Mycotoxin Biosorbents: a promising alternative in the mycotoxins control

The use of agents that suppress or reduce mycotoxin absorption, enhance excretion or modify their mechanisms of action are the main strategies for mycotoxin detoxification in animal production. Within these characteristics, adsorbents have been extensively used as feed additives, such as aluminosilicates, bentonites, zeolites, sepiolites, diatomite, polyvinylpyrrolidone, cholestyramine and activated carbon. However, the use of these agents has certain limitations and most of them are not degraded when released into the environment. The emerging alternatives are natural adsorbents, which have proven to be simple, fast, environmentally friendly and less expensive than conventional ones. Biosorption is thus a new and secondary concept of adsorption, where the sorbent is a biological origin component. Several studies have reported successful in vitro results using biomaterials such as agro-industrial waste for mycotoxin adsorption. Some of the residues are effective in binding mycotoxins in vivo, reducing their bioavailability and allowing their efficient excretion through faeces. Therefore, the use of agro-industrial residues seems to be a promising alternative in the mycotoxins control (Aguilar, 2021).

The most common agro-industrial residues are: leaves, tubers, roots, bark, pulp, seeds, skins, stones and others. In addition to their valuable nutrient content, these products have pores and multi-layered structures with cavities and channels that provide a large surface area for the binding of several molecules. Agro-industrial residues such as fibres, pomaces, fruit peel and seeds have shown a role as mycotoxin binding agents both in vitro and in vivo studies (Aguilar, 2021). Some of the agro-industrial wastes used as biosorbents are listed below.

Agro-industrial wastes
1. Dietary fiber

Dietary fiber is that portion of plants composed of soluble and insoluble carbohydrates non-digestible and lignin, which is not digested and absorbed in the small intestine, while complete or partial fermentation in the large intestine. Whole fiber can be found in food, such as vegetables, whole grains, fruits, cereal bran, and flour.

There are several classifications and elements that go into the concept of fiber. One classification is usually based on solubility. According to this characteristic, soluble fibers are mainly non-cellulose polysaccharides, e.g. galactomannan, pectin, mucilage and β-glucan; while non-soluble fibers constitute the plant cell wall, and include cellulose, lignin and hemicellulose (Aguilar, 2021). Since 1980, dietary fiber has been studied as a mycotoxin binder in animal gut, and it has been reported that its consumption reduces the incidence of mycotoxicosis in animals.

In 2011, a group of researchers patented the use of very fine-grained plant fibers to reduce the bioavailability of mycotoxins in animals (Tangni, 2011). It has been reported that micronized wheat fibers had the potential to reduce the bioavailability of AFB1 and OTA. In addition, the researchers also found that using dietary fibers increased fecal excretion by 15-35%. Despite the effect of dietary fibers as biosorbents, their action can be impaired by the occurrence of certain factors, such as bacteria. In vivo digestive models have been implemented to simulate the physiological conditions of the gastrointestinal tract, including digestive enzymes, pH, salt concentration and digestion time. Through this system, it was observed that bacteria (mainly in the colon) have the ability to ferment certain fibers, causing a greater exposure of the intestine to mycotoxins and increasing their bioavailability. In contrast, low-fermentable fibers (such as cellulose) are more resistant to bacterial action.

Other fibers such as chitosan and β-(1,3)-glucan also reduce bioaccess of mycotoxins through the colon and prevent bacterial fermentation. It is worth mentioning that some probiotic lines have a toxin sequestering effect, thus, the combination of these probiotic organisms with non-fermentable fibers may reduce the bioavailability of mycotoxins in the gut (Aguilar, 2021).

2. Pomaces

Pomaces are by-products of fruit and vegetable processing. They are usually residues of cell walls, seeds or stems. Grape and olive skins have been used extensively in mycotoxin adsorption. Grape pomaces are the result of the vinification process and consist of the pulp, seeds or skins residues after pressing or fermentation (Vázquez, 2022). These residues usually contain phenolic compounds, carbohydrates, fibers, lipids, proteins, vitamins and minerals. Results from in vitro studies conducted on mycotoxins, grape skin has shown promising results in the adsorption of ZEN, AFB1 and OTA (Greco, 2019). This adsorption property of the grape pomaces is not due to the amount of tannins present in its composition, but to the phenolic components and fibers contained, which are more effective in adsorbing aflatoxins (Vázquez, 2022). The application of those biomaterials is influenced by some parameters such as pH conditions, the presence of enzymes, bile salts and the contact time, which impact on the desorption of toxins. For example, changes in pH when using grape pomace could mirror mycotoxin absorption process: AFB1 and ZEN adsorption by grape pomace was stable in monogastric GI tract pH range, whereas pH changes could affect FB1 and OTA adsorption to a certain extent (Aguilar, 2021).

Finally, mycotoxin adsorption such as AFB1 and ZEN from grape pomaces occurs through multiple hydrophobic interactions at sites of similar affinity. This adsorption mechanism varies according to the material used, and the adsorption of mycotoxins may also vary according to the original type of grape from which the residue is derived, for example, white grape skins are the most effective at adsorbing mycotoxins compared to red grape skins. Other types of pomaces that have been studied for their in vitro mycotoxin adsorption capacity include olive, blueberry and cherry pomaces (Aguilar, 2021).

3. Fruit peels

Fruit peels are another significant residue produced by the food processing industry. In vitro studies have been carried out to investigate the adsorption of heavy metals and dyes, as well as mycotoxins removal. The adsorptive capacity was tested on peels from oranges, lemons, pomegranates, bananas and durians. Banana peels have also been studied in the literature. However, there are conflicting results regarding their ability to remove aflatoxin (Aguilar, 2021). However, several studies have reported increased adsorption capacity with extended exposure time of banana peels to aflatoxins (Ali, 2019). In turn, the use of this residue reduces the negative effects of mycotoxins on the liver and kidneys. The adsorption mechanism of banana peel takes place over its entire surface through the formation of a monolayer. It is worth mentioning that agro-industrial residues, such as fruit peels, are composed of a certain number of bioactive compounds which, in addition to their adsorption capacity in vitro, reduce the effects of mycotoxicosis in vivo (Aguilar et al., 2021).

4. Lignin and micronized fibers

Lignin is the main component of the woody structure or xylem of most terrestrial plants. Its use in mycotoxin adsorption has been reported in only a few studies, but the literature suggests that its application may be promising. An in vivo study using a lignin-based diet found that it could mitigate the adverse effects of DON and ZEN in broiler chickens (Grešáková, 2012). Lignin has also been reported to reduce the negative effects of T-2 toxin, but no in vivo models have been found where it reduces the harmful effects of aflatoxins. Thus, lignin has functional groups (OH) and a capillary pore structure associated with different molecules (Vázquez, 2022). Micronized fibers are composed of cellulose, hemicellulose and lignin. Their effective role as mycotoxin binders has also been described. It has been reported that micronized wheat fiber has the ability to reduce ochratoxin A levels in the plasma, kidney and liver of pigs (Aoudia, 2009).

5. Aloe Vera

Aloe Vera is a drought-resistant plant and belongs to the Liliaceae family. This plant has been used for medicinal purposes for many years, and the most representative is the gel extracted from the pulp of its leaves. The gel is composed of numerous phytochemical compounds, including vitamins, enzymes, minerals, phenols and polysaccharides. The gel exhibits germicidal properties (bactericidal, virucidal and fungicidal) and also functions as an adsorbent against organic and inorganic pollutants. Few studies have described its use on mycotoxins, however, one study using gel from mature leaves of A. barbadensis found it to be effective in removing AFB1 in laboratory conditions simulating poultry gastrointestinal tract conditions. According to the literature, Aloe Vera reduces the bioavailability of AFB1 in the gut by 69% (Vázquez, 2022).

6. Horticulture

Since some biosorbents are ineffective in capturing mycotoxins, in vitro studies with lettuce and horsetail (Equisetum arvense L.; Ramirez, 2021) residues had been proposed. Residues from these plants were used for aflatoxin removal and AFB1 was found to adsorb perfectly to both biomaterials, in proportions of 70-100%. In addition, the interaction power of these residues with AFB1 is based on the functional groups present in these biosorbents, as well as the formation of AFB1-chlorophyll complexes. Other mechanisms involved in this binding are non-electrostatic interactions (hydrophobic, dipole-dipole and hydrogen bridge interactions) and electrostatic one (ionic attractions; Vázquez, 2022). Although the actions and mechanisms provided by horticultural residues are known, the affinity and efficacy of these biosorbents still need to be assessed in vivo (Ramales et al., 2016).

7. Other agro-industrial waste products

The adsorption potential of fruit and vegetable seeds has also been reported. These residues contain significant amounts of essential nutrients, phytochemical and phenolic compounds, fibers and also antioxidants. Pomegranate and grape seeds are some of the main examples, being able to remove up to 51 and 86% of ZEN and AFB1; including demonstrating some capacity to adsorb OTA and FB (Aguilar, 2021).

Adsorption of mycotoxins based on modified agro-industrial wastes

The biosorption capacity of the residues can be modified or enhanced. For example, if biosorption takes place on the surface, the modification can improve the affinity of the sorbent for a particular element. This modification can be physical or chemical. The physical form includes thermal drying process, steam cutting or grinding. On the other hand, chemical modification can change the surface characteristics of the biomaterial, exposing binding sites, modifying the surface charge, or both. Many agro-industrial wastes are composed of biological polymers such as cellulose, lignin and hemicellulose, rich in hydroxyl groups and phenols that can be chemically modified to produce agents with different adsorption capacity. For this purpose, the chemical agents used are: centrinomium bromide, sulphuric acid and hydrochloric acid. Although the purpose of modifying the surface of agro-industrial residues is to improve the adsorption capacity, in several cases chemical modifications have not been favorable, especially for the AFB1 adsorption process (e.g. treatment of peach peels and cherry pits with hydrochloric acid). However, in order to modify the residues to improve the adsorption capacity, it is necessary to determine the appropriate components and the methodology to be used in the modification process (Aguilar, 2021).

Factors influencing adsorption of biosorbents
1. Adsorbent properties

Agro-industrial wastes have an adsorption potential that is determined by their chemical, morphological and structural characteristics. Residual surface has, and these interactions define the adsorption power. According to the structure and morphology of the surface, this can vary based on the physical or chemical conditions presented to it. For example, the drying method can affect the biosorption area (Aguilar, 2021).

2. Biosorbent size

The ability to bind mycotoxins is influenced by the change in particle size of the biosorbent. Micronisation of the waste biomass increases the adsorption capacity. However, the use of very fine particles in feed limits its use in animals as it leads to the development of other problems such as gastric ulcers (Aguilar, 2021).

3. Adsorbent dosage

According to reports of AFB1, ZEN and OTA adsorption, increasing the biosorbent or residue dose enhances mycotoxin adsorption, which is due to increased toxin adsorption sites (Aguilar, 2021).

4. pH role

Environmental pH is a key factor that directly impairs the mycotoxin adsorption. The pH parameter modifies the charge distribution on the adsorbent surface, thus affecting the equilibrium and kinetic reactions of the adsorption process. As a consequence of the frequent pH changes that occur throughout the gastrointestinal tract of animals and humans, the biosorbent must be effective in retaining mycotoxins in several compartments during the transit of the food. Due to pH characteristics or conditions, as well as contact time, the gut is the site where most mycotoxin adsorption occurs (Aguilar, 2021).

5. Time exposure

Toxin adsorption increases with the exposure time. However, the rapid and balanced adsorption of mycotoxins shown by agro-industrial residues indicates the potential of using this matrix to reduce the bioavailability of toxins in the gastrointestinal tract (Aguilar, 2021). A study conducted on banana peel found that the adsorption process occurred in less than 10 minutes, with maximum adsorption occurring in 15-30 minutes, however, there was no change in adsorption after 30 minutes of interaction (Shar, 2016).

In conclusion, the use of agro-industrial residues as natural adsorbents shows promising results in the control of mycotoxins in animal production. However, it is important to consider factors that may influence the adsorption capacity, such as particle size, dosage, pH and contact time. Furthermore, the adsorption capacity of these materials can be improved by physical or chemical processes, offering potential solutions to mitigate the harmful effects of mycotoxins.