Risk assessment in compromised food safety due to underestimated hazard of masked mycotoxins or joint mycotoxin exposure and a safe approach to increase food security

Stoycho D. Stoev

doi:10.2478/aoas-2025-0127

Figures & Tables

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).

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).

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).

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).

A strong synergistic effect between OTA and PA in pigs and chicks (Stoev et al, 2000, 2001, 2004)

A more than additive effect between OTA and FB1 in pigs (Stoev et al, 2012)

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

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

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

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

Risk assessment in compromised food safety due to underestimated hazard of masked mycotoxins or joint mycotoxin exposure and a safe approach to increase food security

Figures & Tables

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Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

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)

Impact of combined mycotoxins exposure on body weight gain, productivity, organs damages and immune system of different livestock species

Target toxicity and susceptibility to major mycotoxins based on animal species, age and sex

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)

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