Figure 1.
Macroscopic appearance of kidneys with mycotoxic porcine nephropathy (MPN). Different degree of enlargement and mottled or enlarged and pale appearance of kidneys in pigs of 6–8 months of age taken at slaughter time. (Stoev et al, 1998).
Figure 2.
Carcinoma in the region of ureters (yellow arrows) of male chick exposed to 5 ppm OTA via the feed, which died at the end of the 20th month of the experiment. Large grey-white neoplastic foci are seen along the ureters and protruded significantly above its surface (Stoev, 2010a).
Figure 3.
Malformations in newborn mice whose mothers were exposed to 20 ppm OTA and 6 ppm OTB in the feed given from day 7 up to day 12 of the pregnancy – astomia and anophthalmia (the both fetuses on left), 2 normal fetuses in the centre and spina bifida, e.g. facial cleft and maxillary hypoplasia (the fetus on right) (Stoev, 2022b).
Figure 4.
Small grey-white foci on kidney surface in pig fed on diet containing 180 ppb OTA and 1000–3000 ppb ppb penicillic acid (PA) at the end of the 3rd month. Below – normal appearance of kidney from control pig at the same age (Stoev et al, 2001).
Table 1.
Target toxicity and susceptibility to major mycotoxins based on animal species, age and sex
| Mycotoxins | Organs damaged | Target toxicity | Order of species sensitivity | Age and sex sensitivity |
|---|---|---|---|---|
| AFB1 | Liver, kidneys | Hepatotoxic, nephrotoxic, carcinogenic, teratogenic, immunotoxic | Poultry > rabbits > pigs > ruminants | Young and female animals with increased sensitivity |
| OTA | Kidneys, liver | Nephrotoxic, hepatotoxic, carcinogenic, teratogenic, immunotoxic | Pigs > poultry > rabbits > ruminants | Male animals with increased sensitivity |
| DON | Liver, kidney, lymphocytes | Gastrointestinal toxicity, immunotoxic | Pigs > poultry > ruminants | Male and older animals with increased sensitivity |
| ZEA | Reproductive system (ovaries, testicles, uterus, vulva, vagina, mammary gland), liver, kidneys | Estrogenic | Pigs > dairy cattle > poultry > ruminants | Young prepubertal females with increased sensitivity |
| FB1 + FB2 | Brain, liver, kidneys, small intestine | Neurotoxic, hepatotoxic, nephrotoxic, carcinogenic, teratogenic, | Horses > pigs > poultry > ruminants > fish | Females with increased sensitivity |
| T-2+ HT-2 | Liver, kidneys, lymphocytes | Hepatotoxic, gastrointestinal toxicity, teratogenic, immunotoxic | Poultry > pigs > ruminants | Young animals with increased sensitivity |
Figure 5.
A strong synergistic effect between OTA and PA in pigs and chicks (Stoev et al, 2000, 2001, 2004)
Figure 6.
A more than additive effect between OTA and FB1 in pigs (Stoev et al, 2012)
Table 2.
Impact of combined mycotoxins exposure on body weight gain, productivity, organs damages and immune system of different livestock species
| Mycotoxin combination | Type of interaction | Livestock species | Effect on health/productivity | Reference |
|---|---|---|---|---|
| AFB1+DON | synergistic | pigs | immunosuppression | Chaytor et al, 2011 |
| AFB1+DON | synergistic | pigs | weight loss | Harvey et al, 1989 |
| AFB1+DON | synergistic | dairy cattle | milk yeld reduction | Kiyothong et al, 2012 |
| AFB1+DON+ZEA | synergistic | dairy cattle | milk yeld reduction | Kiyothong et al, 2012 |
| AFB1+DON+ZEA | synergistic | dairy cows | milk yeld reduction | Wu et al, 2022 |
| AFB1+DON+ZEA | additive | dairy cows | immunosuppression | Jovaisiene et al, 2016 |
| DON+ZEA | additive | dairy cows | immunosuppression | Danicke et al, 2017 |
| AFB1+OTA+ZEA | synergistic | dairy cows | milk yeld reduction | Wu et al, 2022 |
| AFB1+OTA+ZEA | synergistic | dairy goats | milk yeld reduction | Huang et al, 2017 |
| AFB1+DON | additive | poultry | weight loss/rejection of feed | Huff et al, 1986 |
| AFB1+T-2 | synergistic | poultry | weight loss | Huff et al, 1988 |
| AFB1+OTA | synergistic | sheep | fertility rate, litter number | Mohamed et al, 2019 |
| AFs+OTA | additive | poultry | egg production, weight loss | Verma et al, 2003 |
| AFB1+OTA | synergistic | broilers | liver/kidney damages | Qing et al, 2022 |
| AFB1+OTA | synergistic | rabbits | weight loss/increased mortality | Prabu et al, 2013 |
| AFB1+FB1 | synergistic/additive | broilers | immunosuppression/liver damage | Tessari et al, 2006 |
| AFs+FB1 | additive | poultry | weight loss | Kubena et al, 1995 |
| AFs+DAS | synergistic | poultry | weight loss | Kubena et al, 1993 |
| AFB1+DAS | synergistic | pigs | weight loss | Harvey et al, 1991 |
| OTA+PA | synergistic | pigs | kidney damage | Stoev et al, 2001 |
| OTA+PA | synergistic | poultry | weight loss/organs damage | Stoev et al, 2004 |
| OTA+T-2 | synergistic | broilers | weight loss/organs damage | Kubena et al, 1989a |
| OTA+T-2 | synergistic | pigs | weight loss/organs damage | Harvey et al, 1994 |
| OTA+DAS | additive | chicks | weight loss/organs damage | Kubena et al, 1994 |
| DON+ZEA | synergistic | pigs | weight loss/feed intake reduction | Jia et al, 2020 |
| DON+ZEA | synergistic | pigs | ovarian/embryo damage | Malekinejad et al, 2007 |
| DON+ZEA | synergistic | sows | damage of reproductive system | Doll et al, 2003 |
| DON+ZEA | synergistic | hens | decrease in egg production | Gimeno et al, 2011 |
| DON+T-2 | synergistic | chickens | weight loss/oral lesions | Kubena et al, 1989b |
| FB1+DAS | additive | turkeys | weight loss | Kubena et al, 1997a |
| FB1+OTA | additive | turkeys | weight loss | Kubena et al, 1997a |
| FB1+OTA | additive | pigs | kidney/lung/brain damages | Stoev et al, 2012 |
| FB1+T-2 | additive | chickens | weight loss, mortality | Kubena et al, 1997b |
| FB1+DON | less than additive | chickens | weight loss | Kubena et al, 1997b |
Table 3.
Maximum permitted content of some target mycotoxins in various feeds designed for animals according to EU legislation and regulation (EC Directive 2002/32/EC, EC Directive 2003/100/EC, EC Recommendations 2013/165/EU and 2006/576/EC)
| Mycotoxins | Cereals or Cereal Products | Maximum permitted levels µg/kg (ppb) |
|---|---|---|
| AFB1 | -Complete feedstuffs for pigs and poultry (except young animals) | 20 |
| -Complete feedstuffs for cattle, sheep and goats with exception of: | 20 | |
| ✓ Complete feedstuffs for dairy animals | 5 | |
| ✓ Complete feedstuffs for calves and lambs | 10 | |
| -Complimentary feedstuffs for cattle, sheep and goats (except dairy animals, calves and lambs) | 20 | |
| OTA | -Cereals and cereal products | 250 |
| -Complimentary and complete feedstuffs with exception of: | 5000 | |
| -Complimentary and complete feedstuffs for pigs | 50 | |
| -Complimentary and complete feedstuffs for poultry | 100 | |
| DON | -Cereals and cereal products without maize by-products | 8000 |
| -Maize by-products | 12000 | |
| -Complimentary and complete feedstuffs with exception of: | 5000 | |
| ✓ Complimentary and complete feedstuffs for pigs | 900 | |
| ✓ Complimentary and complete feedstuffs for calves, lambs and kids | 2000 | |
| ZEA | -Cereals and cereal products without maize by-products | 2000 |
| -Maize by-products | 3000 | |
| -Complimentary and complete feedstuffs for dairy cattle, calves, goats (e.g. kids) and sheep (e.g. lambs) | 500 | |
| -Complimentary and complete feedstuffs for piglets, gilts (young sows) | 100 | |
| -Complete and complimentary feedstuffs for fattening pigs and sows | 250 | |
| Fumonisins FB1 + FB2 | Maize and maize by-products | 60000 |
| -Complimentary and complete feedstuffs for pigs, horses, rabbits, pets | 5000 | |
| -Complimentary and complete feedstuffs for poultry, calves, lambs, kids | 20000 | |
| -Complimentary and complete feedstuffs for adult ruminants and mink | 50000 | |
| -Complimentary and complete feedstuffs for fish | 10000 | |
| T-2 + HT-2 | -Unprocessed barley (e.g. malting barley) and maize | 200 |
| -Unprocessed rye, wheat and other cereals | 100 | |
| -Unprocessed oats (with husk) | 1000 | |
| -Oat milling products (husks) for feed and compound feed | 2000 | |
| -Other cereal products for feed and compound feed | 500 | |
| -Compound feed, escluding the feed for cats | 250 | |
| Rye ergot | -All feedingstuffs containing unground cereals | 1000000 |
Table 4.
Maximum permitted content of some target mycotoxins in various food products intended for human food according to EU legislation and regulation (EC Recommendation 2013/165/EU and EC Regulation 2023/915)
| Mycotoxins | Food Products | Maximum permitted level (EU) µg/kg (ppb) |
|---|---|---|
| AFs sum of B1, B2, G1 and G2 | -All cereals and processed cereal products excluding: | 4 |
| ✓ Maize/rice subjected to physical treatment before placing on the market for the final consumer or being used as a food ingredient, and chillies, chilli powder, cayenne, white or black peppers, paprika, ginger, turmeric and nutmeg | 10 | |
| -Dried fruit subjected to physical treatment, before placing on the market for the final consumer or use as ingredient in foodstuffs | 10 | |
| -Dried fruits used as only ingredient or processed products from dried fruits, placed on the market for the final consumer or use as a food ingredient | 4 | |
| -Groundnuts and oilseeds subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient with exception of that for refined vegetable oil production | 15 | |
| -Groundnuts and oilseeds used as only ingredient or processed products from groundnuts and oilseeds, placed on the market for the final consumer or use as a food ingredient with the exception of: crude vegetable oils and refined vegetable oils | 4 | |
| -Tree nuts to be subjected to physical treatment before placing on the market for the final consumer or use as a food ingredient | 10 | |
| -Tree nuts used as only ingredient or processed products from tree nuts, placed on the market for the final consumer or use as a food ingredient | 4 | |
| -Almonds, pistachios and apricot kernels subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient | 15 | |
| -Almonds, pistachios and apricot kernels, placed on the market for the final consumer or use as a food ingredient | 10 | |
| -Hazelnuts and Brazil nuts subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient | 15 | |
| -Hazelnuts and Brazil nuts, placed on the market for the final consumer or use as a food ingredient | 10 | |
| AFB1 | -Groundnuts and oilseeds subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient with exception of that for refined vegetable oil production | 8 |
| -Groundnuts and oilseeds used as only ingredient or processed products from groundnuts and oilseeds, placed on the market for the final consumer or use as a food ingredient with the exception of: crude vegetable oils and refined vegetable oils | 2 | |
| -Tree nuts to be subjected to physical treatment before placing on the market for the final consumer or use as a food ingredient | 5 | |
| -Tree nuts used as only ingredient or processed products from tree nuts, placed on the market for the final consumer or use as a food ingredient | 2 | |
| -Almonds, pistachios and apricot kernels subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient | 12 | |
| -Almonds, pistachios and apricot kernels, placed on the market for the final consumer or use as a food ingredient | 8 | |
| -Hazelnuts and Brazil nuts subjected to physical treatment, before placing on the market for the final consumer or use as a food ingredient | 8 | |
| -Hazelnuts and Brazil nuts, placed on the market for the final consumer or use as a food ingredient | 5 | |
| -Dried fruit subjected to physical treatment, before placing on the market for the final consumer or use as ingredient in foodstuffs | 5 | |
| -Dried fruits used as only ingredient or processed products from dried fruits, placed on the market for the final consumer or use as a food ingredient | 2 | |
| -All cereals and processed cereal products excluding: | 2 | |
| ✓ Maize/rice subjected to physical treatment before placing on the market for the final consumer or use as a food ingredient, and chillies, chilli powder, cayenne, white or black peppers, paprika, ginger, turmeric and nutmeg | 5 | |
| ✓ Processed cereal-based foods and baby foods for infants or children and food for special medical purposes | 0.1 | |
| AFM1 | -Raw milk, heat-treated milk and milk-based products | 0.05 |
| -Dietary foods for special medical purposes and infant milk | 0.025 | |
| OTA | -Unprocessed cereals | 5 |
| -Processed cereal products and products derived from unprocessed cereals placed on the market for the final consumer | 3 | |
| -Bakery wares, cereal snacks and breakfast cereals not containing oilseeds, nuts or dried fruits | 2 | |
| -Dried vine fruit (currants, raisins and sultanas) and dried figs | 8 | |
| -Other dried fruits | 2 | |
| -Roasted coffee beans, cocoa powder, and ground roasted coffee, excl. soluble instant coffee | 3 | |
| -Soluble coffee (instant coffee) | 5 | |
| -Wine (incl. wine-based drinks,), wine-products or cocktails and grape juice or nectar placed on the market for the final consumer | 2 | |
| -Processed cereal-based foods, baby foods for infants/children and food for special medical purposes intended for infants | 0.5 | |
| -Dried spices and ginger | 15 | |
| -Dried herbs | 10 | |
| -Chillies, chilli powder, cayenne, paprika, | 20 | |
| -Liquorice root, ingredient for herbal infusion | 20 | |
| -Liquorice extract, for use in food in beverages and confectionary | 80 | |
| -Pistachios subjected to physical treatment before placing on the market for final consumer or use as a food ingredient | 10 | |
| -Pistachios placed on the market for final consumer or use as a food ingredient | 5 | |
| -Sunflower seeds, pumpkin seeds, (water) melon seeds, hempseeds, soybeans | 5 | |
| -Non-alcoholic malt beverages | 3 | |
| PAT | -Fruit juices, fruit nectars, spirit drinks, cider and other fermented drinks derived from apples or containing apple juice | 50 |
| -Solid apple products placed on the market for the final consumer, incl. compote or apple puree | 25 | |
| -Baby foods and apple juice or solid apple products for infants and children incl. compote or apple puree | 10 | |
| DON | -Unprocessed cereals other than durum wheat, oats and maize | 1250 |
| -Unprocessed durum wheat, oats and unprocessed maize, with the exception of unprocessed maize intended for wet milling | 1750 | |
| -Cereals placed on the market for the final consumer such as flour, semolina, bran, pasta and germ except rice products | 750 | |
| -Bread and bakery wares, pastries, biscuits, cereal snacks or breakfast | 500 | |
| -Processed cereal-based foods and baby foods for infants and children except rice products | 200 | |
| -Maize flour not placed on the market for the final consumer | 1250 | |
| ZEA | -Unprocessed cereals other than maize | 100 |
| -Unprocessed maize except the maize intended for wet milling | 350 | |
| -Cereals placed on the market for the final consumer such as cereal flour, semolina, bran, germ, except rice and rice products | 75 | |
| -Refined maize oil | 400 | |
| -Bread and bakery wares, pastries, biscuits, cereal snacks or breakfast, excluding maize-snacks and maize-based breakfast cereals except rice and rice products | 50 | |
| -Maize placed on the market for the final consumer such as snacks and breakfast cereals | 100 | |
| -Processed cereal-based foods and baby foods for infants and children | 20 | |
| -Maize flour not placed on the market for the final consumer | 300 | |
| Fumonisins FB1+FB2 | -Unprocessed maize, except the maize intended for wet milling | 4000 |
| -Maize and maize-based food placed on the market for the final consumer, excluding: | 1000 | |
| ✓ Maize-based breakfast cereals and maize-based snacks | 800 | |
| ✓ Processed maize-based foods or baby foods for infants and children | 200 | |
| -Maize flour not placed on the market for the final consumer | 2000 | |
| Ergot sclerotia | -Unprocessed cereal grains except unprocessed rye grains, maize and rice | 200000 |
| -Unprocessed rye grains | 500000 | |
| Ergot alkaloids (sum of ergocornine, ergocristine, ergocryptine, ergometrine, ergosine and ergotamine) | -Milling products of barley, wheat, spelt and oats (with an ash content lower than 900mg/100g dry matter) | 100 |
| -Milling products of barley, wheat, spelt and oats, incl. barley, wheat, spelt and oats grains placed on the market for the final consumer (with an ash content equal or higher than 900mg/100g dry matter) | 150 | |
| -Rye milling products and rye placed on the market for the final consumer | 500 | |
| -Processed cereal-based food for infants and young children | 20 | |
| T-2 + HT-2 | -Cereal grains for direct human consumption: | |
| ✓ Maize | 100 | |
| ✓ Oats | 200 | |
| ✓ Other cereals | 50 | |
| -Cereal products for human consumption: | ||
| ✓ Oat bran and flaked oats | 200 | |
| ✓ Cereal bran except oat bran, oat milling products other than oat bran and flaked oats, and maize milling products | 100 | |
| ✓ Other cereal milling products | 50 | |
| ✓ Bread, bakery wares, pastries, biscuits, cereal snacks, pasta | 25 | |
| ✓ Breakfast cereals including formed cereal flakes | 75 | |
| ✓ Cereal-based foods for infants and young children | 15 | |
| Citrinin (CIT) | -Food supplements based on rice fermented with red yeast Monascus purpureus | 100 |