Introduction
Mycotoxins are not only highly toxic to animals but also pose a significant risk to human health. This risk is of particular concern for children, pregnant women, and individuals with compromised immune systems, making mycotoxin control a critical component of food safety.
Humans may be exposed to mycotoxins through different pathways. When these toxins are ingested directly via contaminated plant-derived foods, the condition is referred to as primary mycotoxicosis. In other instances, exposure occurs through the consumption of contaminated products of animal origin (e.g., meat, milk or eggs), a condition described as secondary mycotoxicosis (Figure 1).
Figure 1. Differences between primary and secondary mycotoxicosis (adapted from Bhat, 1997; Sanchís et al., 2004).
Once ingested, these mycotoxins undergo toxicokinetic processes, including:
- Absorption
- Distribution
- Biotransformation
- Excretion
The relevance of these processes in animals lies in the potential transfer of mycotoxin metabolites to products of animal origin.
This process, whereby such undesirable compounds reach edible animal tissues or products, is commonly referred to as carry-over (Völkel et al., 2011).
The mycotoxins that have attracted the greatest attention in relation to transfer from feed to products of animal origin include aflatoxins (AFB1 and AFM1), ochratoxin A (OTA), zearalenone (ZEN), fumonisins (FBs), T-2 toxin (T-2), and HT-2 toxin (HT-2) (Table 1; Tolosa et al., 2021).
| Mycotoxins | Matrix | Producing fungi |
|---|---|---|
| AFB1, AFB2, AFG1, AFG2 AFM1 | Maize, peanuts, spices, tree nuts Milk, eggs, cheese | Aspergillus flavus, Aspergillus parasiticus |
| OTA | Wheat, barley, maize, coffee, wine, beer | Aspergillus ochraceus, Aspergillus carbonarius, Aspergillus niger, Penicillium verrucosum |
| DON (deoxynivalenol) | Wheat, maize, barley | Fusarium graminearum, Fusarium culmorum |
| T-2, HT-2 | Wheat, maize, barley, rye | Fusarium sporotrichioides, Fusarium poae |
| ZEN | Wheat, maize | Fusarium graminearum, Fusarium culmorum, Fusarium crookwellense |
| FBs | Wheat | Fusarium moniliforme, Fusarium proliferatum |
Table 1. Principal mycotoxins in food and feed for human and animal consumption and their producing fungi (Tolosa et al., 2021).
Mycotoxins in products of animal origin
The occurrence of mycotoxins in products of animal origin, alongside viral and bacterial agents, represents one of the major challenges to the safety, hygiene, and quality of foods intended for human consumption. The main matrices susceptible to contamination by these compounds are outlined below.
Eggs
The consumption of mycotoxin-contaminated feed by laying hens is associated with a range of adverse health effects, leading to significant economic losses due to reductions in both egg quality and production.
The mycotoxins most frequently reported in eggs include aflatoxins, OTA, ZEN and fumonisins (Greco et al., 2014; Jia et al., 2016). In addition, the presence of enniatin B1 (ENN B1) in eggs has also been documented (Jestoi, 2008).
Meat and meat products
Mycotoxin carry-over may occur in meat and meat products, as also observed in milk. Studies assessing mycotoxin presence in meat matrices indicate that, in fresh meat and edible animal organs, the most prevalent toxins are aflatoxins, OTA, fumonisins and ZEN (Meucci et al., 2019; Hort et al., 2020). In cured and fermented meat products, however, OTA and aflatoxins are the mycotoxins most frequently reported.
Aflatoxin contamination in meat and meat products has been extensively studied, particularly in swine and poultry, as these species are considered among the most susceptible to the effects of mycotoxins. This increased susceptibility is associated with the characteristics of their relatively simple, ´digestive systems, which allow many of these toxins to be absorbed in their active forms, leading to greater toxicity.
By contrast, carry-over levels reported in ruminants are generally lower than those observed in monogastric species, owing to detoxification processes occurring both in the rumen and at the hepatic level (Tolosa et al., 2021).
However, greater biological susceptibility does not necessarily imply higher concentrations in edible products. In swine, aflatoxin concentrations detected in meat products are generally low, primarily due to hepatic metabolism. In poultry, the biotransformation of these mycotoxins to aflatoxicol has been described in the liver and this metabolite is not considered a risk to human health (Tolosa et al., 2021). An important consideration is that OTA constitutes one of the most relevant mycotoxins in swine, as it is frequently detected in porcine edible tissues and by-products (Stoev et al., 2002).
With regard to other mycotoxins, ZEN and its metabolite α-zearalenol (α-ZEL) have been detected in porcine liver and meat (Pleadin et al., 2015). In addition, the presence of fumonisins FB1 and FB2 has been reported in sausage products and pig liver (Zhao et al., 2015).
Concerning emerging mycotoxins in meat, these compounds have been identified in turkey and chicken tissues, with enniatin (ENN) and its metabolites being primarily detected in the serum and liver of broiler chickens (Křížová et al., 2021).
Milk
One of the most extensively studied examples of carry-over is the hydroxylated metabolite AFM1, derived from AFB1, which is frequently detected in milk and dairy products (Gonçalves et al., 2020; Tolosa et al., 2021). The toxic effects of aflatoxins and their metabolites, affecting both animal species and humans, have been widely documented, with particular emphasis on their carcinogenic potential.
An important consideration regarding the presence of AFM1 in milk is its high thermostability, as this metabolite is highly resistant to thermal treatments such as UHT (Ultra-High Temperature) processing and pasteurisation (Mohamadi et al., 2010).
OTα, a metabolite derived from OTA (formed through biotransformation by the ruminal microbiota), has also been detected in milk and dairy products, although less frequently (Hashimoto et al., 2016).
The presence of other mycotoxins in milk and dairy products, including fumonisins, ZEN and deoxynivalenol (DON),
has been reported (Becker-Algeri et al., 2016). Regarding fumonisins, available studies indicate that this mycotoxin and its metabolites exhibit low carry-over rates (Flores-Flores et al., 2015).
ZEN has been detected in both fresh milk and powdered milk. However, it does not represent a risk to human health, as the concentrations identified have been very low (Flores-Flores et al., 2015; Huang et al., 2014). In the case of DON, only its less toxic form, deepoxy-deoxynivalenol (DOM-1), has been detected in milk and dairy products (Tolosa et al., 2021).
It is worth noting that, in recent years, emerging and modified mycotoxins, such as beauvericin (BEA) and enniatins, have also been detected in milk. For instance, low levels of enniatins have been reported in sheep milk samples (Piątkowska et al., 2018). In addition, carry-over of these mycotoxins has been confirmed in studies of human milk. However, unlike other mycotoxins, they have not been detected in bovine milk (Křížová et al., 2021).
Fish
Mycotoxin carry-over has been studied less extensively in aquaculture than in other animal products. Nevertheless, the principal mycotoxins of concern for the sector have been investigated, and it is recognised that the fish organs exhibiting the highest mycotoxin concentrations are the liver, kidneys, and edible muscle tissues (Tolosa et al., 2021).
For example, in Atlantic salmon (Salmo salar), the carry-over of DON to muscle and kidney tissues is reported to be significant, in contrast to gilt-head seabream (Sparus aurata), where no carry-over has been observed (Pietsch et al., 2014; Nácher-Mestre et al., 2015). Atlantic salmon does not exhibit carry-over of ZEN or its metabolites in muscle tissues. However, rainbow trout (Oncorhynchus mykiss) has been shown to accumulate this mycotoxin in the intestine, liver, and ovaries (Nácher-Mestre et al., 2020).
With regard to emerging mycotoxins, several studies have highlighted the presence of enniatins in farmed fish species, including European seabass (Dicentrarchus labrax) and gilt-head seabream (Sparus aurata), particularly in muscle and liver tissues (Tolosa klzx9x., 2014).
Conclusion
The carry-over of mycotoxins in products of animal origin represents a significant concern, as it may affect the safety and quality of food and feed, and consequently both human and animal health. The establishment of safe exposure levels for mycotoxins, together with the implementation of good agricultural practices and good feed manufacturing practices, constitutes a key strategy to reduce and prevent mycotoxin contamination. In this context, preventing the transfer of these secondary metabolites into products of animal origin is essential for the protection of consumer health.
