Clinical and patho-anatomical effects
of mycotoxins in animals

We explore with R. K. Asrani and Rakesh Kumar from CSK Himachal Pradesh Agricultural University the clinical and anatomopathological manifestations of exposure to the major mycotoxins found contaminating raw materials and feed.

R. K. Asrani y Rakesh Kumar

Department of Veterinary Pathology, Dr G C Negi College of Veterinary and Animal Sciences, CSK Himachal Pradesh Agricultural University, Palampur, Himachal Pradesh, India

Mycotoxins are secondary harmful mold metabolites that produce significant detrimental health effects in human beings and animals1. These are low molecular weight compounds known to be harmful even at low concentrations2.

Approximately 25% of the crops, including cereal grains and nuts, are often presumed to be contaminated with fungus3.

The most frequently encountered harmful mycotoxins in foodstuffs and feed include aflatoxin B1 (AFB1), ochratoxin A (OTA), trichothecenes, HT-2 and T-2 toxins, fumonisin B1 (FB1), citrinin (CTN), zearalenone (ZEN) and ergot alkaloids.

A predominately marked distribution of fumonisins, zearalenone and deoxynivalenol (DON) is documented globally4.

Cereal crops may become contaminated in the field or during harvesting, transport, processing or storage5,6. The rate of contamination of crops with fungus is more frequently triggered by the rainy season7.

Factors facilitating the production of mycotoxins in contaminated products include8:

  • Moisture content (20-25%)
  • Environmental temperature (22-30ºC)
  • Composition of food items
  • Relative air humidity (70-90%)
  • Physical damage to cereals by pests
  • pH
  • Presence of mold spores

Figure 1. Mycotoxins production and their occurrence in the food chain.

Common routes of entry of mycotoxins into the body are:

Direct consumption of contaminated products of plant origin (cereals, nuts, bread etc.) and products obtained from animals (meat and meat products, milk, offal’s, fermented sausages etc.)9,10.

Dermal contact and inhalation are not very common routes but can act as a potential mode of entry into the body11.

Harmful toxic effects of mycotoxins depend on11,12:

  • Type of mycotoxin
  • Dose introduced into the body
  • Duration of exposure to the mycotoxins

Mycotoxins are known to produce several harmful effects in animals and human beings. Classification of these toxins can be made on the basis of toxicity13 and clinical symptoms related to the organs damaged14.

Figure 2. Classification of mycotoxins on the basis of toxicity.

Figure 3. Classification of mycotoxins on the basis of clinical manifestations.

Table 1. Summary of different Mycotoxins with their toxic effects.

Effects of AFLATOXINS exposure

Episodes of aflatoxicosis are associated with the production of aflatoxins by common fungal species such as Aspergillus flavus and A. parasiticus in contaminated food products33.

In 1960, in the UK, the first report of mortality caused by aflatoxins-contaminated groundnut meal in turkeys and poultry was reported34.

The list of aflatoxins produced by several fungal species includes AFB1, AFB2, AFG1, AFG2 and AFM1.

Among all known aflatoxins, AFB1 is the most common and potent35.

Aflatoxins are very stable and are rarely destroyed after processing36. Additionally, residues of aflatoxins are also reported to be excreted in milk, milk products, meat and eggs33.

AFB1 is well recognized for its hepatotoxic, teratogenic, immunotoxic and mutagenic potential and is classified as group 1 carcinogen by International Agency for Cancer Research (IARC)37, as it causes hepatocellular carcinoma in human beings.

The order of severity of the mutagenic, immunosuppressive and carcinogenic effects of aflatoxins is:


AFB1 is predicted to exhibit developmental defects along with immune system dysfynction38.

Figure 4. Harmful effects of AFB1.

Species susceptibility to aflatoxins

All animal species are sensitive to aflatoxicosis, but outbreaks are usually encountered among pigs, cattle and sheep39.

The significant economic losses, including decline in growth rate
and productivity, are usually reported in farm animals depending
on individual susceptibility and the targeted species40, 41, 42.

Chronic exposure to AFB1 in farm animals can lead to various ailments, including liver dysfunction, compromised immune status and susceptibility to several diseases43,44,45,46,47,48.

  • Some of the animal species, such as monkeys, chickens and mice have been found to be resistant to AFB149, whereas cattle, horses and sheep are quite prone to AFB1-induced toxicity.
  • Younger animals have proven to be more susceptible than adult and older animals50.
  • Among aquatic animals, trout have been observed to be the most sensitive to AFB1 toxicity51.
  • Among poultry, the order of sensitivity is: ducks > turkeys> Japanese quail> chickens52.

Figure 5. Flow chart indicating mode of action of aflatoxin B1.


Abdominal pain, vomiting and oedema can be observed in acute stages, whereas development of hepatocellular carcinoma is evident in later stages56.

AFB1 toxicity in ruminants leads to:

  • Decline in ruminal motility
  • Decline in the cellular digestion and fatty acid production
  • Decline in feed efficiency and is secreted in milk as AFM1 after 12 h of consumption

Aflatoxin M1

Aflatoxin M1 (AFM1) is a group 1 carcinogen (IARC) formed through CYP1A2-dependent hydroxylation microbial biotransformation from AFB1. The nuclear adducts are formed and secreted in milk and urine.

The concentration of AFM1 in milk is influenced by several factors, such as duration of lactation and the milk yield of the animal57.

Figure 6. Aflatoxin M1 in the food chain.

Table 2. Permissible limits of aflatoxins consumption58, 59.

Table 3. Clinical and patho-anatomical effects of aflatoxins.

Image 1. Gross pathological alterations associated with AFB1. Liver of a rabbit showing chronic hepatitis along with tumorous growth.

Image 2. Photomicrographs of pathological alterations associated with AFB1 a. Liver showing diffuse hemorrhages along with a necrotic area in the hepatocytes along with hemosiderin deposition (H&E*66). b. Liver showing swollen hepatocytes with hydropic changes (H&E*66). c. Photomicrograph of liver showing portal fibrosis with bile duct hyperplasia (H&E*33). d. Liver showing peripheral shifting of nucleus giving a signet ring appearance indicating fatty changes in hepatocytes (H&E*66).

Effects of OCHRATOXIN A exposure

Aspergillus ochraceus, Auplopus carbonarius and Penicillium verrucosum are the most common fungal species associated with the production of ochratoxins in contaminated grains, raw and cooked food items and beverages (coffee, beans, and wine).

Aspergillus ochraceusand Penicillium verrucosum are the most potent moulds responsible for the production of Ochratoxin A (OTA) in tropical and temperate regions, respectively.

This mycotoxin was first reported in contaminated cornmeal72 and it is considered to be the most common and potent mycotoxin produced by these fungi73.

OTA is readily known for its nephrotoxic, carcinogenic, immunosuppressive, teratogenic and genotoxicity in animals74,75,76. Additionally, it has been found to produce hepatocellular carcinoma as well, apart from the nephrotoxic properties, in a dose dependent manner77.

Pigs and poultry more sensitive to OTA induced toxicity.

Ruminants are usually resistant, as OTA is degraded by ruminal microflora to less toxic metabolites such as OTAα78.

Some researchers have shown the release of OTA in breast milk, which means it can act as a potent threat to the newborns through breastfeeding79.

Figure 7. Flow chart indicating the mechanism of action of OTA in kidney tubular cells80 81 82.

Table 4. Tolerable limits of OTA.

Table 5. Clinical and patho-anatomicaleffects of ochratoxins.

Image 3. Gross pathological alterations associated with OTA. a. Swollen and pale kidneys of Japanese quail (right) after administration of Ochratoxin A in diet in comparison to the kidneys on the left side b. Ruffled appearance of feathers in a Japanese quail after feeding Ochratoxin A.

Image 4. Photomicrograph of pathological alterations associated with OTA. Kidney showing fibrous tissue accumulation in the interstitial tissue causing atrophy of renal tubules in OTA toxicity (H&E*66).

Effects of FUMONISIN exposure

Fumonisins are produced by fungal species such as Fusarium verticillioides and F. proliferatum, and they are frequently spotted on maize giving it a whitish appearance99.

The most common forms of fumonisins include fumonisin A and fumonisin B (B1, B2, B3 and hydrolyzed B1), and among these fumonisin B1 is the most common and potent100.

Toxicity associated to fumonisins was firstly reported in 1980 as a cause of equine encephalomalacia (ELEM) and porcine pulmonary oedema (PPE) in the United States, and esophageal cancer in Africa.

These mycotoxins cause neurotoxicity, hepatotoxicity, embryo toxicity and nephrotoxicity in animals101,102.

Fumonisins are also reported to cause leukoencephlomacia in horses, hepatocellular carcinoma in rats and pulmonary oedema in association with hydrothorax in pigs103, whereas the IARC has also documented the carcinogenic potential of fumonisins in human beings104.

The production of this mycotoxin is promoted when moisture content is < 19%.

As per JECFA, the maximum tolerable limit of FB on the basis of no-observable-effect-level (NOEL) of 0.2 mg/kg bw/day with a safety factor 100 is 2 μg/kg/day105.

Mechanisms of action of Fumonisins102:

  • Competitive inhibition of the ceramide synthase enzyme
  • Oxidative stress and endoplasmic reticulum stress
  • Autophagy modulation
  • Alteration of DNA methylation

Figure 8. Mechanisms of inhibition of sphingolipid metabolism.

Table 6. Clinical and patho-anatomical effects of fumonisins.

Image 5. Gross pathological alterations associated with FB1. a. Enlarged liver of a Japanese quail after feeding Fumonisin (FB1) for 3 weeks at the dose of 300 ppm. b. Enlargement of liver (right side) with Fumonisin (FB1) toxicity in comparison to normal liver on the left side.

Image 6. Photomicrograph of pathological alterations associated with FB1. Liver of a Japanese quail reflecting necrotic changes along with heterophilic infiltration admixed with mononuclear cells after the administration of FB1 (H&E*330).

Effects of TRICHOTHECENES exposure

Trichothecenes are toxic secondary metabolites produced by Fusarium graminearum, Stachybotrys, Fusarium poae, Fusarium langsethiae, etc, often found contaminating wheat, maize, barley and oat kept in damp environmental conditions.

Production of these mycotoxins is often favored by ambient temperature (0-32oC) with humid conditions120, 121.

The main mycotoxins belonging to the trichothecene group include type A (T-2) and type B toxins (DON), and their toxic potential is due to the presence of an epoxide ring122.

These toxic metabolites are quite resistant to processing and are only destroyed at temperatures above 260ºC for more than 30 min.

Harmful effects and tolerable limits of trichothecenes

In pigs, cattle, broilers and rats, trichothecenes damage the liver and stomach123.

Therefore, trichothecenes toxicity in farm animals is often associated to symptoms such as vomiting, diarrhoea, anorexia, weight loss and death124,125. Additionally, the malabsorption induced by trichothecenes in pigs, poultry and rats is often associated with necrosis of intestinal villi126,127.

According to the EU, the maximum limit for the presence of DON in cattle feed is 5 mg/Kg feed, whereas it is around 1 mg/Kg feed for calves.

Figure 9. Clinical and patho-anatomical effects of trichothecenes20, 21, 22, 23.

oIn studies conducted by Ingalls129 and Cote et al.130 no marked variation in the milk production was reported when DON is given at a rate of 14 mg/kg for 3 weeks and 66 mg/kg for 5 days, respectively.

Based on the presence of ester-ether bonds between C-4 and C-15 at C-12 we can divide trichothecenes into 2 types: macrocyclic and non-macrocyclic. The non-macrocyclic trichothecenes are enlisted in Table 7.

Table 7. Classification of trichothecenes.

The maximum tolerable limits of DON in most parts of the world are limited to 0.75 mg/kg in human diets and 1-5 mg/kg in animal rations128.

Table 8. Clinical and patho-anatomical effects of trichothecenes.

Effects of ZEARALENONE exposure

The most common fungal species involved in the production of zearalenone (ZEN) include Fusarium culmorum, F. cerealis and F. graminearum. This mycotoxin is commonly found in cereal grains in temperate regions with warm weather144, 145 and can remain stable at temperatures up to 150˚C146.

The highest production of ZEN is reported at 25˚C with 16% moisture content147,148.

Five major metabolites of ZEN include α-zearalenone (α-ZEN), β-zearalenone (β-ZEN), α-zearalenol (α-ZAL), β-zearalenol (β-ZAL) and zearalenol (ZON), α-ZEN having the highest estrogenic activity149, 150.

Zearalenone is responsible for causing ear rot in maize and head blight in wheat and barley151, with immunotoxic, genotoxic, hepatotoxic and hematotoxic effects in animals, as well as significant nephrotoxic potential with an ability to produce pituitary adenomas152,153,154,155. Additionally, ZEN is linked to reproductive disorders in animals and hyperestrogenic syndrome in human beings156.

Table 9. Tolerable limits of zearalenone (ZEN).

Pigs are speculated to be the most sensitive species for ZEN-induced reproductive disorders as compared to other animals157.

  • About 80-85% of oral dose of ZEN is found to be efficiently absorbed in pigs158.
  • The concentration of ZEN and α-ZEN in follicular fluid of swine is 38.9 and 17.6 pg/ml, respectively159.
  • Very limited data is documented about the folliculogenesis in ovaries of domestic animals160, but ZEN shows affinity towards estrogen receptors in uterus, mammary gland, brain and bones, which reflects its estrogenic potential161.

Figure 10. Mechanism of action of ZEN.

Table 10. Clinical and patho-anatomical effects of Zearalenone.

Effects of MONILFORMIN exposure

Fungal sources involved in the production of monilformin (MON) include Fusarium moniliforme, F proliferatum, F. avenaceum, F. subglutinans, F. tricinctum and Pencillium melanoconidium177, 178, 179, 180.

Contaminated cereal grains and plants used for silage preparation are the major source of production of this mycotoxin.

MON is cardiotoxic and hematotoxic181, with acute toxicity that is comparable to trichothecene toxicity (T2, HT-2)182, 183. Fatal outbreaks of MON are reported in animals, but experimental studies in birds and rats have shown potential pathological effects184,185,186.

Figure 11. Mechanisms of action of MON187, 188.

Clinical and patho-anatomical effects of moniliformin

In birds and laboratory rodents, intestinal hemorrhages are seen in acute cases, whereas cardiac hemorrhages are typical lesions in sub-acute and chronic cases of MON toxicity189.

  • In one of the sub-acute toxicity studies conducted by Jonsson et al.190 reflected intestinal hemorrhages with pulmonary congestion in rats without other specific lesions in other organs.
  • Cardiomyopathy depicted by necrotic and degenerative changes in the heart with hypertrophy of muscle fibers causing cardiac arrest in quail birds fed with MON at the dose of 100 ppm has also been documented in previous studies191.

Image 7. Gross pathological alterations associated with MON. Japanese quail showing rounding and dilation of heart (Right side) after feeding MON at the dose of 110- ppm for 3 weeks; Left side showing normal heart.

Image 8. Photomicrographs of pathological alterations associated MON. a. Heart of a Japanese quail showing hypertrophy of cardiac muscle fibers following MON administration (H& E*132). b. Glomerular tufts occupied by needle shaped uric acid crystals in MON toxicity (H&E*66).


In field conditions, it is most common to find raw materials to be contaminated with one or more mycotoxins, with variations in the symptoms associated with exposure, as the combination of these toxins can involve different types of interactions, such as synergistic, additive or antagonistic effects as shown in Table 11.

Table 11. Combined toxic effects of various mycotoxins.


Mycotoxins are very harmful metabolites known to contaminate food items and are majorly implicated in several clinical and pathological impairments in human beings and animals.

Excessive levels of mycotoxins can cause health hazards to the animals directly and through animal products to human beings.

Although in many of the countries tolerable limits for various mycotoxins are standardized, a wide range of developing regions around the globe still need a thorough establishment of such standards with a strict follow-up to reduce the levels of mycotoxins in the food chain.

It is of utmost concern to prevent fungal contamination of food products by providing high-quality crops or animal products with controlled storage, harvesting and distribution strategies.

Regular monitoring of food items, animal feed etc. by employing proper guidelines and safety standards definitely will help to limit the fungal contamination.

In order to limit the production of mycotoxins, several strategies are proposed and followed time and again by various agencies and regulatory bodies. In the present scenario, to minimize the production of mycotoxins during processing of raw material and final food products for animal or human use the basic principles to be followed include:

  • Good Agricultural Practices (GAP)
  • Good Manufacturing Practices (GMP)
  • Hazard Analysis Critical Control Points System (HACCP)


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