As is well known, mycotoxin contamination is a global problem that affects various agricultural products. To date, up to 18,000 secondary metabolites from fungi have been detected, but research has been limited to a selected number due to their significant impact on animal and human health. The mycotoxin groups that have received the most attention in research are aflatoxins, trichothecenes, ochratoxins, fumonisins, zearalenone, citrinin, patulin and certain toxins produced by endophytic fungi (such as ergot alkaloids mycotoxins) (Gallo et al., 2015).
The group of diseases developed by mycotoxin exposure is known as mycotoxicosis and these syndromes can result from ingestion, inhalation or direct contact with fungal toxins. In livestock, the development of the disease can be acute, presenting clinical signs or even causing death. However, acute mycotoxicosis on farms is not common. On the other hand, the chronic effect of mycotoxin ingestion is of greater relevance and can lead to the development of hidden disorders that reduce food consumption, productivity and fertility. Additionally, mycotoxins can disrupt the metabolism of nutrients and have a toxic effect on the endocrine and immune systems, ultimately affecting the overall health of the animals and causing substantial economic losses (Gallo et al., 2015).
Mycotoxins in the ruminal environment
The sensitivity of ruminants to mycotoxins is lower than that demonstrated by monogastric animals. The microbiotic and physiological conformation of the rumen compartment effectively degrades, inactivates, and inhibits the binding of these toxic metabolites. However, the issue arises from the fact that the diets of ruminants include starch and protein-rich foods in addition to grazing on forages, silages, grasses, and legumes. Consequently, the consumption of this wide variety of foods increases the risk of exposure to mycotoxins, in contrast to certain monogastric animals (mainly birds and pigs) whose diets consist of a narrower range of food products. Information on mycotoxin contamination in forages is still limited, compared to research carried out on cereals (Gallo et al., 2015).
Mycotoxins contamination in forages
Within forages, several of the filamentous fungi can continue to grow and often establish themselves in hay and silage. Many factors can influence the presence of these fungi in food, among which the different agricultural practices and climatic conditions stand out. In silage, several of these fungi can be eliminated. However, certain fungi can tolerate conditions of low oxygen availability and high concentrations of organic acids. Hence, it is crucial to prevent the introduction of oxygen during the ensiling process or storage to prevent mold growth and the subsequent formation of mycotoxins (Ogunade et al., 2018). The occurrence of mycotoxins and fungi in forages can vary considerably and is determined based on both environmental factors (management and type of forage, meteorology, ensiling process, agricultural practices, among others) and laboratory factors (handling and sampling, sample storage, analysis methods, among others) (Gallo et al., 2015).
Effects of mycotoxins in ruminants
Aflatoxins
The mechanism of action of this group of mycotoxins on the physiological state of ruminants will depend mostly on the type and form of presentation of the toxin when it is ingested. The main aflatoxins studied are B1, B2, G1, G2, M1 and M2; with the first two being of greatest relevance. Aflatoxin B1 and B2 can be hydroxylated and distributed in milk or its derived products. They are even capable of contaminating food inputs such as hay, silage and grains; representing a serious risk for the large number of mammals that supply themselves with these foods (Jiang et al., 2021). The damage caused by aflatoxins can be even more serious when their action is synergistic with that of other metabolites. High concentrations of aflatoxins can be detrimental to the growth, health and production of animals. Furthermore, the immune system can be compromised and several plasma metabolites may be altered in the event of liver dysfunction (Chebutia et al., 2020). In the rumen, the effect of aflatoxins may involve lower microbial activity due to their significant capacity to inhibit the synthesis of DNA and RNA, which decreases the growth and performance of the animals. However, these conditions are only seen in the laboratory. In the natural environment, the rapid degradation and absorption of toxins into the bloodstream mitigate adverse effects at the ruminal level. Therefore, the negative effect of aflatoxins on productive performance is better explained by systemic toxicity, which includes immunosuppression and liver damage, rather than by direct intoxication or injury to the rumen (Jiang et al., 2021).
Trichothecenes
T2 and HT-2: These two toxins develop in warm and humid environments, preferably in cereal grains and less frequently in silage forages. In ruminants, these toxins are extensively detoxified by the rumen flora, although T-2 toxin has commonly been associated with cases of gastroenteritis, intestinal bleeding, immunosuppression and reproductive pathologies in cattle (Ogunade et al., 2018).
Deoxynivalenol (DON): Type B trichothecene produced mainly by species of the genus Fusarium. It has two less toxic forms, which are 3-Ac-DON and 15-Ac-DON, which can occur at the same time as the DON and are typically detected at lower concentrations. In ruminants, DON is absorbed into an approximate rate of 7 to 10%, with the ruminal epithelium acting as a protective barrier against its effects. Furthermore, rumen protozoa and certain bacteria are capable of deacetylating and deepoxidizing ingested DON, thereby neutralizing its harmful effects. In dairy cows, it was found that DON disappears after 24 hours of ingestion, with a serum half-life of 4 hours. The ruminal degradation of DON allows the formation of its derivative, called de-epoxy-DON or DOM-1. DOM-1 represents the majority of DON absorbed by the body, with a value of 81 to 93%. DON and its metabolites are excreted in feces and urine (Gallo et al., 2022). At the cellular level, DON has the ability to inhibit protein and nucleic acid synthesis by interfering with ribosomes and affecting cellular kinases. It also interferes with steroidogenesis. This toxin is commonly called vomitotoxin, and in sensitive animals, acute exposure causes gastrointestinal problems such as melena and diarrhea. In chronic conditions, DON can result in weight reduction, growth retardation and adverse effects on the immune and neurological systems (Ogunade et al., 2018).
Fumonisins
Fumonisins are responsible for a range of conditions in animals, such as pulmonary edema in pigs, leukoencephalomalacia in horses and hepatotoxicity in mice, rats and rabbits. This is because their mechanism of action disrupts the biosynthesis of sphingolipids. In the case of ruminants, sensitivity to fumonisins is much lower than in other species since fewer are absorbed. In newborn calves, it has been observed that exposure to fumonisins can cause liver toxicity on rare occasions, but in most cases, no signs of disease or decreased feed consumption have been seen. The limited pathological findings are attributed to the low bioavailability of the toxin, which is swiftly distributed and excreted by the liver and kidneys (Gallo, 2022).
Zearalenone
Zearalenone is a type of mycotoxin produced by the fungi Fusarium graminearum, F.culmorum, F.roseum and F. crookwellense. It is a lipophilic molecule, with affinity for estrogen receptors, inducing a response similar to estradiol. In terms of reproductive function, its effects can lead to alterations in the estrous cycle, decreased fertility, reproductive tract pathologies in both females and males, reduced neonatal survival, and disturbances in spermatogenesis. There is limited information available on the absorption of zearalenone in ruminants, but the literature suggests that the ruminal microbiota efficiently degrades this mycotoxin into two byproducts such as α-zearalenol (α-ZEL) and β-zearalenol (β-ZEL). Consequently, the distribution of ZEN, along with its metabolites, occurs at low concentrations (Gallo, 2022).
Ochratoxins
Due to the activity of protozoans and the rest of the rumen microbiota, ochratoxin is largely degraded to a less toxic molecule, known as α-ochratoxin. However, a certain amount of ochratoxin escapes ruminal degradation and is subsequently absorbed in the lower digestive tract (Mobashar et al., 2010). Animals in the early stages of poisoning show clear signs of discomfort, such as polyuria and reduced food intake. Studies conducted in cows have shown that exposure to high doses of ochratoxin (13,000 ug/kg body weight) results in symptoms such as lethargy, inappetence, decreased milk production and diarrhea. In sheep exposed to doses of 500 ug/kg, the observed signs included decreased food consumption and polyuria, while, in goats the administration of high doses of ochratoxin resulted in the death of the animal (Mobashar et al., 2010). I
In line with the aforementioned findings, the adverse effects expected by ochratoxins in ruminant animals are observed when the concentration of these toxins at the body level is extremely high. Therefore, the accumulation of ochratoxin represents the most critical point in the health of the ruminant. Since not all the toxin is degraded in the rumen and the ingestion of concentrates can increase its bioavailability (both due to contamination and alteration of ruminal pH), ochratoxin may be absorbed and bind to blood serum proteins. The blood protein-toxin connection differs between species, being 2 to 3 times stronger in cattle, humans and pigs than in sheep. It should be noted that the urinary pH of herbivores facilitates its elimination, unlike what occurs in pigs, humans and rats. Consequently, it is important to emphasize that chronic ingestion of ochratoxin has the potential to develop a cumulative effect in the animals, despite the wide range of factors that protect the physiology of the ruminant against these toxins (Mobashar et al., 2010).
Prevention: The key to mitigate the impact of mycotoxins in ruminants
In conclusion, the anatomical and physiological characteristics of ruminants have enabled them to adapt and, in some cases, protect themselves against different toxic metabolites from fungi. The vast microbiological diversity within the rumen acts as a natural defense mechanism against the harmful effects of mycotoxins. However, this delicate balance can be disrupted by various factors, including nutrition, health, and management practices. Therefore, when it comes to mycotoxin poisoning in ruminants, the critical factor lies in preventing the prolonged ingestion of mycotoxins, which can accumulate in the animal’s body and adversely affect both its health and production capabilities.
