Biological decontamination of fungi/mycotoxins by microorganisms is reviewed in some papers [8, 13, 16, 20, 21], however, there are no many reviews on decontamination of fungi/mycotoxins by microorganisms involved in food fermentation and its implications. Fermentation is one of the easiest and cheapest means of food preservation in addition to imparting nutritional and organoleptic benefits to fermented foods. Fermentation is effected by the natural microbiota of raw materials, microorganisms attached to the fermentation equipments or from externally added starter cultures. Yeasts, especially
However, question remains on the toxicity of products of enzymatic degradation and undesired effects of fermentation with non-native microorganisms on the quality of food [21]. In this chapter the biocontrol of aflatoxins, trichothecenes (type A and B), zearalenone, fumonisins, ochratoxins and patulin by bacteria, fungi and yeasts will be discussed more in depth to fill the existing gaps and to develop further proper management practices using biocontrol agents to ensure food safety and to protect consumer’s health.
2. Possible approaches of microorganisms and enzymes to biodegradation of mycotoxins
One of the most frequently used strategies for biodegradation of mycotoxins includes isolation of microorganisms able to degrade the given mycotoxin and treatment of food or feed in an appropriate fermentation process. From a food safety point-of-view, fermentation with microorganisms commonly used in food production (fermentation with lactic acid bacteria, alcoholic fermentation, traditional fermentation of vegetable protein used in South Asia, etc.) should be preferred.
Knowledge of enzymes that take part in degradation of mycotoxins opens some new approaches:
the production of genetically modified species of microorganisms commonly used in food production and their use for production of enzymes mentioned above; or
the transfer of genes coding for these enzymes to transgenic plants and use the plants for production of mycotoxin degrading enzymes.
In staple food such as bread and bakery products in the flour sector, yeast and lactobacilli now play an important role. It thus stands to reason that the same microbes and enzymes are the first to have been considered for use as detoxifying or decontaminating agents. This type of biodegradation could therefore prove a useful strategy for partially overcoming the problem of some mycotoxins. Indeed, this already takes place in bread and in sourdough processes [24]; and OTA in food can also undergo biodegradation [25] and certain antagonistic yeast strains can substantially degrade OTA. This might offer new possibilities for reducing this mycotoxin in bread and bakery products and their raw materials [15]. The use of enzymes or engineered micro-organisms (provided that these are allowed by legislation) as processing aids in the bread and bakery sector would also prove beneficial. Genetic engineering technologies will improve the efficiency with which enzymes can be produced from these organisms, and will allow the production of engineered organisms which have the target genes. They will additionally increase the availability and bioavailability, and will improve the quality of the end product.
2.1. Inhibition of mycotoxins biosynthesis by lactic acid bacteria
Several papers dealing with the inhibition of mycotoxin biosynthesis by LAB have focused on aflatoxins [26]. During cell lysis, it is possible that LAB releases molecules that potentially inhibit mould growth and therefore lead to a lower accumulation of their mycotoxins [27]. These “anti-mycotoxinogenic” metabolites could also be produced during LAB growth. Gourama [28], using a dialysis assay, demonstrated the occurrence of a metabolite that inhibits aflatoxin accumulation in
2.2. Decontamination of mycotoxins using microorganisms by binding or degradation
Biological detoxification of mycotoxins works mainly
the entire organism can be used as a starter culture, as in the fermentation of beer, wine and cider, or in lactic acid fermentation of vegetables, milk and meat;
the purified enzyme can be used in soluble or immobilized (biofilter) forms;
the gene encoding the enzymatic activity can be transferred and overexpressed in a heterologous system; interesting candidates for this application include yeasts, probiotics and plants.
2.2.1. Binding by yeast and LAB
Live microorganisms can absorb either by attaching the mycotoxin to their cell wall components or by active internalization and accumulation. Dead microorganisms too can absorb mycotoxins, and this phenomenon can be exploited in the creation of biofilters for fluid decontamination or probiotics (which have proven binding capacity) to bind and remove the mycotoxin from the intestine.
Yeast and LAB cells are known to bind different molecules such as killer toxins and metal ions on complex binding structures on the cell wall surface [34-36]. Yeast cell wall is known to bind sterols from the medium and the binding molecule was identified as the cell wall mannan [37]. It is confirmed that removal of mycotoxins is by adhesion to cell wall components rather than by covalent binding or by metabolism, as the dead cells do not lose their binding ability [38-41]. Reported literature indicates that mannan components of the cell wall play a major role in aflatoxin binding by
Differences between strains of LAB with respect to aflatoxin binding indicates that binding ability is highly strain specific [48]. In some of the earlier studies, LAB are considered to be inefficient binders of aflatoxin B1 [26, 30]. This may be due to the strains used in those studies were binding low amounts of aflatoxins occurs. Binding of aflatoxin B1 by viable or heat and acid treated bacteria depend on the initial concentration of the toxin [49]. Haskard
2.2.2. Degradation or biotransformation
Another approach to the biological decontamination of mycotoxins involves their degradation or conversion into less toxic molecules by enzymes and selected microorganisms. Initial research in the field of mycotoxin biotransformation started 40 years ago. It has been demonstrated that some microorganisms produce enzymes that could alter the structure of mycotoxins and/or proteins that can conjugate these compounds, making them less active as pathogenic agents [53]. However, only few microorganisms have shown the capacity of degrading mycotoxins.
Karlovsky [20] has shown that the 12,13-epoxide ring of trichothecenes is responsible for their toxicity and that a reductive de-epoxidation caused by specific enzymes (deepoxidases) entails a significant loss of toxicity. For the elimination of the toxic effects of trichothecenes (deoxynivalenol or DON and T-2 toxin are the most well known members)
Garvey
Very few scattered reports are available on the use of yeast and fungal strains for degradation zearalenone.
In the case of ochratoxin A (OTA), two pathways may be are involved in OTA microbiological degradation [25]. First, OTA can be biodegraded through the hydrolysis of the amide bond that links the L-
As a conclusion, mycotoxin risk management strategies must comprise several components. The elimination of adsorbable mycotoxins is possible to be done through adsorption; however, for the elimination of the toxicity of non-adsorbable mycotoxins, such as zearalenone, ochratoxins and trichothecenes biotransformation is crucial. Biotransformation, which is enabled by enzyme-producing microorganisms, allows the conversion of the toxic structure of mycotoxins into non-toxic, harmless metabolites.
3. Possible approaches of microorganisms and enzymes for biodegradation of mycotoxins in food
Mycotoxins frequently contaminate the food raw materials such as cereals, fruits, nuts, spices, milk and meat at various levels. Hence, for the food industry, it has always been an uphill task to keep the mycotoxin levels under check in the products, because mixing high contaminated commodities with low contaminated commodities to reach a level below the regulatory maximum limit is standard not allowed in the EU. Normally, low mycotoxin levels in the food are ensured by using mycotoxin-free, or raw materials with low levels of mycotoxins. In spite of these efforts, sporadically mycotoxin contamination is reported in the food products such as wine, beer, milk and milk products [63-65]. Strains of
3.1. Aflatoxins (AF)
As the first mycotoxins being discovered were the aflatoxins (AF), also the first being targeted to be screened for microbial degradation were the aflatoxins. Several examples of the detoxification of the most common and important mycotoxins are reviewed. Almost 40 years ago, several species of microorganisms – including yeasts, moulds, bacteria, actinomycetes and algae – were screened for detoxification activity; based on this studies only one isolate was found,
Later AF decontamination during fermentation was reported in several cases. About 50% reduction in aflatoxins B1 and G1 (AFB1 and AFG1) has been reported during an early stage of miso fermentation. It was attributed to the degradation of the toxin by microorganisms. Significant losses of AFB1 and OTA were observed during beer brewing [66]. Detoxification of AFB1 occurred during the fermentation of milk by LAB and in dough fermentation during breadmaking. Govaris
Digestive tract microorganisms are able to reduce mycotoxin levels not only by binding and removal but also by detoxification. Most data dealing with the effects of LAB on the accumulation of mycotoxins are related to aflatoxin-producing moulds. Wiseman and Marth [68] revealed the existence of an amenable relationship between
Several studies have suggested that the antimutagenic and anti-carcinogenic properties of probiotic bacteria can be attributed to their ability to non-covalently bind hazardous chemical compounds such as AF in the colon [70, 76]. Both viable and non viable forms of the probiotic bacterium
3.2. Ochratoxin A (OTA)
The major OTA producers in food and feed products are considered to be
Several reports of OTA biodegradation by
Reports about the capacity of some filamentous fungi to biodegrade OTA can also be found. Some strains of
Several enzymes may be involved in the microbiological degradation of OTA. However, little information is available and very few have been purified and characterized. The first reported protease able to hydrolyze OTA was carboxypeptidase A (CPA) from bovine pancreas [107]. Subsequently, a screening study which included several commercial hydrolases, verified that a crude lipase product from
3.3. Patulin (PAT)
PAT contamination of apple and other fruit-based foods and beverages is an important food safety issue due to the high consumption of these commodities. PAT contamination is considered of greatest concern in apples and apple products; however, this mycotoxin has also been found in other fruits, such as pears, peaches, strawberries, blueberries, cherries, apricots and grapes as well as in cheese [8]. A number of studies have shown that PAT is generally unstable during fermentation so that products such as cider are usually free of PAT. It is likely that when PAT is reported in cider this is the result of the addition of apple juice to produce ‘sweet cider’.
The initial studies concerning degradation of PAT by actively fermenting yeasts were reported by Stinson and co-authors [111]. However, authors were not able to chemically characterize the products of degradation. More recently, Moss and Long [112] reported that under fermentative conditions, the commercial yeast
3.4. Trichothecenes (type A and B) – Fusarium toxins such as DON and T-2/HT-2
Several microorganisms have been found that can degrade deoxynivalenol (DON) and T-2 toxin. On the basis of morphological and phylogenetic studies, the degrader strain was classified as a bacterium belonging to the
Studies on the effect of detoxification procedures for
Considerable amounts of other
3.5. Fumonisins
Concerning the mechanisms of action involved in the removal of fumonisins by LAB, Niderkorn [126] suggested that peptidoglycans were the most plausible fumonisin binding sites. The quenching ability of LAB was increased when bacteria were killed using different physical and chemical treatments, while lysozyme and mutanolysin enzymes that target peptidoglycans partially inhibited it. It was also reported that tricarballylic acid chains found in fumonisin molecules played an important role in the binding process since hydrolysed fumonisin had less affinity for LAB, and free amine group inactivation had no effect on the binding process. The same article attempted to explain the low affinity of FB1 using a molecular modelling approach. In fact, an additional hydroxyl group in FB1 could form a hydrogen bond with one of the tricarballylic acid chains, resulting in a spatial configuration where the tricarballylic acid chain is less available to interact with bacterial peptodoglycans. Removal of fumonisins by LAB was ascribed to adhesion to cell wall components rather than covalent binding or metabolism, since the dead cells fully retained their binding ability. Peptidoglycans probably play a key rule in this binding process. Therefore, elucidating the differences between bacterial cell wall components of LAB strains might make it possible to select LAB species with the potential to act as biopreservative agents capable of reducing exposure from fumonisins that occur in foods.
4. Detoxification of mycotoxins in animal feed
Different mycotoxins are more commonly found in or associated with certain feedstuffs. Some develop in the growing crop due to its being susceptible to certain toxigenic fungi, while infection and toxin production by others is facilitated by the preservation and storage system used if insufficient care is taken to prevent this.
Most feeds are produced from crops at the farm and consumed by the animals some time later. However, some straight feeds and particularly mixed feeds are also produced and sold by feed mills. Feed raw materials are often divided into (1) cereals and by-products; (2) oilseed by-products; (3) leguminous seeds; (4) roots and tubers; (5) animal by-products; (6) green crops/pasture; (7) silages; (8) hays; (9) straws. They can be used straight, single or in combination in the feeding regime. Component types 1–5 are often combined and used as mixed feed and concentrates. The other raw material groups (6–9) are combined as roughage and mainly used for ruminants and horses.
4.1. Ensiling
Ensiling of mycotoxin-contaminated crops for detoxification has been proposed as an interesting and possible method for elimination or reduction of mycotoxins. Normal ensiling has, however, only rarely been studied for its mycotoxin degrading potential. A study by Rotter
4.2. Yeasts as feed additives
Yeasts have been fed to animals for more than a century and commercial yeast products are being specifically produced in commercial scale for animal feeding [39]. Hence, yeasts have immense potential as tools in tackling the problem of mycotoxins in animal feed.
In the poultry industry,
In a recent study, seven different trichothecene 3-
4.3. Impact of enzymes on alcohol fermentation of mycotoxin contaminated grains and safety of distiller’s dried grains with solubles (DDGS)
A valuable co-product of fuel ethanol production, known as distillers dried grains with solubles (DDGS), is increasingly being used as a feed source for domestic animals. DDGS contains high levels of protein, fiber, minerals and vitamins [135, 136]. An increase in the supply and demand for DDGS [137] is expected to coincide with the increased production of fuel ethanol in commercial plants [138], which rely on the sale of DDGS to turn a profit [139]. One of the challenges facing the fuel ethanol industry is the management of mycotoxins such as DON in DDGS.
The degradation of mycotoxins during alcohol fermentation for the production of ethanol has been investigated only in a few studies, but many papers have appeared on the fate of mycotoxins during the production of beer and wine. Bennett
Mycotoxin-contaminated cereals may in the future be used more often in industrial ethanol production. Enhanced degradation of mycotoxins by eventual addition of microorganisms with mycotoxin-degradation ability is needed if the DDGS are to be utilized for animal feed.
The impact of
The complex of amylolytic enzymes with xylanase from
The results indicated that DON concentrations in the DDGS were significantly higher than in the starting material (
Sample | Moisture content (g kg-1) | Dry weight (kg) | DON concentration, dry matter | DON recovery (%) | |
Absolute (mg) | mg kg-1 | ||||
Input wheat | 118 ± 2 | 0.882 ± 0.002 | 3.48 ± 0.01 | 3.95 | |
DDGS, without xylanase | 68 ± 5 | 0.266 ± 0.005 | 2.57 ± 0.01 | 9.66 | 74 |
DDGS, 2000 XU kg-1 | 82 ± 9 | 0.253 ± 0.003 | 2.41 ± 0.01 | 9.53 | 69 |
DDGS, 3000 XU kg-1 | 79 ± 8 | 0.246 ± 0.006 | 2.34 ± 0.01 | 9.51 | 67 |
DDGS, 4000 XU kg-1 | 74 ± 7 | 0.245 ± 0.003 | 2.05 ± 0.01 | 8.37 | 59 |
DDGS, 5000 XU kg-1 | 80 ± 9 | 0.245 ± 0.005 | 2.10 ± 0.01 | 8.57 | 60 |
The decrease in DON levels may have occurred due to absorbtion by yeast cells or extracellular metabolism resulting in protection from mycotoxin-induced toxicities [124]. According to Yiannikouris and Jouany [119], glucomannans from the external part of the cell wall of S.
Another approach to reduce DON in DDGS might be to add an exogenous trichothecene 3-
5. Conclusion and future concerns
Prevention of mycotoxin formation is the best defence for protecting the consumer’s health. However, prevention is not always possible, especially for those mycotoxins formed under field conditions. Introduction of further legislation for a wider range of mycotoxins in more food commodities means that there is a much greater need to determine how mycotoxins survive processing so that this can be taken into account when setting statutory or guideline limits. It is thus expected that there will be a trend towards further study of the fate of those mycotoxins that pose the greatest potential risk for humans. In some instances it may then be possible to introduce modifications to commercial processes that result in a significant reduction of mycotoxin content in the retail product.
Contaminated crops condemned as food can otherwise be diverted for use as animal feed. Therefore, prevention and reduction of mycotoxin contamination during feed production will become more important. Mycotoxin-contaminated crops must be used in more cases for purposes other than direct food and feed and their utilization will be further investigated. Decontamination procedures will be further studied. Physical methods will be studied, but biological methods probably more so. Mycotoxin-contaminated cereals may in the future be used more often in industrial ethanol production. An enhanced degradation of mycotoxins by eventual addition of microorganisms or enzymes with mycotoxin-degradation ability is needed if the fermentation remains are to be utilized for animal feed.
In this chapter, we have tried to provide information on decontamination of various mycotoxins during fermentation procceses using bacteria, yeasts, fungi and enzymes. Based on the available reports, we can conclude that microorganisms are the main living organisms applicable for mycotoxin decontamination in foods. Results of various researchers showed that yeasts and bacterial strains had differences in decontamination of mycotoxins. For example,
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