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Influence of grains postharvest conditions on mycotoxins occurrence in milk and dairy products

Published: July 13, 2022
By: Clara Mariana Gonçalves LIMA 1, Herique Riley Duarte COSTA 2, Jorge Pamplona PAGNOSSA 3, Nathalia de Castro ROLLEMBERG 4, Josiane Ferreira da SILVA 2, Flávia Michelon DALLA NORA 5, Gaber El-Saber BATIHA 6, Silvani VERRUCK 4.
1 Introduction
Fungi have the ability to transform organic materials into a rich and diverse set of useful products and provide distinct opportunities for tackling the urgent challenges before all humans. Fungal biotechnology can advance the transition from our petroleum-based economy into a bio-based circular economy and has the ability to sustainably produce resilient sources of food, feed, chemicals, fuels, textiles, and materials for construction, automotive and transportation industries, for furniture and beyond. Fungal biotechnology offers solutions for securing, stabilizing and enhancing the food supply for a growing human population, while simultaneously lowering greenhouse gas emissions (Meyer et al., 2020). However, fungi can cause economic losses regarding food deterioration and contamination (Bernardi et al., 2019). Food contamination by fungi occurs in several ways, however, the most worrying form is since some genera of filamentous fungi can produce secondary metabolites, which have toxic characteristics (Conte et al., 2020). These metabolites are called mycotoxins and, when present in food, they cause adverse effects to consumers, called mycotoxicosis (Liao et al., 2019). In this context, the presence of mycotoxins in crops and animal products is a serious problem globally and calls for efforts to safeguard consumers’ health globally (Coppock et al., 2018).
The development of fungi depends on several factors such as substrate composition, temperature, moisture content, water activity, relative humidity, redox potential, and pH (Van Long et al., 2017). Besides, inadequate harvest and post-harvest practices, insect attacks, dry periods, poor fertilization, and competition with other crops may also favor the growth of mycotoxin-producing fungi (Manu et al., 2019).
Toxigenic fungi are considered villains in food for both human and animal consumption (Conte et al., 2020). This is due to the fact that some species have the ability to release toxins with high toxic potential, causing serious complications to consuming organisms (mycotoxicoses). These substances originating from toxigenic fungi are called mycotoxins and are produced mainly by fungi of the genera Fusarium, Aspergillus and Penicillium. There are several types of mycotoxins, such as aflatoxins (AFB1, AFB2, AFG1, AFG2 and AFM1), ochratoxin A (OTA), deoxynivalenol (DON), fumonisins (FB1 and FB2), patulin (PAT) and zearalenone (ZEA) (Luo et al., 2018; Al-Jaal et al., 2019). These toxins are present mainly in grains, cereals and oilseeds, such as wheat, corn, oats, rice, coffee, beans, nuts, peanuts, among others, but they can also be present in foods such as meats, milk and their derivatives, mainly from the consumption of feed produced with contaminated raw materials (Al-Jaal et al., 2019; Yang et al., 2020). It is also important to mention that after aflatoxin AFB1 is ingested by dairy cattle in feed, this mycotoxin undergoes biotransformation by partially converting it into AFM1 that is excreted in milk. In addition, both may be present in the processing of dairy products (Wochner et al., 2017).
It is important to note that milk is considered as a healthy product with substantial health benefits. Therefore, dairy foods could be considered an essential component of an equilibrated diet from a nutritional and functional point of view. It is noteworthy that they are excellent sources of proteins and minerals, especially calcium in a highly bioavailable form. Dairy products can also be considered an excellent matrix for the release of bioactive compounds. Dairy products can improve health or well-being and, when consumed at recommended levels, their benefits include improved immune system function, reduced risk of cardiovascular, reduced risk of bone mass loss, and protection against free radical damage (Verruck et al., 2019a). Since milk and milk products are daily consumed in many parts of the world and they are especially important in the diets of children, who may be more vulnerable to adverse effects from AFM1, multiple nations around the world have enacted food safety regulations for the presence of AFM1 in milk and other dairy products (Turna & Wu, 2021).
In this sense, the consumption of contaminated food can cause serious complications in the short and long term. In humans, teratogenic, carcinogenic, immunosuppressive, and mutagenic effects have been described mainly. For animals, the consumption of feed and grains, especially corn, when contaminated with mycotoxins can cause low food intake, worsen the conversion of nutrients into body mass, thus reducing weight and can reduce productive capacity (Silva et al., 2021; Yang et al., 2020). It is worth mentioning that high AFM1 levels in milk indicate high levels of AFB1 in animal feed. This may imply that the crops used to make that feed such as maize, may have high AFB1 levels, which upon consumption could harm both animal and human health (Turna & Wu, 2021).
The monitoring of mycotoxin content in food is done with great caution, and some foods are subjected to analysis of these contaminants both before domestic market consumption and for export. In this sense, both grains, kinds of cereal, oilseeds, and by-products of these raw materials are periodically evaluated for the content of mycotoxins present, as well as knowledge of their harmful effects on consumers. Thus, the implementation of increasingly lower tolerated ceilings has been reported in the regulations of several countries. These measures aim to ensure that produced food does not have contaminants above acceptable levels. Another important factor that is highlighted in this context is the control of these foods, because, considering that contamination can occur during cultivation and not only in the storage stage, it is necessary to the adoption of practices of crop management, and disease control in the field, as well as in post-harvest to minimize the risks of contamination (Shi et al., 2018).
In this context, Zhang et al. (2019) state that the factors that most influence the production of these toxins are related to storage conditions, as humidity and temperature are the most important factors affecting both the growth and production of toxins. Thus, the moisture requirements may vary between the species of fungi, both in the lower limit of growth moisture and in the interval over which they will prevail. Temperature is another factor that affects grain storage, and the interaction of biotic and abiotic factors that promote grain deterioration is crucial. As the grain is commonly harvested dry or may have its moisture content reduced to a safe level, it now has a less important role than temperature. Thus, the knowledge and understanding of the control of these two variables during storage is extremely important, because the rigid control of these conditions after harvest directly reflects on the chemical health of foods most commonly compromised by mycotoxins. In this sense, the present study aimed to report current information in the literature on the influence of postharvest conditions of grains and animal feed on the occurrence of mycotoxins in milk and dairy products.
2 Mycotoxins
overview Mycotoxins and health disorders associated with the consumption of these contaminants in humans and animals have been recognized as a major health and also an economic problem. When ingested, mycotoxins can cause acute or chronic episodes of diseases, with carcinogenic, mutagenic, teratogenic, estrogenic, hemorrhagic, nephrotoxic, hepatotoxic, neurotoxic, and immunosuppressive effects. Mycotoxins are not equally toxic, their toxicity changes during metabolism, while the susceptibility of animals and humans varies with species, age, nutrition, duration of exposure, and other factors (Moretti et al., 2017). The assessment of adverse health effects is complex by multiple exposures to various mycotoxins, which can lead to additive, synergistic, or antagonistic toxic effects (Ficheux et al., 2012).
The fungi can contaminate the grains through the soil or during planting, harvesting, drying, transportation, and storage of products (Ismaiel & Papenbrock, 2015). Also, another important form of food contamination is when they are exposed to the condition of stress and nutrient unbalance, in which mycotoxins can be produced on food matrices (Telles et al., 2017). The main genera of fungi that are the cause of the formation of these contaminants are Aspergillus, Penicillium, and Fusarium. There are hundreds of identified mycotoxins, but not all have been equally studied. Given the higher occurrence and degree of toxicity, the studies already conducted focus on mycotoxins of the type aflatoxins, patulin, fumonisins, zearalenone, ochratoxins, trichothenines, citrinin, cyclopiazonic acid, gliotoxin and griseofulvin as well as their metabolites (Luo et al., 2018).
It is important to note that the optimal conditions of fungal growth are not necessarily the same for the production of mycotoxins. However, if fungal growth is controlled, the production of mycotoxins can be indirectly controlled. It is worth highlighting the possibility of occurrence of the synergistic effect when different species of fungi contaminate the same food, so under appropriate conditions, more than one toxin is produced using the same substrate. Thus, there is a need to know each toxin separately and the most favorable conditions for its production (Oga et al., 2014).
According to Torres et al. (2014), the main foods affected by the presence of fungi are grains, cereals, and some oilseeds, with peanuts having the highest rates of contamination, constituting a public health problem. In this context, maximum limits of the presence of the main mycotoxins are established by several countries and Table 1 shows the maximum levels stipulated by the “Codex Alimentarius”
3 Grain storage conditions and association with mycotoxin production
The release of mycotoxins by the producing fungi is caused by several factors, which can be divided into two groups, those that influence the production of mycotoxins in the stage of cultivation and harvest and those related to the postharvest period (Tran et al., 2020). In the stage of cultivation is where fungi are inserted in food, however, their growth depends on specific conditions, and the main fungi that attack grains, cereals, and oilseeds are considered fungi of the field, which act in high water activity, being the species of Fusarium graminearium and Aspergillus flavus representing these groups. Aspergillus flavus is also considered, as Penicillium verucossum, a mycotoxinproducing fungus during the storage stage, given that these fungi can release mycotoxins even in foods with low water activities (Midio & Martins, 2000).
Influence of grains postharvest conditions on mycotoxins occurrence in milk and dairy products - Image 1
In addition to the type of fungus present in these grains, cereals, and oilseeds, other factors, such as climatic conditions, water availability, management during cultivation, and type of crop are high influencers in the amount and type of mycotoxins present in food (Ráduly et al., 2020). Besides, the post-harvest stages, among which transport, drying, and storage stand out, can be key steps to reduce the number of mycotoxins in food (Perrone et al., 2020).
Concerning contamination in the cultivation phase, some authors point out that the climatic condition is the one that most influences the production of mycotoxins by fungi (Stanciu et al., 2017). In some studies, data are found that evidence that the higher the humidity and temperature during cultivation, the greater the number of fungi and mycotoxins found in these crops (Kluczkovski, 2019). Thus, in countries where climate change is less intense between seasons, a higher prevalence of these contaminants is found in food (Piacentini et al., 2015). Under certain specific conditions, weather might pose a negative influence on the prevention or control of mycotoxins, due to marked environmental variances between regions, and even between crops planted with different dates of sowing (Ponce-García et al., 2018). Tabuc et al. (2009), studied the presence of mycotoxins in cereals and, they realized through the data obtained in their study, that the cold climate prevents the accumulation of some mycotoxins during cultivation, showing the high correlation of contamination of products with the climate in which they are cultivated.
However, storage is a very worrying step and it is possible to control the production of mycotoxins. This is because the conditions to which food and products are subjected may or may not be favorable for the development of fungi and/or the production of mycotoxins (Luzardo et al., 2016). The conditions related to the composition of food itself, pH, presence of metals and oxygen are extremely important and should be taken into account during the storage of these products. Also in this context, the moisture of the grains, as well as the temperature at which they are stored, are the conditions with the greatest impact on grain quality about the presence of these contaminants (Ponce-García et al., 2018; Ashraf et al., 2021).
For Soldati (2010), temperature and time are closely related to the production of these toxins. However, the minimum temperature for the fungus to grow is not necessarily the minimum temperature with which the toxin is produced, because usually, the production of mycotoxins occurs at a higher temperature. The temperature range that is considered optimal for the production of mycotoxins is between 24 °C and 28 °C. In this sense, considering the storage temperature together with time, the grains can be stored for longer periods when the temperature is maintained in the range between eight and 10 ºC and the relative humidity of the air does not exceed 70%. In this sense, the binomial temperature and humidity should be chosen according to the time that is necessary to store the grains, making this step allow adequate sanitary control of these products (Brooker et al., 1992).
Based on what has been described above, it is emphasized that fungal contamination before harvest is mainly governed by plant host fungi and other biological interactions, while the appearance of fungi in the postharvest stage is due to physical (humidity and temperature) and biotic (insects) factors (Mohapatra et al., 2017). In this context, Mannaa & Kim (2017) divided the mycotoxin-producing species into three distinct groups. According to the authors, the field fungi (pre-harvest) where the species of the genus Alternaria, Epicaccum and Fusarium are included with aw = 1.0. The second group consists of storage fungi post-harvest), represented by the species of the genus Aspergillus, Eurotium and Penicillium with aw < 1.0. Finally, the third fungal group is classified as intermediate (off-season), being composed of the species of the genus Aureobasidium, Cladosporium, Geotrichum and Verticullium which develop during the storage stage in aw between 0.95 and 1.0.
Stored grains and seeds can be affected by some problems, such as fungal growth and the production of toxins by them. Besides, during storage, there is a loss of germination power and dry matter, in addition to changes in nutritional value (Mohapatra et al., 2017). The deterioration of the grain begins with the increase of moisture due to the condensation of water by the effect of “cold wall contact”, mainly with metal structures, and by the emergence of a “hot spot” by a grain load with a moisture content of level higher than the limit for safe storage. They can induce loss of germination capacity and dry matter loss (Fleurat-Lessard, 2017).
Gruzdevienè et al. (2006) analysed flax seed infection at harvest and during storage, found the predominantly fungi of the genus Alternaria and Fusarium. The authors observed fungal development for eight months in a storage site. There was an increase in internal and external contamination by fungal propagules. As a rule, the number of mycotoxins found in the flaxseed of some cultivars was very low, however, a large increase in mycotoxins was observed during storage. In the storage stage, the level of contamination by fungi can vary mainly by factors such as humidity, temperature variations. Since the storage temperature does not exceed 15 °C and has air humidity of 40%.
The amount of water present in a product, such as in food is directly related to the relative humidity of the air and, when these products are stored in an environment with a high concentration of humidity, the food absorbs a certain content of the same. Also in this context, the water activity (aw) of food, which is characterized by the amount of water available for the occurrence of chemical, physical reactions and also for microbial metabolism will be changed depending on the amount of water present in the environment. It is known that the greater the availability of free water in a food, the higher the rates of microbial metabolism and, in foods with reduced aw, and the reactions occur more slowly (Damoraran & Parkin, 2019).
Fungal proliferation becomes lower when food is stored at low relative humidity. It is known that the lower the amount of water available in these foods, the lower the production of mycotoxins. This is because mycotoxins are considered secondary metabolites of the process of obtaining energy that happens at the cellular level and, decreasing the rate of metabolism, consequently, the production of mycotoxins is also slowed (Adeyeye, 2016).
The growth of toxigenic fungi occurs in aw above 0.8, however, each species presents a minimum value for its growth, as can be observed in Table 2. In this table, some values of aw are shown for fungal proliferation and the production of mycotoxins by the main toxigenic fungi (Andrade & Caldas, 2015). As can be observed, the production of mycotoxins by fungi requires higher values of aw when compared to the fungus requirement. Therefore, the proliferation or presence of fungi is not necessarily tied to the presence of mycotoxins in a certain matrix, and an adequate condition is necessary for the release of these contaminants.
Another extremely important factor that has a direct influence on fungal growth and mycotoxin production is the temperature. It is known that most fungi have optimum growth at room temperature and, with this, it is done the control of several processes within the food industry (Midio & Martins, 2000). About toxigenic fungi, Table 3 shows the temperature values for the growth of some fungal species and the production of mycotoxins by them. In general, the optimum growth temperature remains between 20 and 30 °C, with a minimum temperature of three to seven degrees Celsius for fungal growth (Vujanovic et al., 2001).
Several authors studying the influence of temperature and aw on fungal growth and mycotoxin production have concluded that these two factors are dependent on each other. Besides, through these two factors, it is possible to ensure a longer storage time of grains with a lower incidence of fungi and the presence of mycotoxins (Wawrzyniak et al., 2018). Depending on the fungal species in question, the temperature or amount of water present will be a factor of greatest influence and several studies have been conducted to increasingly ensure the health of products such as grains, cereals, and oilseeds from the point of view of the presence of mycotoxins (Shibamoto & Bjeldanes, 2014). In general, it is known that the higher the temperature and the higher the moisture content of the grains, the shorter the grain useful time about fungal proliferation. On the other hand, when using intermediate temperatures with also reduced moisture content, the shelf life of the products increases considerably (Wawrzyniak et al., 2018).
Influence of grains postharvest conditions on mycotoxins occurrence in milk and dairy products - Image 3
Grains, cereals, and oilseeds when stored at temperatures close to 25 °C and relative humidity of 26% are suitable for consumption for up to one week. On the other hand, when this humidity, for example, is reduced to 18% and the temperature to about five degrees Celsius, the storage time grows to up to 50 weeks, showing the high correlation between these two factors (Pitt & Hocking, 2009).
The control of fungal growth and the production of mycotoxins is extremely important for obtaining products suitable for human and animal consumption. In this sense, the control of some factors, such as temperature and aw the most commonly affected foods is of fundamental importance, with constantly seeking an adequate safety of the foods that are consumed by the population (Kluczkovski, 2019; Wawrzyniak et al., 2018).
4 Influence of animal feed on the occurrence of mycotoxins
The incidence of mycotoxins in the products is variable and sporadic in different years and geographic locations due in part to the variation in climatic conditions. Climate can significantly affect growth, distribution, and mycotoxin production in fungi and its increasing change has the potential to increase the risks that mycotoxigenic fungi pose to food and feed safety (Magnoli et al., 2019).
Many developing countries and transitional nations are unaware of the prevalence of mycotoxins in animal products while most do not have strict monitoring and surveillance practices regarding safety of animal products. The livestock management practices mainly focus on increasing the production and yield without much consideration on the safety of the animal product (Coppock et al., 2018). Mycotoxin residues are transferred from the feed to products of animal origin; however, less attention has been paid to this in such countries (Andrade et al., 2020).
Toxic residues in animal products are mainly related to the consumption of contaminated feed or forages. Animal by-products viz., meat, milk, and eggs are obtained after consumed feedstuff has been subjected to enzymatic and microbial transformations leading to the production of absorbable metabolites in the gut. During this process, nutrients, volatile fatty acids, and metabolites (toxic and beneficial) are absorbed into the bloodstream of the animal and may be later excreted through urine and feces. The toxins that are not excreted generally remain as residues in the edible organs and muscles. Monogastric and younger animals are more sensitive to mycotoxins than ruminant and older animals. Grazing animals are also exposed to mycotoxin intake which corresponds to a high level of mycotoxins in their products including meat and milk (Adegbeye et al., 2020).
Several factors can alter the nutrition of animals such as species, breed, genetics, sex, consumption of ration, diet energy level, nutrients availability, room temperature, air humidity, health status among others. Poultry, pigs, and aquatic vertebrates are very sensitive to mycotoxins. Because of their high consumption, they are exposed to cereal mycotoxins and chronic contamination. Ruminants are usually more resistant to the adverse effects of mycotoxins since the rumen microbiota partially degrades mycotoxins. It is important to highlight that mycotoxins’ effects on horses are limited when compared to those of other animals (Bhat et al., 2010).
The most economically important mycotoxins in terms of their prevalence and their negative effects on animal performance are aflatoxin B1 (AFB1), DON, ZEA, OTA, trichothecenes, and fumonisin B1 (FB1). The high ingestion of mycotoxins can cause deterioration in animal health and productivity. The diseases caused by mycotoxins, the mycotoxicosis, reduce animal production and increase conversion rates. Moreover, they generate greater morbidity and mortality. Low mycotoxins concentrations can cause subclinical losses in production and increase the risk and incidence of other diseases. It is important to consider the exposure to mycotoxins co-contamination due to the harmful additive and/or synergistic effects on animal health. The use of a safe diet in which the risk of mycotoxin contamination can be minimized and the cost/benefit is accurately quantified should allow the maximization of herd productivity (Magnoli et al., 2019).
5 Mycotoxins in milk and dairy products
Milk is one of the main sources of nutrients essential for the growth, development, and maintenance of human health. It is worth mentioning that dairy products are related to nutritive value and positive health benefits attached to these products and are widely consumed in the world (Verruck et al., 2019b). However, if good agricultural practices are not careful done, it can also be a vehicle of toxic agents, causing serious health risks in individuals who consume, especially children (Gabai & Novelli, 2018).
Among food contaminants, aflatoxins stand out, as secondary metabolites of fungi of the Aspergillus genus relevant to human and animal health. Among the aflatoxin analogs identified so far, aflatoxin B1 (AFB1) is the most prevalent and the most toxic. Aflatoxin B1 is known as a natural carcinogenic agent (hepatotoxicity) and its incidence is high in several raw materials such as grains and, consequently, rations and silage, which are part of the dairy cattle diet. When ingested by animals, it undergoes liver biotransformation, partially converting to aflatoxin M1, which is excreted in milk (Figure 1). Once present in milk, these aflatoxins can withstand most treatments for obtaining dairy products, therefore, they can be present in cheeses and yogurts (Wochner et al., 2019). AFB1 and AFM1 are classified as cancerous agents for humans and animals by the International Agency for Research on Cancer (IARC). According to the agency, there is sufficient evidence regarding the carcinogenicity of AFB1 and AFM1 in humans and experimental animals to classify it in carcinogenicity group 1 (International Agency for Research on Cancer, 2012).
Sibaja (2019) conducted a survey of the occurrence of AFM1 in milk and dairy products in Latin America and the Caribbean in the literature, as well as the estimated risk of exposure of this population by daily intake (ID). The results show that 70% (n=3267) and 63% (n=969) of the milk and dairy samples analysed in the last 15 years were contaminated by AFM1, at concentrations range of 0.001‐23.10 μg L-1 and 0.001–18.12 μg kg-1, respectively. In addition, the highest ID values were observed in Brazil, Costa Rica, Colombia and Mexico, i.e., 0.0024, 0.0010, 0.0012 and 0.0209 μg kg-1 mc day-1, respectively. Besides, a study was conducted in 51 samples of milk powder marketed in the Caribbean region of Colombia, in which the occurrence of FMA1 was found at levels ranging from 0.20 to 1.19 μg kg-1, Finally, it was estimated that the maximum ingested level of AFM1 in milk powder consumption in this region is 0.013 μg kg-1 mc day-1, which is above the estimated average consumption for Latin America according to the FAO/WHO Joint Committee of Experts (0.0058 μg kg-1 mc day-1).
The current Brazilian legislation stipulates the maximum concentration of 20 μg.kg-1 of aflatoxins in food intended for human consumption. Concentrations of up to 50 μg.kg-1 are allowed for raw materials intended for animal consumption. Regarding the presence of AM1 in milk, RDC No . 07 of 2011 stipulates a maximum of 5.0 μg.kg-1 and 0.5 μg.kg-1 for milk powder and fluid milk, respectively (Brasil, 2011). Due to the high toxicity of aflatoxins, many countries have established stricter regulations for aflatoxins in food, and these values vary widely between different countries. In Brazil and the United States the maximum residue limit (MRL) of AM1 in milk is the same, however, in most Asian and European countries, the acceptable levels of this mycotoxin are 10 times lower.
Influence of grains postharvest conditions on mycotoxins occurrence in milk and dairy products - Image 4
Hajmohammadi et al. (2020) investigated samples of raw cow’s milk produced during the summer and winter in an Iran province. All milk samples had high frequency of AFM1 contamination, with higher AFM1 levels (74 ng/L) in the summer compared with the milk samples produced during winter (47 ng/L). Forty per cent of the analysed samples could be considered as not safe for human consumption, since they had AFM1 levels above the Maximum Permitted Level (MPL) established in Iran (50 ng/L). The authors reported the need for urgent measures to control aflatoxins in the production of milk samples with a special focus on the food management of the dairy cow in order to avoid aflatoxin contamination in milk. Ahmadi (2020) studied the probable public health hazard imposed by bovine milk in relation to AFM1 in the West of Iran. The assessment of AFM1, using an ELISA test, indicated 62.22% and 21.11% of 45 samples of raw and pasteurized milk were above the permissible content of Codex and Iranian standard levels, respectively.
In the study conducted by Daou et al. (2020) was reported high contamination levels of AFM1 in raw, pasteurized, and UHT milk in addition to dairy products. The consumption of milk and dairy in Lebanon can be considered hazardous and may present a significant risk on the health of the Lebanese population especially children. Therefore, there is an urgent need for governmental authorities to set a clear strategy that aims at reducing AFM1 contamination. This strategy must include; supporting small scale farms and educating farmers on proper practices that increase milk quality; ensuring the safety of feed administered to cattle; strengthening collection centers and cooperatives and supplying them with necessary laboratory equipment to facilitate analysis of milk delivered to them; and finally reinforcing strict regulations and measures and continuously monitoring AFM1 contamination in order to preserve the quality and ensure the safety of milk and dairy products consumed by Lebanese population. In this context, Gonçalves et al. (2021) evaluated the occurrence of AFM1 in bulk raw and pasteurized milks, and the resulting Minas Frescal cheese manufactured in cheese-processing plants from São Paulo, Brazil and a high incidence of AFM1 was observed in samples. This reinforces the need to control AFM1 in dairy products. Although all samples complied with the Brazilian’s MPL for AFM1 in milk or cheese, 1 sample (4%) of raw milk and 2 samples (8%) of pasteurized milk contained AFM1 levels exceeding the European MPL of 0.05 µg/L. As a consequence, the AFM1 milk concentration levels reported could contribute for the overall exposure to dietary aflatoxins.
In other countries such as Uruguay, AFM1 levels are also worrisome, considering that in some studies the amount of samples with a concentration higher than MRL is 11% of the samples evaluated. Studies conducted in Europe, Africa and Asia also corroborate that the presence of mycotoxins in both plant and animal foods is a worrying point when related to food safety and public health (Capelli et al., 2019; Min et al., 2020; Sharma et al., 2020). In this sense, some studies have been conducted in order to perform the decontamination of food products (Assaf et al., 2019; Porto et al., 2019). Adsorption through nonviable microorganisms and clay materials are the most effective, promising approaches for decontamination of AFM1 from milk and dairy products (Muaz et al., 2021).
5 Conclusion
The presence of mycotoxins in food and feed is a public health problem since these products are consumed by humans and animals, respectively. In this sense, effective control at all stages of the production chain is extremely important. Some factors, such as the temperature and humidity at which the grains are stored, are the main conditions that can be controlled during storage, aiming to reduce the growth of fungi and the production of mycotoxins. Animal feed contaminated with toxins results in animal products with health risks, especially bovine milk. Further studies on exploring the prevalence of mycotoxins in different materials and strategies to minimize their occurrence and harmful effects are highly encouraged.
      
This article was originally published in Food Science and Technology, Campinas, v42, e16421, 2022. DOI: https://doi.org/10.1590/fst.16421. This is an Open Access article licensed under a Creative Commons Attribution License.

Adegbeye, M.J., Reddy, P.R.K., Chilaka, C.A., Balogun, O.B., Elghandour,
M.M.M.Y., Rivas-Caceres, R.R., & Salem, A.Z.M. (2020). Mycotoxin toxicity and residue in animal products: Prevalence, consumer exposure and reduction strategies–A review. Toxicon, 177, 96-108. http://dx.doi.org/10.1016/j.toxicon.2020.01.007.
Adeyeye, S. A. (2016). Fungal mycotoxins in foods: A review. Cogent
Food & Agriculture, 2(1), 1213127. http://dx.doi.org/10.1080/2331
1932.2016.1213127.
Andrade, P. D., Dias, J. V., Souza, D. M., Brito, A. P., van Donkersgoed,
G., Pizzutti, I. R., & Caldas, E. D. (2020). Mycotoxins in cereals and cereal-based products: Incidence and probabilistic dietary risk assessment for the Brazilian population. Food and Chemical
Toxicology, 143, 111572. http://dx.doi.org/10.1016/j.fct.2020.111572.
PMid:32673632.
Ahmadi, E. (2020). Potential public health risk due to consumption of contaminated bovine milk with aflatoxin M1 and Coxiella burnetii in the West of Iran. International Journal of Dairy Technology, 73(3),
479-485. http://dx.doi.org/10.1111/1471-0307.12687.
Al-Jaal, B. A., Jaganjac, M., Barcaru, A., Horvatovich, P., & Latiff,
A. (2019). Aflatoxin, fumonisin, ochratoxin, zearalenone and deoxynivalenol biomarkers in human biological fluids: A systematic literature review, 2001-2018. Food and Chemical Toxicology, 129,
211-228. http://dx.doi.org/10.1016/j.fct.2019.04.047. PMid:31034935.
Andrade, P. D., & Caldas, E. D. (2015). Aflatoxins in cereals: worldwide occurrence and dietary risk assessment. World Mycotoxin Journal,
8(4), 415-443. http://dx.doi.org/10.3920/WMJ2014.1847.
Ashraf, S. A., Siddiqui, A. J., Elkhalifa, A. E. O., Khan, M. I., Patel, M.,
Alreshidi, M., Moin, A., Singh, R., Snoussi, M., & Adnan, M. (2021).
Innovations in Nanoscience for the Sustainable Development of Food and Agriculture with Implications on Health and Environment.
The Science of the Total Environment, 768, 144990. http://dx.doi. org/10.1016/j.scitotenv.2021.144990. PMid:33736303.
Assaf, J. C., Khoury, A. E., Chokr, A., Louka, N., & Atoui, A. (2019).
A novel method for elimination of aflatoxin M1 in milk using
Lactobacillus rhamnosus GG biofilm. International Journal of Dairy
Technology, 72(2), 248-256. http://dx.doi.org/10.1111/1471-0307.12578.
Bernardi, A. O., Garcia, M. V., & Copetti, M. V. (2019). Food industry spoilage fungi control through facility sanitization. Current Opinion in
Food Science, 29, 28-34. http://dx.doi.org/10.1016/j.cofs.2019.07.006.
Bhat, R., Rai, R. V., & Karim, A. A. (2010). Mycotoxins in food and feed: present status and future concerns. Comprehensive Reviews in Food
Science and Food Safety, 9(1), 57-81. http://dx.doi.org/10.1111/j.1541-
4337.2009.00094.x. PMid:33467806.
Brasil. Ministério da Saúde. (2011, Fevereiro 07). Dispõe sobre limites máximos tolerados (LMT) para micotoxinas em alimentos (Resolução n° 07 de 18 de fevereiro de 2011). Diário Oficial [da] República
Federativa do Brasil.
Brooker, D. B., Bakker-Arkema, D. B., Hal, L. F. W., & Carl, W. (1992).
Drying and storage of grains and oilseeds (1st ed.). New York: Springer.
Capelli, A., Suárez, G., & García y Santos, C. (2019). Aflatoxinas en alimentos y leche de vacas de 18 establecimientos comerciales de las regiones centro-sur y este de Uruguay. Veterinaria (Montevideo),
55(212), 52-56.
Conte, G., Fontanelli, M., Galli, F., Cotrozzi, L., Pagni, L., & Pellegrini,
E. (2020). Mycotoxins in feed and food and the role of ozone in their detoxification and degradation: An update. Toxins, 12(8), 486. http:// dx.doi.org/10.3390/toxins12080486. PMid:32751684.
Coppock, R. W., Christian, R. G., & Jacobsen, B. J. (2018). In R. C.
Gupta (Ed.), Aflatoxins in veterinary toxicology basic and clinical principles. Waltham: Academic Press.
Damoraran, S., & Parkin, K. L. (2019). Química de Alimentos de Fennema (5. ed.). Porto Alegre: Artmed.
Daou, R., Afif, C., Joubrane, K., Khabbaz, L. R., Maroun, R., Ismail, A.,
& Khoury, A. (2020). Occurrence of aflatoxin M1 in raw, pasteurized,
UHT cows’ milk, and dairy products in Lebanon. Food Control, 111,
107055. http://dx.doi.org/10.1016/j.foodcont.2019.107055.
Ficheux, A. S., Sibiril, Y., & Parent-Massin, D. (2012). Co-exposure of
Fusarium mycotoxins: in vitro myelotoxicity assessment on human hematopoietic progenitors. Toxicon, 60(6), 1171-1179. http://dx.doi. org/10.1016/j.toxicon.2012.08.001. PMid:22921581.
Fleurat-Lessard, F. (2017). Integrated management of the risks of stored grain spoilage by seedborne fungi and contamination by storage mould mycotoxins–An update. Journal of Stored Products Research,
71, 22-40. http://dx.doi.org/10.1016/j.jspr.2016.10.002.
Gabai, G., & Novelli, E. (2018). Investigating the troublesome relationship between the cow milk and human health. Research in Veterinary
Science, 120, 1-3. http://dx.doi.org/10.1016/j.rvsc.2018.08.003.
PMid:30144621.
Gonçalves, B. L., Ulliana, R. D., Ramos, G. L., Cruz, A. G., Oliveira, C. A.,
Kamimura, E. S., & Corassin, C. H. (2021). Occurrence of aflatoxin
M1
in milk and Minas Frescal cheese manufactured in Brazilian dairy plants. International Journal of Dairy Technology, 74, 1-4.
Gruzdevienè, E., Mankeviciene, A., Lugauskas, A., & Repeckiene, J. (2006). The effect of environmental conditions on the variation of fungi and mycotoxin contents in oil flax seed. Ekologija (Lietuvos
Mokslu Akademija), 3, 64-70.
Hajmohammadi, M., Valizadeh, R., Naserian, A., Nourozi, M. E., Rocha,
R. S., & Oliveira, C. A. (2020). Composition and occurrence of aflatoxin M1 in cow’s milk samples from Razavi Khorasan Province,
Iran. International Journal of Dairy Technology, 73(1), 40-45. http:// dx.doi.org/10.1111/1471-0307.12661.
International Agency for Research on Cancer – IARC. (2012). Chemical agents and related occupations. Retrieved from https://monographs. iarc.fr/wp-content/uploads/2018/06/mono100F.pdf
Ismaiel, A. A., & Papenbrock, J. (2015). Mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture, 5(3), 492-537. http:// dx.doi.org/10.3390/agriculture5030492.
Kluczkovski, A. M. (2019). Fungal and mycotoxin problems in the nut industry. Current Opinion in Food Science, 29, 56-63. http://dx.doi. org/10.1016/j.cofs.2019.07.009.
Liao, Y., Peng, Z., Chen, L., Liu, L., Wu, Q., & Yang, W. (2019). Roles of microRNAs and prospective view of competing endogenous
RNAs in mycotoxicosis. Mutation Research/Reviews in Mutation
Research, 782, 108285. http://dx.doi.org/10.1016/j.mrrev.2019.108285.
PMid:31843139.
Luo, Y., Liu, X., & Li, J. (2018). Updating techniques on controlling mycotoxins-A review. Food Control, 89, 123-132. http://dx.doi. org/10.1016/j.foodcont.2018.01.016.
Luzardo, O. P., Bernal-Suárez, M. M., Camacho, M., HenríquezHernández, L. A., Boada, L. D., Rial-Berriel, C., Almeida-González,
M., Zumbado, M., & Díaz-Díaz, R. (2016). Estimated exposure to
EU regulated mycotoxins and risk characterization of aflatoxininduced hepatic toxicity through the consumption of the toasted cereal flour called “gofio”, a traditional food of the Canary Islands (Spain). Food and Chemical Toxicology, 93, 73-81. http://dx.doi. org/10.1016/j.fct.2016.04.022. PMid:27132021.
Magnoli, A. P., Poloni, V. L., & Cavaglieri, L. (2019). Impact of mycotoxin contamination in the animal feed industry. Current Opinion in Food
Science, 29, 99-108. http://dx.doi.org/10.1016/j.cofs.2019.08.009.
Mannaa, M., & Kim, K. D. (2017). Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology, 45(4), 240-254. http://dx.doi.org/10.5941/
MYCO.2017.45.4.240. PMid:29371792.
Manu, N., Opit, G. P., Osekre, E. A., Arthur, F. H., Mbata, G., Armstrong,
P., Danso, J. K., McNeill, S. G., & Campbell, J. F. (2019). Moisture content, insect pest infestation and mycotoxin levels of maize in markets in the northern region of Ghana. Journal of Stored Products
Research, 80, 10-20. http://dx.doi.org/10.1016/j.jspr.2018.10.007.
Meyer, V., Basenko, E. Y., Benz, J. P., Braus, G. H., Caddick, M. X.,
Csukai, M., de Vries, R. P., Endy, D., Frisvad, J. C., Gunde-Cimerman,
N., Haarmann, T., Hadar, Y., Hansen, K., Johnson, R. I., Keller,
N. P., Kraševec, N., Mortensen, U. H., Perez, R., Ram, A. F. J.,
Record, E., Ross, P., Shapaval, V., Steiniger, C., van den Brink, H., van Munster, J., Yarden, O., & Wösten, H. A. B. (2020). Growing a circular economy with fungal biotechnology: a white paper. Fungal
Biology and Biotechnology, 7(1), 1-23. http://dx.doi.org/10.1186/ s40694-020-00095-z. PMid:32280481.
Midio, A. F., & Martins, D. I. (2000). Toxicologia de Alimentos (1. ed.).
São Paulo: Varela.
Min, L., Li, D., Tong, X., Sun, H., Chen, W., Wang, G., Zheng, N., &
Wang, J. (2020). The challenges of global occurrence of aflatoxin M1 contamination and the reduction of aflatoxin M1 in milk over the past decade. Food Control, 117, 107352. http://dx.doi.org/10.1016/j. foodcont.2020.107352.
Mohapatra, D., Kumar, S., Kotwaliwale, N., & Singh, K. K. (2017). Critical factors responsible for fungi growth in stored food grains and nonChemical approaches for their control. Industrial Crops and Products,
108, 162-182. http://dx.doi.org/10.1016/j.indcrop.2017.06.039.
Moretti, A., Logrieco, A. F., & Susca, A. (2017). Mycotoxins: An underhand food problem. In Moretti, A., & Susca, A. Mycotoxigenic
Fungi. New York: Humana Press. http://dx.doi.org/10.1007/978-1-
4939-6707-0_1.
Muaz, K., Riaz, M., Oliveira, C. A. F. D., Akhtar, S., Ali, S. W., Nadeem,
H., Park, S., & Balasubramanian, B. (2021). Aflatoxin M1 in milk and dairy products: Global occurrence and potential decontamination strategies. Toxin Reviews, 20, 1-18. http://dx.doi.org/10.1080/1556
9543.2021.1873387.
Oga, S., Camargo, M. M. A., & Batistuzzo, J. A. O. (2014). Fundamentos de Toxicologia (4th ed.). São Paulo: Atheneu.
Perrone, G., Ferrara, M., Medina, A., Pascale, M., & Magan, N. (2020).
Toxigenic Fungi and Mycotoxins in a Climate Change Scenario:
Ecology, Genomics, Distribution, Prediction and Prevention of the Risk. Microorganisms, 8(10), 1496. http://dx.doi.org/10.3390/ microorganisms8101496. PMid:33003323.
Piacentini, K. C., Savi, G. D., Pereira, M. E., & Scussel, V. M. (2015).
Fungi and the natural occurrence of deoxynivalenol and fumonisins in malting barley (Hordeum vulgare L.). Food Chemistry, 187, 204-209. http://dx.doi.org/10.1016/j.foodchem.2015.04.101. PMid:25977017.
Pitt, J. I., & Hocking, A. D. (2009). Fungi and food spoilage (1st ed.).
United States: Springer.
Ponce-García, N., Serna-Saldivar, S., & Garcia-Lara, D. (2018). Fumonisins and their analogues in contaminated corn and its processed foods–a review. Food Additives & Contaminants: Part A, 35(11), 2183-2203. http://dx.doi.org/10.1080/19440049.2018.1502476. PMid:30028638.
Porto, Y. D., Trombete, F. M., Freitas-Silva, O., De Castro, I. M., Direito, G.
M., & Ascheri, J. L. R. (2019). Gaseous ozonation to reduce aflatoxins levels and microbial contamination in corn grits. Microorganisms,
7(8), 220. http://dx.doi.org/10.3390/microorganisms7080220.
PMid:31357684.
Ráduly, Z., Szabó, L., Madar, A., Pócsi, I., & Csernoch, L. (2020).
Toxicological and medical aspects of Aspergillus-derived Mycotoxins entering the feed and food chain. Frontiers in Microbiology, 10,
2908. http://dx.doi.org/10.3389/fmicb.2019.02908. PMid:31998250.
Sharma, H., Jadhav, V. J., & Garg, S. R. (2020). Aflatoxin M1 in milk in Hisar city, Haryana, India and risk assessment. Food Additives
& Contaminants: Part B, 13(1), 59-63. http://dx.doi.org/10.1080/1
9393210.2019.1693434. PMid:31766982.
Shi, H., Li, S., Bai, Y., Prates, L. L., Lei, Y., & Yu, P. (2018). Mycotoxin contamination of food and feed in China: Occurrence, detection techniques, toxicological effects and advances in mitigation technologies. Food Control, 91, 202-215. http://dx.doi.org/10.1016/j. foodcont.2018.03.036.
Shibamoto, T., & Bjeldanes, L. F. (2014). Introdução à toxicologia de alimentos (2. ed.). Rio de Janeiro: Elsevier.
Sibaja, K. V. M. (2019). Leite: ocorrência de aflatoxinas B1 e M1 e o uso de peroxidade como estratégia de mitigação (Doctoral thesis).
Federal University of Rio Grande, Rio Grande.
Silva, J. V. B. D., Oliveira, C. A. F. D., & Ramalho, L. N. Z. (2021). An overview of mycotoxins, their pathogenic effects, foods where they are found and their diagnostic biomarkers. Food Science and
Technology. In press.
Soldati, R. C. (2010). Micotoxinas em alimentos vegetais. Aspectos gerais (1st ed.). São Paulo: Ixtlan.
Stanciu, O., Juan, C., Miere, D., Dumitrescu, A., Bodoki, E., Loghin,
F., & Mañes, F. (2017). Climatic conditions influence emerging mycotoxin presence in wheat grown in Romania–A 2-year survey.
Crop Protection (Guildford, Surrey), 100, 124-133. http://dx.doi. org/10.1016/j.cropro.2017.06.014.
Tabuc, C., Marin, D., Guerre, P., Sesan, T., & Bailly, J. D. (2009). Molds and mycotoxin content of cereals in southeastern Romania. Journal of Food Protection, 72(3), 662-665. http://dx.doi.org/10.4315/0362-
028X-72.3.662. PMid:19343960.
Telles, A. C., Kupski, L., & Badiale-Furlong, E. (2017). Phenolic compound in beans as protection against mycotoxins. Food Chemistry,
214, 293-299. http://dx.doi.org/10.1016/j.foodchem.2016.07.079.
PMid:27507478.
Torres, A. M., Barros, G. G., Palacios, S. A., Chulze, S. N., & Battilani,
P. (2014). Review on pre-and post-harvest management of peanuts to minimize aflatoxin contamination. Food Research International,
62, 11-19. http://dx.doi.org/10.1016/j.foodres.2014.02.023.
Tran, T. M., Ameye, M., Phan, L. T. K., Devlieghere, F., Saeger, S.,
Eeckhout, M., & Audenaert, K. (2020). Post-harvest contamination of maize by Fusarium verticillioides and fumonisins linked to traditional harvest and post-harvest practices: a case study of smallholder farms in Vietnam. International Journal of Food Microbiology,
339, 109022. http://dx.doi.org/10.1016/j.ijfoodmicro.2020.109022.
PMid:33340942.
Turna, N. S., & Wu, F. (2021). Aflatoxin M1
in milk: A global occurrence, intake, & exposure assessment. Trends in Food Science & Technology,
110, 183-196. http://dx.doi.org/10.1016/j.tifs.2021.01.093.
Van Long, N. N., Vasseur, V., Coroller, L., Dantigny, P., Le Panse, S., Weill,
A., Mounier, J., & Rigalma, K. (2017). Temperature, water activity and pH during conidia production affect the physiological state and germination time of Penicillium species. International Journal of Food Microbiology, 241, 151-160. http://dx.doi.org/10.1016/j. ijfoodmicro.2016.10.022. PMid:27780083.
Verruck, S., Balthazar, C. F., Rocha, R. S., Silva, R., Esmerino, E. A.,
Pimentel, T. C., Freitas, M. Q., Silva, M. C., Da Cruz, A. G., &
Prudencio, E. S. (2019a). Dairy foods and positive impact on the consumer’s health. Advances in Food and Nutrition Research, 89, 95-
164. http://dx.doi.org/10.1016/bs.afnr.2019.03.002. PMid:31351531.
Verruck, S., Dantas, A., & Prudencio, E. S. (2019b). Functionality of the components from goat’s milk, recent advances for functional dairy products development and its implications on human health. Journal of Functional Foods, 52, 243-257. http://dx.doi.org/10.1016/j. jff.2018.11.017.
Vujanovic, V., Smoragiewicz, W., & Krzysztyniak, K. (2001). Airborne fungal ecological niche determination as one of the possibilities for indirect mycotoxin risk assessment in indoor air. Environmental
Toxicology: An International Journal, 16(1), 1-8. http://dx.doi. org/10.1002/1522-7278(2001)16:1<1::AID-TOX10>3.0.CO;2-8.
PMid:11345539.
Wawrzyniak, J., Waskiewicz, A., & Ryniecki, A. (2018). Evaluation of critical points of mould growth and mycotoxin production in the stored barley ecosystem with a hazardous initial microbiological state of grain. Journal of Stored Products Research, 77, 166-176. http://dx.doi.org/10.1016/j.jspr.2018.04.008.
Wochner, K. F., Becker-Algeri, T. A., Colla, E., Badiale-Furlong, E., &
Drunkler, D. A. (2017). The action of probiotic microorganisms on chemical contaminants in milk. Critical Reviews in Microbiology,
44(1), 112-123. http://dx.doi.org/10.1080/1040841X.2017.1329275.
PMid:28537817.
Wochner, K. F., Moreira, M. C., Kalschne, D. L., Colla, E., & Drunkler,
D. A. (2019). Detoxification of Aflatoxin B1 and M1 by Lactobacillus acidophilus and prebiotics in whole cow’s milk. Journal of Food
Safety, 39(5), e12670. http://dx.doi.org/10.1111/jfs.12670.
Yang, C., Song, G., & Lim, W. (2020). Effects of mycotoxin-contaminated feed on farm animals. Journal of Hazardous Materials, 389, 122087. http://dx.doi.org/10.1016/j.jhazmat.2020.122087. PMid:32004836.
Zhang, Y., Pei, F., Fang, Y., Li, P., Xia, J., Sun, L., Zou, Y., Shen, F., &
Hu, Q. (2019). Interactions among Fungal Community, Fusarium
Mycotoxins, and Components of Harvested Wheat under Simulated
Storage Conditions. Journal of Agricultural and Food Chemistry,
67(30), 8411-8418. http://dx.doi.org/10.1021/acs.jafc.9b02021.
PMid:31246458.

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