Mycotoxins Affecting Animals, Foods, Humans, and Plants: Types, Occurrence, Toxicities, Action Mechanisms, Prevention, and Detoxification Strategies—A Revisit
Abstract
:1. Introduction
2. Major Groups of Mycotoxins: Occurrence, Production, and Toxicities
2.1. Aflatoxins
2.2. Ochratoxins
2.3. Trichothecenes (Trichothecene Mycotoxins)
2.4. Deoxynivalenol (a Trichothecene)
2.5. Fumonisins
2.6. Emerging Fusarium Mycotoxins (Enniatins, NX-2 Toxin, Beauvericin, Moniliformin, Fusaproliferin)
2.7. Sterigmatocystin
2.8. Ergot Alkaloids
2.9. Zearalenone
2.10. Alternaria Toxins (Altenuene, Tentoxin, Tenuazonic Acid, Altertoxin, Alternariol Methyl Ether, Alternariol)
2.11. Patulin (PAT)
Mycotoxin | Common Fungal Species | Foods Where Commonly Found | Toxicities | Maximum Allowable Limits and Associated Remarks | Reference(s) |
---|---|---|---|---|---|
Aflatoxins (aflatoxins B1, B2, G1, G2, M1, M2) | Aspergillus parasiticus, Aspergillus flavus, Aspergillus bombycis, A. pseudotamarii, A. nomius, etc. | Cereals, legumes, fruits, seeds, vegetables, nuts, etc. | Liver cancer; hepatocellular carcinoma; target DNA; mutagenic and teratogenic effects | The EU set limits of 4 μg/kg and 2 μg/kg for total aflatoxins and AFB1 permitted, respectively, in nuts, dried fruits, and cereals meant for direct consumption by humans. The AFM1 maximum residue level in milk is set by the European Union and the United States at 50 ng/kg and 500 ng/kg of raw milk, respectively. The AFB1 maximum residue level in feeds of lactating cows is set at 5 μg AFB1/kg, 10 μg/kg, and 20 μg/kg of feeds in the EU, in China, and in the US, respectively | [19,26,27,34,176] |
Ochratoxins (ochratoxins A, B, C) | Species of Aspergillus and Penicillium, including Aspergillus ochraceus, Aspergillus niger, Aspergillus carbonarius, Penicillium verrucosum | Cereals, legumes, seeds, fruits, vegetables, nuts, etc. | Immunotoxic, teratogenic, neurotoxic, hepatotoxic, and nephrotoxic activities; nephropathy in pigs; in humans, ochratoxin A was linked to urothelial tumors, chronic interstitial nephropathy, renal failure, and Balkan endemic nephropathy; etc. | In the EU, OTA limits in imported foods are set to a maximum of 10.0 μg/kg for instant coffee, 5 μg/kg for roasted coffee, 2 μg/kg for grape juice, 2 μg/kg for wine, 3 μg/kg for processed cereal food products, and 5 μg/kg for unprocessed cereal grains | [1,81] |
Trichothecenes (trichothecene mycotoxins), examples include deoxynivalenol (vomitoxin), 3- and 15-acetyldeoxynivalenol, nivalenol, anguidine, T-2 toxin, HT-2 toxin, crotocin, diacetoxyscirpenol, macrocyclics, etc. | Species of Fusarium (Fusarium crookwellense, F culmorum, F graminearum, F poae), Myrothecium, Verticimonosporium, Trichothecium, Trichoderma, Cephalosporium, Stachybotrys, and Spicellum | Rice, oats, rye, barley, maize, wheat, vegetables, etc., and animal foods, including eggs, milk, liver, and kidneys | They can diffuse into cells and block translation by interacting with eukaryotic ribosomes; this is their primary action mechanism. Other action mechanisms for toxicity include inhibiting DNA, RNA, and protein synthesis, lipid peroxidation, apoptosis, inhibiting mitochondrial functions, neurotransmitters changes, and cytokine activation. Exposure to trichothecenes affects nearly all key systems in vertebrates … alimentary toxic aleukia (ATA) in humans, etc. | The US FDA has established a level of 1 ppm restriction for deoxynivalenol. The range of TDI of 100 ng/kg bw for the sum of T-2 and HT-2 toxins is used by the EFSA. | [16,96,98] |
Fumonisins (fumonisins B1, B2, B3, etc.) | Fusarium species such as Fusarium verticillioides, Fusarium nyagamai, F. oxysporum, F. globosum, F. fujikuroi, F. proliferatum, Aspergillus awamori, A. niger etc. | Along with corn and corn food products, fumonisins have been reported in asparagus, sorghum, beer, rice, soybeans, beans, etc. | Fumonisins are linked to atherosclerosis in monkeys, esophageal and liver cancer in human, equine leukoencephalomalacia in horses, porcine pulmonary edema and pulmonary artery hypertrophy in swine, and kidney and liver cancer in rodents. Fumonisins inhibit sphingolipids synthesis. | The International Agency for Research on Cancer (IARC) has classified fumonisin B1 as possibly carcinogenic to humans (group 2B). The EU has put the maximum total fumonisin (fumonisins B1 and B2) limit at 1000 μg/kg for maize and maize products meant for direct consumption by humans and at 800 μg/kg for snacks and breakfast cereals produced from maize. The US FDA set a total limit of fumonisins at 2 to 4 mg/kg in corn and corn products intended for human consumption and at 3 mg/kg in corn used for popcorn. The Joint FAO/WHO Expert Committee on Food Additives put the maximum fumonisins tolerable intake per day at 2 μg/kg bw for fumonisins B1, B2, and B3, in combination or alone. | [19,114,116,117] |
Emerging Fusarium mycotoxins (enniatins, NX-2 toxin, beauvericin, moniliformin, fusaproliferin, etc.) | Species of Fusarium, including Fusarium verticillioides, Fusarium subglutinans, Fusarium proliferatum, Fusarium acuminatum, F. avenaceum, F. arthrosporiodes, F. chlamydosporum, F. redolens, F. oxysporum, F. beomiforme, etc.; Beauveria bassiana | Corn, rice, corn products, seeds, nuts, coffee, tree nuts, dried fruits, beans, vegetable oil, etc. | As a result of their high prevalence in foods and feeds and their potential toxicity to humans and animals, the interest in emerging mycotoxins is increasing. Beauvericin has insecticidal, antifungal, and antibacterial properties and can have toxic effects, including apoptosis induction, increased cytoplasmic calcium concentration, and fragmentation of DNA in cell lines of mammals. | Not available | [126,127,133] |
Sterigmatocystin | Aspergillus species, such as A. versicolor (major producer), A. sydowi, A. quadrilineatus, A. aureolatus, A. amstelodami, A. ruber, A. chevalieri, as well as species of Penicillium, Emiricella, Chaetomium, and Bipolaris | Peanuts, corn, barley, rice, wheat, grain products, etc. | Sterigmatocystin has teratogenic, mutagenic, and carcinogenic effects but is less potent than AFB1 and can cause hepatic toxicity in most animals; hepatocellular carcinoma and squamous cell carcinomas in rats; bloody diarrhea and death in cattle; LD50 in mice is 800 mg/kg and above | The IARC placed STC under class 2B carcinogens. The California Department of Health Services used values TD50 from the Cancer Potency Database to produce “no significant risk” intake levels for humans. The resulting level was 8 mcg/kg bw per day for a 70 kg adult. No limit has been made available in many countries | [140,144] |
Ergot alkaloids | Comprised of a complex family of the derivatives of indole produced by the Clavicipitaceae (such as Neotyphodium and Claviceps) and Trichocomaceae (such as Penicillium and Aspergillus) families. Claviceps purpurea is the dominant producer | Rye (most common host), triticale, barley, wheat, oats, etc. | Causes ergotism; ergot alkaloids are both harmful and beneficial to humans; can cause delirious seizures, fits, St. Anthony’s Fire, etc.; can cause gangrenous and convulsive forms of toxicities | Maximum tolerable limits are in the EU commission pipeline while current ergot sclerotia content is set in unprocessed cereals at a maximum of 0.05%. In the US, rye and wheat are considered unsafe for consumption by humans if they contain above 0.3% sclerotia by weight, and barley, triticale, or oats are graded when they contain above 0.1%. The maximum ergot level set by the European Union is 0.05% in common wheat and durum, i.e., 500 mg/kg w/w sclerotia. | [147] |
Zearalenone (formerly referred to as F-2 toxin) | Species of Fusarium, such as Fusarium crookwellense, Fusarium cerealis, Fusarium semitectum, Fusarium equiseti, Fusarium graminearum, Fusarium culmorum, etc. | Maize, soybean, rice, rye, sorghum, oats, barley, wheat, grain products, etc. | Zearalenone or its metabolic compounds are known to bind transcription factors, including pregnane X receptors involved in expressing enzymes in pathways of biosynthesis; zearalenone chronic administration can cause uterine fibroids, pituitary adenomas, hepatocellular carcinoma, and liver damage in mice, and chronic progressive hematotoxicity, testicular atrophy, cataracts, retinopathy, and nephropathy in rats; among other animals, pigs are more prone its toxicities | The tolerable daily intake (TDI) for zearalenone was set by the EFSA at 0.25 μg/kg bw/day, and is also recommended by other international bodies such as the Joint FAO/WHO Expert Committee on Food Additives (JECFA) | [155,156] |
Alternaria toxins (altenuene, tentoxin, tenuazonic acid, altertoxin, alternariol methyl ether, alternariol) | Alternaria species such as Alternaria triticina, Alternaria tenuissima, Alternaria solani, Alternaria japonica, Alternaria dauci, Alternaria brassicae, Alternaria alternata | Fruits and vegetables, seeds, grains, plants, beer, fruit juices, vegetable juices, wine, peppers, fresh and dried tomatoes, flour, bran, wheat, dried fruit, cereal products (e.g., rice and oat flake), sunflower oil, sunflower seeds, etc. | Tenuazonic acid has phytotoxic and antibacterial properties and acute toxicities for dogs, chicken, and mice, in addition to hematological disorders in humans. Although most Alternaria toxins show low acute toxicities, alternariol methyl ether and alternariol are mostly toxic because of their genotoxic, cytotoxic, carcinogenic, and mutagenic effects, with scientific-based findings from toxicological studies in vitro involving mammalian and bacterial cells. | The toxicological concern threshold (TTC approach) was put into use by the EFSA; for genotoxic Alternaria toxins (AME and AOH), a 2.5 ng/kg body weight per day TTC value was set, while for non-genotoxic Alternaria toxins (TEN and TeA), a 1500 ng/kg body weight per day TTC value was set | [162,164] |
Patulin | Penicillium expansum, A. clavatus, Penicillium patulum (Penicillium griseofulvum and Penicillium urticae), Penicillium crustosum, etc. | Apples, apple products, fruits, vegetables, cereals, legumes, seeds, nuts, etc. | Mutagenicity, teratogenicity, carcinogenesis, immunotoxicity, and neurotoxicity are chronic and acute effects patulin showed on cell cultures. PAT causes neurotoxic and immunotoxic effects in animals, but no reliable evidence has shown its carcinogenicity to humans. However, studies have shown human toxicities, such as hemorrhages, ulcerations, vomiting, and nausea | The US, EU, and Chinese authorities all set 50 μg/L/kg as the patulin upper limit in fruit and apple juices. The EU established a 10 μg/kg to 50 μg/kg limit depending on the type of food | [164,174,175] |
Other common mycotoxins (tremorgenic mycotoxins, fusarins (fusarins A–F), 3-nitropropionic acid, cyclochlorotine, sporidesmin) | Tremorgenic mycotoxins are produced by Aspergillus terreus, species of the Penicillium genus, etc.; Pithomyces chartarum produces sporidesmin; cyclochlorotine is produced by Penicillium islandicum; 3-nitropropionic acid (3-NPA) is produced by the species of Arthrinium; fusarins are produced by the species of Fusarium, such as Fusarium verticillioides (formerly Fusarium moniliforme), Fusarium graminearum (Fusarium venenatum), Fusarium poae, Fusarium sporotrichioides, Fusarium oxysporum | Several foods and feeds | Tremorgenic mycotoxins cause “staggers syndrome” in livestock and are linked to neurological conditions, such as seizures, tremors, mental confusion, and even death in humans. Fusarins are mutagenic; 3-nitropropionic acid interjects mitochondrial electron transport; Cyclochlorotine interrupts myofibrils and is hepatotoxic in animals; due to the hydrophobicity of sporidesmin, it can be integrated easily into the membranes of cells, in which it changes the organization of the bilayer | The EU, the US, the WHO, etc., all have various limits for these mycotoxins | [175,176,177,178] |
2.12. Other Common Mycotoxins
3. Action Mechanisms of Mycotoxins: Key Aspects
- (a)
- Ribosomal binding: Trichothecene toxicities occur due to their capability to bind the eukaryotic ribosomes’ 60S subunit and inhibit the reaction of peptidyl transferase [80]. Ochratoxin A competes with phenylalanine–tRNA ligase and inhibits the synthesis of protein; both aspartame and phenylalanine reduce toxicity of OTA by competing with it [95,97].
- (b)
- Protein interaction: The plasma albumin binds to aflatoxins. After oxidation of AFB1 by cytochrome P450s, two epoxides are formed and they react with the lysine ε-amino group forming AFB1–albumin adducts [15,194,195]. Aflatoxins are immunosuppressive, and in several studies they suppressed immune response mediated by the cell and impaired phagocytosis and chemotaxis. Most immunotoxic properties of fumonisin B1 may be a result of its capability to alter the levels of mRNA and/or expression of IL-1β, IFN-γ, and TNF-α as shown in several scientific experiments [196,197]. Penitrem obstructs uptake of glutamate and GABA (γ-aminobutyric acid) into cerebellar synaptosomes, modulating the function of GABA receptors. One of the ways patulin exerts its toxicities is by causing a dose- and time-dependent phosphorylation increase of c-Jun N-terminal kinase, protein kinases 1 and 2 regulated via extracellular signal, and p38 kinase, contributing to downstream effects, including cell death and DNA damage [197,198]. A mycotoxin known as secalonic acid D, which causes “cleft palate”, phosphorylates the binding protein of the cAMP response element [198,199].
- (c)
- (d)
- Ionophore activity: Beauvericin and enniatins that are produced by species of Fusarium have ionophoric activities specific to potassium and cause an influx of potassium into the matrix of the mitochondria followed by swelling of the mitochondria [201].
- (e)
- Metabolic enzyme inhibition: OTA, citroviridin, and AFB1 affect the metabolism of carbohydrates, while rubratoxin B and trichothecenes interfere with the metabolism of lipids [117,125]. The checmical structure of fumonisins has a high similarity to those of sphinganine and sphingosine, the sphingolipid backbones. Consequently, fumonisins inhibit ceramide synthase competitively. Fumonisin B1 inhibits argininosuccinate synthetase [125].
- (f)
- (g)
- (h)
- (i)
- Necrosis and apoptosis: AFB1 cytotoxic effects in lymphocytes of humans involve necrosis, caspase activation, and apoptosis [206], which lead to programmed cell death and irreversible cell damage. The death of cells induced by necrosis does not follow the signal transduction pathway of apoptosis.
- (j)
- Mitochondrial interactions: Fumonisin B1 was found to obstruct the mitochondrial complex I in human neuroblastoma cells and rat primary astrocytes, resulting in reduced cellular and mitochondrial respiration and an increase in reactive oxygen species (ROS) generation with calcium signaling deregulation [207,208]. By binding covalently to the enzyme active site, 33-NPA permanently deactivates succinate dehydrogenase. Acrebol, from Acremonium exuviarum, inhibits mitochondrial complex III, consequently causing ATP depletion by inhibiting the chain of respiration [207,209].
4. Mycotoxin Prevention Measures, Decontamination, and Detoxification Approaches
4.1. Pre-Harvest Preventive Measures
4.2. Post-Harvest Preventive Measures
4.2.1. Biological Strategies
Fermentation and Dietary Diversification
Fungi
Bacteria
Yeast
4.2.2. Physical Strategies
Storage Conditions
Radiation (Irradiation)
Use of Mycotoxin Binders
Sorting and Cleaning
Cold Plasma
Other Processing Methods (Frying, Baking, Peeling, Drying, etc.)
4.2.3. Detoxification with Enzymes
4.2.4. Chemical Strategies
Chitosan Usage
Ozone (O3)
Bases (Hydrated Oxide, Ammonia)
4.2.5. Other Emerging Strategies
Nanoparticles (NPs)
Extracts from Plants
Other Emerging Green Strategies
5. Conclusions and Future Prospects
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Awuchi, C.G.; Ondari, E.N.; Ogbonna, C.U.; Upadhyay, A.K.; Baran, K.; Okpala, C.O.R.; Korzeniowska, M.; Guiné, R.P.F. Mycotoxins Affecting Animals, Foods, Humans, and Plants: Types, Occurrence, Toxicities, Action Mechanisms, Prevention, and Detoxification Strategies—A Revisit. Foods 2021, 10, 1279. https://doi.org/10.3390/foods10061279
Awuchi CG, Ondari EN, Ogbonna CU, Upadhyay AK, Baran K, Okpala COR, Korzeniowska M, Guiné RPF. Mycotoxins Affecting Animals, Foods, Humans, and Plants: Types, Occurrence, Toxicities, Action Mechanisms, Prevention, and Detoxification Strategies—A Revisit. Foods. 2021; 10(6):1279. https://doi.org/10.3390/foods10061279
Chicago/Turabian StyleAwuchi, Chinaza Godswill, Erick Nyakundi Ondari, Chukwuka U. Ogbonna, Anjani K. Upadhyay, Katarzyna Baran, Charles Odilichukwu R. Okpala, Małgorzata Korzeniowska, and Raquel P. F. Guiné. 2021. "Mycotoxins Affecting Animals, Foods, Humans, and Plants: Types, Occurrence, Toxicities, Action Mechanisms, Prevention, and Detoxification Strategies—A Revisit" Foods 10, no. 6: 1279. https://doi.org/10.3390/foods10061279