Mycotoxins Associated with Meat and Meat Products Contamination: History
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Food sustainability and safety have been heavily prioritized by consumers, producers, and government entities alike. In this regard, filamentous fungi have always been a health hazard due to their contamination of the food substrate with mycotoxins. Additionally, mycotoxins are proven resilient to technological processing. Mycotoxins are considered an increasing health hazard, causing internal organ disorders, immunosuppression, or even death. Some mycotoxins, such as aflatoxins, ochratoxins, and fumonisins, have additional genotoxic effects and can be associated with certain types of cancer, as recognised by the International Agency for Research on Cancer (IARC).

  • meat
  • meat products
  • essential oils
  • mycotoxins

1. Ochratoxin A

Ochratoxin A (OTA) occurs naturally in food poisonings and is found in a variety of agricultural sectors. It is considered one of the most noxious mycotoxins, along with aflatoxin B1, and is commonly found in meat products [8]. It is produced by several fungi which require varying conditions (temperature and water activity), such as Aspergillus carbonarius, Aspergillus niger, Aspergillus ochraceus, Penicillium verrucosum, and others. In the meat industry, it is most often produced by Aspergillus ochraceus (8–37 °C, aw-0.95–0.99) and P. verrucosum (0–30 °C, aw-0.80) [65,66].
In terms of incidence, the route of meat product contamination is usually related to animal feed, with OTA being identified as residues [67]. This is due to the increased bioavailability and long half-life in certain monogastric animals such as pigs.
Some studies indicate that OTA absorption is predominantly gastrointestinal, with the distribution in the systemic circulation depending on the species: 40% chickens, 66% pigs, and 56% rabbits after oral administration. However, there is a variation in the absorption rate and attainment of maximum serum levels after single oral dosing (0.33 h chickens, 1 h rabbits, 10 h pigs) [68]. Other studies mention that the primary site for absorption is gastric, as the acidic environment enhances this phenomenon. In cattle, transport and accumulation of OTA is considered negligible due to the microbial metabolism in the rumen, but there are some discussions regarding animals with immature digestive systems [8].
Among food-producing animals, pigs seem to have the highest level of OTA, especially in Northern European countries. This is associated with the fat solubility of OTA [68].
In terms of maximum concentrations in specific tissues and organs, the highest were found in the kidney, lung, liver, blood, spleen, heart, and adipose tissue [66].
The analysis of the occurrence probability and risk severity indicates the involvement of OTA in the development of renal cancers in certain animal species, as well as the teratogenic, nephrotoxic, and immunosuppressive effects [65].
In regards to human health, a relatively conclusive association was made with a number of renal pathologies (Balkan Endemic Nephropathy and Chronic Interstitial Nephropathy), with OTA being classified by the IARC as a Group B2 carcinogenic [69]. For Balkan Endemic Nephropathy, the main features are associated with familial involvement, manifestations occurring after 15 years of living in an endemic area, as well as the presence of upper urothelial tract cancer. Chronic Interstitial Nephropathy has an acute or chronic evolution with manifestations occurring within days to months [65,70].
In animals, Perši et al. [71] observed that following an oral dosing of 300 μg/kg/day for 30 days in pigs, OTA accumulated in the kidneys, lungs, and adipose tissue, which resulted in minimal concentrations in final products such as black pudding frankfurters (14.02 μg/kg), liver sausage (13.77 μg/kg), and pâté (9.33 μg/kg).
However, given the increased incidence of OTA in food of animal origin, many countries have set stricter maximum limits and others have developed national guidelines. For example, in Romania, the maximum limit is 5 µg/kg in pig liver, kidney, and meat, while Italy developed national guidelines for achieving a limit of 1 µg/kg in pig meat and meat products [72].
In terms of reducing OTA levels in meat products, there are two general directions: prevention and decontamination. Prevention is achieved by following and implementing a food safety management system, while decontamination is achieved by using various physical and chemical treatments [73]. It is important to note that the use of chemical treatments (preservatives) may affect the sensory qualities of cured meat products and may contravene current consumer demands to purchase products without chemical residues, such as residues of fungicidal chemicals [74].

Applicable EO in Meat Products for the Prevention of OTA Development/Detoxification

As previously mentioned, perhaps the biggest challenge in terms of EO applicability is the changes in the sensory properties of the food products. Thus, in addition to the conventional methods, other practices to reduce the interference between EO and the food substrate have been identified using modern encapsulation technologies (nanoparticles, microencapsulation, active packaging).
Among the most effective EO are wild oregano (carvacrol, thymol), garlic, sage (camphor, borneol, 1,8-cineole), and peppermint (neomenthol, menthol, and menthone) [10].
Furthermore, in a study to demonstrate the efficacy of EO against OTA, Koteswara Rao et al. [75] concluded that neem and eucalyptus might also be efficient.
For cured products, Álvarez et al. [76] conducted a study on the efficacy of rosemary EO and Debaryomyces hansenii on artificially contaminated (Penicillum nordicum) dry-cured fermented sausages, during the ripening period. The application method varied by using rosemary as an ingredient for casings maceration or by the direct application of the EO, but the results were similar-decreased levels of OTA synthesis. Rosemary EO (alone or in combination with D. hansenii) reduced the number of proteins associated with OTA biosynthesis, affected cell wall integrity, and disrupted phenylalanine and ergosterol-associated proteins.
Regarding various food or beverage substrates, a study conducted on cocoa showed that Aframomum danielli EO demonstrated maximum OTA-reducing properties at a concentration of 2000 ppm [77]. Abd-El Fattah et al. [78] observed that using a concentration of 0.05% lemongrass EO in yoghurt resulted in a marked reduction of OTA and aflatoxins. Both EO have the potential to be the subject of further studies in meat products or feed.

2. Aflatoxins

Aflatoxins are specific to hot and humid areas and are produced by species of the genus Aspergillus (A. flavus and A. parasiticus). The most known and commonly found in food is aflatoxin B1, which has the highest carcinogenic and genotoxic potential of this group. Aflatoxin M1 is a metabolite of aflatoxin B1 and is often found in the milk of the animals fed contaminated feed [79].
Aflatoxins are characteristic of certain dried foods, spices, rice, corn, figs, cocoa beans, and others, and can contaminate before or after harvesting. In terms of incidence in meat products, OTA is most often identified, with AFB1 being detected less frequently and in lower concentrations [79]. In contrast, there has been multiple evidence of carry-over in tissues that can be found in the liver, muscle, and adipose tissue [8].
Aflatoxin B1 (AFB1) is classified by the IARC as a Group 1 human carcinogen and is associated with liver cancer [8].
In terms of the aflatoxin incidence in meat products, a study by Elzupir et al. [80] in Riyadh, KSA, showed that processed meat products had high levels of aflatoxins, with 37.5% of samples contaminated and a small percentage exceeding the permitted limits (4%).
Additionally, the cancer risk analysis from eating contaminated food identified a very high exposure limit. The most common types of aflatoxins were AFB1 and AFG1, concluding that this is of real importance for veterinary public health [80].
Furthermore, Shaltout et al. [81] observed from a study of one hundred samples that meatballs (kofta) had the highest level of aflatoxins.
In terms of contamination pathways, a study in Egypt found that the most frequent aflatoxin contamination of meat products was associated with the addition of spices [54].

Applicable EO in Meat Products for the Prevention of Aflatoxin Development/Detoxification

There are few studies on the actual application of EO to meat products, given their lower incidence. However, there are multiple studies on the efficacy of certain EO on the growth of A. flavus and A. parasiticus, some of which also have antiaflatoxigenic properties [82].
For example, a study by Masouri et al. [83] concluded that Mentha piperita EO could be used to suppress the effects of aflatoxins on various tissues. EO obtained from Origanum vulgare and Ageratum conyzoides were effective against aflatoxin B1 production in a study on maize and soybeans [84].
Razzaghi-Abyaneh et al. [85] reported a reduction of aflatoxin B1 up to 89.6% and up to 89.2% in aflatoxin G1 following the in vitro use of lime EO.
Neem EO caused irreversible inhibition of aflatoxin biosynthesis due to the alteration of the mycelial cell wall, according to a study by Abyaneh et al. [86].
Another EO with high potential for use in the meat processing and meat product industry is onion EO, with aflatoxin production inhibitory properties of 94.9% for A. flavus and 76.2% for A. parasiticus var. globulosus [87].
Other usable EO could be saffron, Zataria multiflora Boiss, Artemisia dracunculus, Callistemon lanceolatus, basil, Nigella sativa, coriander, dill seeds, and Boswellia sacra [88,89,90,91,92,93,94,95,96].

3. Zearalenone

Zearalenone (ZEA) is produced by many Fusarium species and is a nonsteroidal mycotoxin. Of its most known effects, the most important is the oestrogenic one, with synthetic derivatives of the mycotoxin being used in the meat processing industry as a growth promoter for cattle (Zeranol-α-ZAL). However, this practice is not accepted in the European Union. ZEA is also classified as a Group 3 carcinogenic risk by the IARC with the adverse health effects being a consequence of hormonal imbalance (various reproductive system disorders such as cervical, ovarian, and prostate cancer) [97,98].
Regarding the contamination of meat and meat products, Mirocha et al. [99] conducted a study on the distribution and determination of ZEA residues in broilers, concluding that the level of this mycotoxin was minimal under experimental conditions. In contrast, a 2014 study by Iqbal et al. [39] pointed out that 52% of poultry meat samples tested were contaminated with ZEA, with a maximum level of 5.10 µg/kg identified in the liver. Thus, the need for continuous monitoring of these mycotoxins in poultry meat was emphasized.
Another problem related to the meat processing industry and the presence of ZEA is associated with the contamination of beef and sheep meat. Some authors assume that the conversion of ZEA to zeranol takes place in the rumen and is an irreversible reaction. In this regard, numerous metabolic studies have determined increased levels of urinary excreted ZEA from cattle and sheep [100].
On the other hand, the identification of ZEA at the biliary and urinary levels led other authors to conclude that a distinction can be made between the natural presence of ZEA and that which is used to enhance industrial performance. This distinction is facilitated by the fact that α-zearalenol levels are always higher than those of zeranol—a factor of 5:1, making it possible to distinguish between abuse (<5:1) or contamination (>5:1) [100].

Applicable EO in Meat Products for the Prevention of ZEA Development/Detoxification

Parameters such as high humidity and low temperatures are known to promote zearalenone production by Fusarium. In terms of prevention, ZEA is quite stable at standard cooking temperatures, with the exception of high-pressure cooking and alkalinity. Thus, additional measures are needed [97,101].
For the purposes of this research, no studies on the reduction of ZEA levels by the addition of EO to contaminated meat products (decontamination and/or detoxification) were found, but there are numerous in vitro studies on the efficacy of the EO on ZEA production.
An example is the use of lemon, grapefruit, eucalyptus, and palmarosa EO, which have been shown to be effective, and even enhanced under controlled pH and temperature conditions [101]. On the other hand, another study by Velluti et al. [102] on maize, it was concluded that the efficacy of EO (oregano, cinnamon, lemongrass, clove, and palmarosa) is dependent on environmental conditions.

4. Citrinin

Citrinin (CIT-C13H14O5) is a polyketide-derived mycotoxin with hepatic and nephrotoxic effects, produced mainly by Penicillium citrinum, but also by other species of the genera Penicillium, Aspergillus, and Monascus. This mycotoxin was originally named monascidin A due to its identification in Monascus fermented products [19,22]. It is also noteworthy that it may be one of the most common contaminants globally, being produced mainly by the same fungi that produce OTA [23]. In this regard, the pathological health effects may even be additive, synergistic, or antagonistic to those produced by OTA.
The main organ of choice for CIT is the kidney, causing renal degeneration associated with weight loss, and is a possible causal agent of porcine nephropathy [19]. Although the main organ is the kidney, there are studies in which CIT has also been identified in the bone marrow. CIT is not classified as carcinogenic in humans and is classified as pertaining to Group 3 by the IARC [103].
In terms of the carry-over phenomenon, a study by Meerpoel et al. [104] on the effects of chronic citrinin consumption in pigs, broilers, and laying hens pointed out that there is a minimal contribution to increased CIT intake in humans, given the low rate of CIT transfer from feed to tissue for consumption.
An important problem is that of cured meat products. The surface of these traditionally obtained products is covered with species of the Penicillium, Aspergillus, and Eurotium genera. Studies have been conducted in which Penicillium expansum has been isolated from meat, producing CIT [23,105].
In another study conducted in Turkey by Sari et al. [106], it was observed that CIT was detectable at various concentrations (0.28–1.79 ng/g) in 36.84% of meat products samples and in one sausage sample (beef, lamb, and turkey). It was not detected in minced meat or salami samples.
Additionally, in another study certain fermented meat products were identified as co-contaminated with AFB1, OTA, and CIT [53].
In view of climate change, CIT levels have varied over the years. In this respect, it is important to consider the effect on the carry-over phenomenon. Meanwhile, the artisan-type meat products, obtained under uncontrolled conditions, might also be affected. In addition, depending on the integrity of the outer coating of meat products, mycotoxins may enter from the surface, similar to the OTA situation in dry-cured meat products during long-time ripening, and dry-fermented sausages during ripening [23].

Applicable EO in Meat Products for the Prevention of CIT Development/Detoxification

Regarding the applicability of EO for the prevention of CIT production or detoxification in meat products, no specific studies were identified in the literature. On the other hand, there are studies on effective control strategies identification where EO of peppermint and neem leaf extract were mentioned as potential measures to inhibit CIT production. Experiments on in vitro inhibition of P. citrinum in cheese by means of Z. multiflora Boiss EO have also been performed [108].
Moreover, Aruna et al. [109] concluded that neem oil, eucalyptus, and olive EO could be effective in controlling Aspergillus terreus and CIT production.

5. Patulin

Patulin (PAT) is an uncomplex lactone produced by several species of Penicillium (most commonly P. expansum), Aspergillus, and Byssochlamys. This mycotoxin is most often identified in fruits and fruit products [110,111,112].
This mycotoxin is known for its potential toxigenicity to plant and animal tissues through reactions with the terminal sulfhydryl groups of proteins and polypeptides present in food [111].
Among the most known effects of PAT, immunological, gastrointestinal, and neurological effects are mentioned [111]. In studies on PAT toxicity using various experimental models, it was observed that the most common effects were cerebral and pulmonary oedema and haemorrhage, capillary destruction in the liver, and various types of nervous system damage, as well as multiple macrophage function inhibition [113]. PAT may also be of interest to veterinary public health due to its carcinogenic potential, being classified as a Group 3 by the IRAC [114].
In regards to the identification of PAT in meat products, it should be noted that it most often co-exists with other mycotoxins. Its toxicity depends largely on the pH of the food substrate being as acidic as possible, so PAT is quite stable [115]. In a study conducted by Bailly et al. [116], it was observed that PAT and OTA were not produced by toxigenic strains of Penicillium in dry-cured ham compared to CIT and cyclopiazonic acid. At the same time, after direct contamination, the initial PAT level decreased rapidly during the first hours of incubation at 20 °C.
Although limited, there are studies in which PAT has been identified in animal tissues intended for human consumption, an example being the results obtained by Cao et al. [41], where PAT was identified in pig liver.

Applicable EO in Meat Products for the Prevention of PAT Development/Detoxification

No studies were identified concerning the use of EO in food of animal origin for the prevention or detoxification of patulin. This is most likely due to the low incidence of this mycotoxin in animal tissues.
However, a study by Nguefack et al. [117] identified possible natural alternatives against P. expansum growth. In this study, Ocimum gratissimum EO was identified as effective, as well as the combination of Cymbopogon citratus, Ocimum gratissimum, and Thymus vulgaris.
Other effective EO could be tea tree, orange, and lemon [118,119].

6. Sterigmatocystin

Sterigmatocystin (STC) is a precursor of AFB1, with a similar chemical structure, known to have significant carcinogenic effects [29,120]. In this regard, the CONTAM Panel of EFSA (European Food Safety Authority) conducted a comparative study for the carcinogenic potential of the two mycotoxins, concluding that the hazard associated with STC is approximately three orders of magnitude lower than AFB1 [29].
In terms of health effects, STC is classified by IRAC as pertaining to Group 2B [29]. The scientific opinion on the risk of STC to veterinary public health in the EFSA Journal states that although the carcinogenic risk is low, more data on exposure are needed.
Aflatoxins and STC cause similar toxic effects, predominantly affecting the kidneys and liver in acute toxicity cases [29].
Regarding the determination of STC in meat products, a study by Cao et al. [41] identified the presence of this mycotoxin in pork muscle in a concentration ranging from 0.76–1.23 μg/kg. Additionally, El-Kady et al. [121] observed in an experiment related to the mycotoxin production potential of fungi isolated from meat products that STC was produced by E. Chevalieri, E. Chevalieri var. intermedium, E. amstelodami, E. pseudoglaucum, and E. rubrum.

Applicable EO in Meat Products for the Prevention of STC Development/Detoxification

In terms of A. versicolor growth inhibition and STC production, onion (75%) and garlic (25%) EO were shown to have a synergistic effect [122]. Onion EO used individually completely inhibited STC production in A. versicolor at a concentration of 200 ppm [87]. In addition, Kocić-Tanackov et al. [123] demonstrated the efficacy of oregano EO against Aspergillus spp.

7. Fusarenon-X (4-acetylnivalenol)

Trichothecenes (TX) are mainly produced by Fusarium fungi and there are over 180 derivatives, which are divided into four types (A, B, C, and D) according to their functional groups. Fusarenon-X (FX) belongs to the B group of TX and is often associated with the contamination of feed and food for human consumption [5].
In terms of toxicity, it was observed in experimental studies that the maximum concentration of TX was found in the liver and kidney, concluding that these are the primary organs for the conversion of TX to NIV (Nivelanol—a secondary metabolite of TX). TX was also identified in the spleen in a study on piglets, 3 h after oral administration [5].
Organs primarily affected by TX are those with proliferative cells such as the spleen, thymus, testicles, small intestine, and hematopoietic tissues [5].
In terms of health effects, the chronic exposure of mice to TX and NIV most often results in reduced body mass, severe leukopenia, increased relative organ mass, and reduced feed efficiency. In addition, as there are not enough studies regarding carcinogenicity in humans, IARC has classified these toxins as belonging to Group 3. However, there are studies on various experimental models indicating tumour incidence caused by TX [124].
In addition, a study by Bony et al. [125] observed a genotoxic potential of FX and NIV, highlighting the need for more studies in this area.
Most often FX contaminates plant substrates such as wheat, barley, maize, and other cereals. There are also studies on the identification of FX in fish products such as gula substitutes. However, more studies are needed [51].

Applicable EO in Meat Products for the Prevention of FX Development/Detoxification

Trichothecenes, including FX, are found in relatively low concentrations in meat products, most often as a result of carry-over. In this regard, for the prevention of feed contamination, a study by Perczak et al. [126] concluded that Cinnamomum zeylanicum, O. vulgare, Cymbopogon martini, Citrus aurantium dulcis, Thymus hiemalis, Mentha viridis, Foeniculum vulgare dulce, and Aniba rosaeodora EO have a reduction effect on group B TX concentration levels of 94.51–100%.

8. T-2 Toxin

T-2 toxins are among the most relevant toxins in agriculture worldwide and are most often identified in grains. They belong to a family of chemically related toxins called trichothecenes, produced by species of the genera Fusarium, Myrothecium, and Stachybotrys [127].
The incidence of this mycotoxin is associated with developing countries and specific environmental conditions (substrate moisture, relative humidity, temperature, and oxygen availability) [127].
In terms of toxicity, T-2 toxins are some of the most toxic compared to the other members of the family to which it belongs. Poisoning in humans is known as Alimentary Toxic Allukemia (ATA) [127].
TX consumption can induce manifestations such as anorexia, emesis, carcinogenicity, haematotoxicity, neurotoxicity, and immunotoxicity [32]. Increased toxicity to mucous membranes and skin is also documented [128].
In terms of the risk of poisoning in humans, the consumption of contaminated animal products appears to be the primary cause [129].
In a study on carry-over for chickens, the EFSA-recommended limits for chicken feed of 0.25 mg/kg were found to be effective, resulting in minimal risk to human health [130].
Another study identified traces of T-2 toxins in back muscle, pig back fat, and chicken muscle in concentrations less than 0.5 μg/kg [68].

Applicable EO in Meat Products for the Prevention of T-2 Toxin Development/Detoxification

In order to prevent the carry-over effect, a study by Ancsin et al. [131] observed that the addition of garlic EO to broilers’ feed had desirable effects on some redox parameters.

9. Deoxynivelanol

Deoxynivelanol (DON) belongs to group B TX and is produced by Fusarium graminearum and Fusarium culmorum. The effects associated with this mycotoxin consumption include acute manifestations such as emesis, gastroenteritis, diarrhoea, and reduced food consumption with chronic implications [132].
DON exhibits increased thermostability under cooking and baking conditions, which is of interest in the food processing industry. It can also persist in meat after the consumption of contaminated feed or water by animals. According to the studies, this problem is associated with a minor risk, particularly when compared to the direct consumption of cereal products, but should be taken into account nonetheless [132].
Regarding the incidence in meat and meat products, a study by Zou et al. [43] identified DON as a residue in pig back fat samples at concentrations less than 0.5 μg/kg.
Furthermore, in an experimental administration of contaminated feed to pigs, traces of DON were detected in muscle (0.0016 ± 0.0016 mg/kg), liver (0.0057 ± 0.0043 mg/kg), and back fat (0.0002 ± 0.0004 mg/kg), which did not represent a hazard to the consumers [133].

Appliable EO in Meat Products for the Prevention of DON Development/Detoxification

According to a recent study, the effectiveness of lemon balm and palmarosa EO was observed, with better results obtained by controlling temperature and pH (20 °C, pH 3–6) [134].

This entry is adapted from the peer-reviewed paper 10.3390/foods11223666

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