A review of the role of mycotoxin adsorbing agents for aquafeed decontamination

Insights

Mursal Abdulkadir Hersi1, Dogukan Kaya2 and Ercument Genc1* 1Department of Fisheries and Aquaculture Engineering, Faculty of Agriculture, Ankara University, Ankara, Turkey

Applications and Research Center, Tokat Gaziosmanpasa University, Tokat, Turkey Corresponding author: egenc@ankara.edu.tr

In the first part of this article, we reviewed the main effects associated with mycotoxin exposure in aquatic species. In the second part of this article, the various mycotoxin adsorbing agents and feed additives used in aquaculture and their efficacy are reviewed and discussed.

Mycotoxin adsorbing agents and detoxifying feed additives

The main goal of aquaculture and other food and feed production industries is to prevent mycotoxin occurrence. However, the formation of mycotoxins is sometimes inevitable due to many environmental factors and microbial interactions.

In such cases, substances, compounds, or microbes can:

Remove mycotoxins by excretion from the body of exposed animals.

Minimize their adsorption by the animal

Mitigate their effects

(Vila-Donat et al., 2018)

Nevertheless, applying such substances does not necessarily mean that animals should be fed with feed containing mycotoxins over the maximum allowable doses.

Currently, three basic methods (chemical, physical and biological) can be used to detoxify mycotoxins, all of which have undergone substantial research studies (Karlovsky et al., 2016; Zhou et al., 2018).

CHEMICAL METHODS

Chemical approaches imply the application of different chemical compounds such as oxidizing substances, alkalis, and acids to destroy mycotoxins (Čolović et al., 2019).

However, the use of chemicals is associated with severe health effects. For example:

Chlorine dioxide used to purify mycotoxin-contaminated feed has been reported to deteriorate both the taste and texture of diets.

Ozone, which can also destroy most mycotoxins, is unsafe for animals and humans.

Sodium hypochlorite, which is been reported to disinfect trichothecenes, has detrimental consequences (Yuet al.,2020).

Therefore, applying chemicals to detoxify mycotoxins is not recommended (Conte et al., 2020).

PHYSICAL METHODS

Physical methods include detoxifying mycotoxins through adsorptio (Yu et al., 2020). After ingestion and before the mycotoxin is absorbed and systematically circulated, binding or adsorbing agents bind to it so it can be easily excreted.

Mycotoxin adsorbents have different mechanisms to bind to mycotoxins such as hydrophobic interactions, dipole-dipole interactions, and electrostatic attraction or repulsion (Di Gregorio et al., 2014).

The success of these sequestering or adsorbing agents are also affected by their physical properties, such as their shape and pores, the polarity and solubility of the targeted mycotoxin, and the pH level (Kabak et al., 2006).

Although mycotoxin binders are effective methods compared to chemical mechanisms, they cannot detoxify all toxins (Battilani, 2008; Ji and Xie, 2021).

BIOLOGICAL METHODS

With biological methods, mycotoxins are not removed from the body but rather bio-transformed into less toxic compounds. This mechanism involves the use of microorganisms (bacteria, fungi, etc.) and enzymes to break down mycotoxins (Wielogórska et al., 2016).

However, there are many challenges in the application of biological methods, including:

Limited data on the mode of action of microbes during mycotoxin detoxification.

The safety of derived products after degradation.

How the process can affect the nutrient content of feeds (Conte et al., 2020)

Nevertheless, under favorable environmental conditions, the microbes involved have a higher detoxification capacity and, thus, this strategy is considered the best remedy against mycotoxins (Zychowski et al. 2013).

Mycotoxin Binders

As mentioned above, different adsorbing agents or nano-clay particles are used to remove mycotoxins from the body of the exposed animal.

Due to their importance and wide range of applications in recent years, nano-clay particles have been significantly incorporated into various fields, including aquaculture, to improve water quality parameters (Nathanail et al., 2016).

Adsorbing agents are ultrafine nanoparticles that are usually smaller than 100 nm and have the potential to provide a good surface for mycotoxin binding (Feng et al., 2009). They can be classified as synthetic adsorbents, obtained through mechanical or machine grinding, and natural adsorbents (Wagner et al., 2014).

The most common nanoparticles for mycotoxin binding are aluminosilicates (hydrated sodium calcium aluminosilicate, bentonites, zeolites, etc.) and yeast cell walls (Arana et al., 2011).

The mycotoxin removal efficiency rate of most nanoparticles or adsorbing agents is estimated to be between 20% and 80% (Nathanail et al., 2016).

However, one major drawback of mycotoxin binders is their ability to also adsorb other micronutrients in the animals’ bodies which may result in mineral deficiency (Kolosova and Stroka, 2011).

Therefore, additional micronutrients are supplemented to the feed to adjust for such problems, usually around 20% higher than average (Brown et al., 2014).

Aluminosilicates

Representing the most abundant rock-forming minerals, aluminosilicates characterize the silicon-oxygen tetrahedron bonded together by octahedral aluminum sheets (Tapia-Salazar et al. 2010) Sheet silicates (phyllosilicates) and tectosilicates are the two major groups of aluminosilicates.

Among the most common adsorbents in the phyllosilicates group are bentonites, kaolinites, smectites, and montmorillonites, while zeolites are the most widely used sequestering agents in the tectosilicates group (Di Gregorio et al., 2014).

BENTONITES

Bentonites, also known as montmorillonites, are a group of sheet silicate clay particles that are efficient in mycotoxin adsorptions (Kolosova and Stroka, 2011).

The binding capacity of bentonites is associated with the presence and content of smectite minerals (montmorillonite), the primary raw material used in producing nano-clay particles (Benvindo da Luz and Lins, 2008).

All these mycotoxin binders deliver a large surface area for binding mycotoxins and are affected by their size, porous, shape, and selectivity (Huwig et al., 2001).

Bentonites are cosmopolitan minerals and are usually incorporated into most commercially available aquafeeds to improve water quality indices (Hussain, 2018).

In recent years, many studies have been conducted to investigate the role of bentonite on mycotoxin detoxification in aquaculture.

A survey by Neeratanaphan y Tengjaroenkul (2018) evaluated the efficacy of 1% sodium bentonite in improving the growth and tissue histomorphology of Nile tilapia fed with diets containing 10-40 mg/kg of AFB1

Pathological examinations of the groups fed with diets containing aflatoxin without bentonite supplementation showed significantly decreased growth rate, lesions in the gills, leukocyte infiltration, vascular dilation, degeneration, and lack of integrity in the liver.

However, this study detected improvements in growth performance and tissue histomorphology when 1% sodium bentonite was supplemented with tilapia feeds.

Similar results were reported by Hussain et al. (2017b) when the amelioration effect of 0.5% calcium bentonite clay against growth retardation caused by 2 and 4 mg/ kg of aflatoxins was examined.

Before the supplementation of bentonite, the animals experienced significant growth reductions and poor feed utilization. Still, considerable growth and feed efficiency improvements were noted when feed containing adsorbent was fed to animals.

Bentonites are mainly used for aflatoxin detoxification.

Another experiment by Hussain et al. (2017a) examined how 0.5% and 10% of calcium bentonite ameliorate an inferior growth performance induced by 4 mg/kg AFB1. The results of this study depicted significantly improved growth rates of Nile tilapia.

Kannewischer (2006) emphasized that the application of bentonites in aquaculture has a promising result and, therefore, should be used for detoxification.

HYDRATED SODIUM CALCIUM ALUMINOSILICATE

Hydrated sodium calcium aluminosilicate is another potent adsorbent of mycotoxins in general, particularly aflatoxins (Di Gregorio et al., 2014).

The agent, generally used as an anti-caking agent, has also demonstrated its importance in mycotoxin binding and removal from the body.

Huwig et al. (2001) discussed the efficacy of different mycotoxin binders, including zeolites, bentonites, yeast cell walls, and hydrated sodium calcium aluminosilicate.

They concluded that hydrated sodium calcium aluminosilicate had the highest mycotoxin removal capacity.

Fadl et al. (2020) evaluated the amelioration effects of dietary hydrated sodium aluminum silicates (0.2-0.5g) against the toxicity of ochratoxin A (1 mg/kg) on Nile tilapia growth, serum biochemical and tissue histopathology for six weeks.

The results showed that the supplementation of hydrated sodium aluminium silicates protected from abnormal histopathological effects, maintained stable growth performance, and promoted healthy biochemical parameters.

Likewise, El-Alim et al. (2017) also tested the efficacy of 0.5% hydrated sodium aluminum silicate supplementation against toxicity induced by 2.5 mg/kg of aflatoxins on Nile tilapia for six weeks.

Anemia, leukopenia, lymphopenia, decreased phagocytic index, and a mortality rate of more than 16% in the groups fed diets containing aflatoxin alone were detected.

However, improvement in growth and biochemical parameters was reported in groups fed diets containing both aflatoxin and hydrated sodium aluminium silicate.

ZEOLITES

Zeolites are microporous tectosilicate crystalline aluminosilicates used extensively in aquaculture in recent years.

Due to their outstanding physical and chemical properties, including adsorption and ion exchange, various industries have applied zeolites for different purposes (Ghasemi et al., 2018).

In aquaculture, zeolites are used for multiple purposes, such as:

Maintaining water quality and removing ammonia (Shaban et al., 2017).

Improving feed utilization (Sava et al., 2019).

Adsorbing mycotoxins (Daković et al., 2015).

However, during this study, most of these pathological results were reduced by adding 5-10 g/kg nano-zeolite particles to tilapia feed.

Different authors have reported similar results using other fish species such as Nile tilapia (Zahran et al., 2020) and rainbow trout (Alinezhad et al., 2020)

A three-month experiment carried out by Hassaan et al. (2020) revealed that aflatoxins at a dose of 3 mg/kg caused a significant decrease in feed use, growth rate, digestion, and antioxidant enzymes and increased liver enzymes, as well as aggravated DNA and left residue in the body of Nile tilapia.

ACTIVATED CHARCOAL

Activated charcoal is a substance produced after biomass undergoes a process called pyrolysis. The agent is highly porous and is one of the most efficient mycotoxin adsorbents mainly used in the livestock industry (Avantaggiato et al., 2005). In addition to binding mycotoxins, in aquaculture, activated charcoal is used for different purposes, such as water purification and improving fish welfare (Selim et al., 2013)

The capacity of activated charcoal to bind or sequester mycotoxins is affected by its size, shape, porosity, and structure. Like other adsorbents, activated charcoal tends to attach to other micronutrients in the body, especially when they are higher in presence than mycotoxins, hence should be addressed (Vekiru et al., 2007).

Selim et al. (2013) revealed that aflatoxins significantly damage growth and blood biochemistry parameters of Nile tilapia, but the addition of activated charcoal to the feed results in improvements in haematological and growth performance indices.

Many studies have shown the positive effect of activated charcoal in mitigating mycotoxins, especially vomitoxin (Diaz and Smith, 2005).

Microorganisms and other feed additives

MICROBES

In addition to the application of mineral-binding materials for mycotoxins, microorganisms that adsorb or decompose the toxic substances are also applied

MYCOTOXIN ADSORPTION

For adsorption, various microbes have a unique cell wall structure that can bind with different mycotoxins through different interactions such as hydrogen bonds and ionic and hydrophobic bonding (Haskard et al., 2001

This is achieved before mycotoxin interaction with the body and significantly reduces mycotoxin bioavailability (Kolosova and Stroka, 2011)

The most commonly used microbes for this purpose are Saccharomyces cerevisiae and lactic acid bacteria.

SACCHAROMYCES CEREVISIAE

S. cerevisiae has a variety of applications in both the food and feed industry and has long been used in fermentation processes (Taheur et al., 2017).

Authors have reported that S. cerevisiae adsorbs and removes different mycotoxins (Zearalenone, Ochratoxin A, and Fumonisins) from the bodies of animals (Fruhauf et al., 2012; Taheur et al., 2017).

LACTIC ACID BACTERIA

Lactic acid bacteria are gram-positive bacterial groups commonly found in dairy products and decaying plant biomass.

Previously, different species of this group, such as Lactobacillus rhamnosus, have shown a strong ability to sequester mycotoxins, particularly aflatoxins and Zearalenone (Rahaie et al., 2012).

During this degradation process, different microbes that produce various enzymes are utilized.

Some of those enzymes are:

Aflatoxin oxidase produced by Armillariella tabescens (Cao et al., 2011).

Peroxidase produced by Pseudomonas species (Zaid, 2017).

Reductase produced by Mycobacterium smegmatis (Li et al., 2019).

MYCOTOXIN DETOXIFICATION

Microorganisms may also, at some point in their life cycle, secrete chemicals that can either:

Alter the structure of mycotoxins and produce less toxic compounds.

Destroy the mycotoxins.

Probiotic microorganisms should be the first choice during the application of microbes for mycotoxin detoxification (Guan et al., 2021). Including probiotics not only accelerates mycotoxin detoxification but also mitigates the negative effects of these toxins (Fang et al., 2020).

Probiotics are also known to improve both zootechnical and biochemical indices of aquatic animals.

A recent study by Sadeghi et al., (2020) tested the amelioration effect of probiotic bacteria L. rhamnosus against aflatoxicosis in rainbow trout for 4 weeks.

At the end of the experiment, the groups fed diets containing aflatoxins showed a considerable increase in cortisol, alkaline phosphate enzyme, blood glucose, and mortality as well as significant reductions in chymotrypsin enzyme of the digestive system. However, upon inclusion of L. rhamnosus, amelioration effects in growth, survival, and enzyme balance were found.

Similarly, a more recent study by Khalafalla et al. (2022) examined the effect of 106 CFU/mL per kg diet of probiotic bacteria Lactobacillus acidophilus against aflatoxicosis induced by 0.5-1 mg/kg aflatoxins on the growth, blood biochemistry and histopathology of grey mullet (Liza ramada) for 8 weeks.

Significant reductions in growth rates, leukocytes, erythrocytes, haemoglobin, hematocrit, total protein and albumin in the blood, and cholesterol, as well as a considerable increase in liver enzymes, blood glucose, and cortisol, were reported from the groups fed only aflatoxin-containing feeds. Tissue histomorphology in aflatoxin groups also showed significant damage.

Groups supplemented with L.acidophilus and aflatoxins showed notable improvements in growth, blood biochemistry, antioxidant enzymes such as catalase and superoxide dismutase, and liver and intestinal histopathology.

Another trial by Fang et al. (2020) also revealed that the probiotic bacteria Lactiplantibacillus pentosus improved aflatoxin-induced growth retardation, immunosuppression, and damage to the gut microbiota, and tissue histomorphology of pacific white shrimp.

To accelerate the detoxification process of mycotoxins in aquaculture a combination of microorganisms (probiotics preferably), degrading enzymes, and/or adsorbing agents can also be implemented (Guan et al., 2021).

Huang et al. (2018b) found that applying a combination of Bacillus subtilis, Lactobacillus casei, and degrading enzyme produced by Aspergillus oryzae significantly accelerated the mycotoxin detoxification process.

Plant-based feed additives against mycotoxicosis

Among the different strategies used to deal with the challenges of mycotoxins in aquaculture is the concept of plant-based feed additives.

Plants display a variety of essential oils, spices, herbs, and other extracted products that can play a noble role in mitigating the health effects caused by mycotoxins (Gowda et al., 2013).

They are considered eco-friendly, available, and affordable products to tackle not only mycotoxins but also many other problems in the feed and food industries (Iram et al., 2016).

In recent years, the plant-derived compounds, coumarins and flavonoids have been found to inhibit the carcinogenic effect of aflatoxins (Lee et al., 2001).

Curcumin, the bioactive ingredient of turmeric, has also been reported to have a curative effect against aflatoxicosis (Ferreira et al., 2013).

A study conducted by Vijayanandraj et al. (2014) examined the degradation capacity of various plant extracts and concluded that they also showed the highest aflatoxin degradation rate (about 98%).

It has also been reported that oil extracted from Chenopodium ambrosioides is an inhibitor of both aflatoxin and Fusarium mycotoxins (Sandosskumar et al., 2007).

Abdelhiee et al. (2020) conducted a four-week study to examine how 0.5-1% of Moringa oleifera mitigates the adverse impacts induced by 1 mg/ kg of AFB1 on the growth, immune response, blood biochemical, and haematological indices of Nile tilapia.

Necroscopic examinations of the groups fed with diets with aflatoxins but without moringa resulted in inferior growth performance (weight gain, specific growth rate, etc.), serum biochemistry (red and white blood cells, haemoglobin, hematocrit, and albumin), antioxidant enzymes (superoxide dismutase and catalase), as well as significant increase in liver enzymes.

In the histopathological examination of the groups fed with aflatoxincontaining feeds, vascular dilation, congestion, and necrotic liver, as well as lack of integrity in the intestines and lesions in the gills, were detected. In addition, when Moringa oleifera was supplemented with the diets of this experiment, significant improvements in growth, serum biochemical indices, tissue histomorphology, gene expression, and immune system were obtained.

Table 1 summarizes recent studies on applying physical, biological, and microbial strategies to mitigate the adverse effects induced by mycotoxicosis on a variety of aquatic animals.

Table 1. Studies on the application of physical, biological, and microbial strategies to mitigate the adverse effects induced by mycotoxicosis in aquaculture.

Species Mycotoxin and its concentration

Mycotoxin detoxification agent and its concentration Duration

Nile tilapia AFB1 (10-40 mg/kg) Thai sodium bentonite (1%) 16 weeks

Nile tilapia AFB1 (2-4 mg/ kg) Calcium bentonite clay (0.5 and 10%) 10 weeks

Nile tilapia OTA (1 mg/kg) Hydrated sodium aluminium silicates (0.2-0.5 g/kg) 6 weeks

Amelioration effect of used mycotoxin detoxification substance(s) Reference

Improvements in growth performance and tissue histomorphology (gills, liver, and intestine).

Neeratanaphanand Tengjaroenkul(2018)

Significantly improved growth rates. Hussain et al. (2017a)

Protection from abnormal histopathological effects, maintaining stable growth performance, and promotion of healthy biochemical parameters. Fadl et al. (2020)

Nile tilapia AFB2 (2.5 mg/ kg) Hydrated sodium aluminium silicate (0.5%) 42 days Reduced mortality rate of 16%, enhanced growth performance, and serum biochemistry indices. El-Alim et al. (2017)

Nile tilapia AFB1 (3 mg/kg) Nano-zeolite particles (5-10 g/kg) 12 weeks Increased feed utilization, growth, digestion, and antioxidant enzymes, as well as increased liver enzymes.

Hassaan et al. (2020)

Rainbow trout AFB1 (5 mg/kg) Nano-zeolite particles (0.5- 1%)56 days Increased serum protein, albumin, and globulin levels, as well as improved tissue histomorphology. Alinezhad et al. (2020)

Nile tilapia AFB1 (0.2 mg/ kg) 0.25% of each: S. cerevisiae, hydrated sodium calcium aluminosilicates, and

In vitro (experimental) DON (100.2 mg/L) and AFB1 (2 mg/L)

10 semanas Mejora notable del crecimiento, de los parámetros bioquímicos del suero y de la respuesta inmunitaria, así como de la disminución de los residuos de AFB1 en la musculatura de los peces.

Selim et al. (2013)

Activated charcoal, bentonite clays, cellulose products, yeast cell wall product Not Specified Prevention of mycotoxin formation in aquafeed. Kongetal.(2014)

In vitro (experimental) ZEN (0.02mg/L) Bacillus subtilis and Bacillus natto –Not specified 24 hours Degradation of approximately 80-100% of ZEN, respectively. Tinyiroetal.(2011)

European seabass ZEN (0.76 mg/ kg) Dietary garlic (30 g/kg) and chitosan (10 g/kg) 28 daysSignificant improvement of red and white blood cells means, as well as corpuscular haemoglobin, haemoglobin, serum total protein, albumin, globulin, lysozyme, and resistance against mortality induced by ZEN and Vibrio alginolyticus.

European seabass ZEN (0.76 mg/ kg) Dietary garlic (30 g/kg) and chitosan (10 g/kg) 28 days

Rainbow trout AFB1 (Not specified)

L. rhamnosus- Not specified 4 weeks

Grey mullet AFB1 (0.5-1 mg/kg) L. acidophilus (106 CFU/mL) 8 weeks

Pacific white shrimp AFB1 (0.5 mg/ kg)

Lactiplantibacillus pentosus (5 × 108 CFU/g) 6 weeks

Nile tilapia AFB1 (1 mg/kg) Moringa oleifera (0.5-1%) 4 weeks

Amelioratedoxidativestress(lowersuperoxide dismutase,catalase,andglutathioneperoxidase activitiesandhighermalondialdehyde), immunosuppression,andhistopathologicallesions inducedbyZEN.

Improvement in cortisol, alkaline phosphate enzyme, blood glucose, and growth. Reduction in mortality and chymotrypsin enzyme.

Markedly improved serum biochemistry parameters, liver enzymes oxidative stress and ameliorated histopathological lesions in the liver and intestines.

Improved aflatoxin-induced growth retardation, immunosuppression and damage to the gut microbiota, and tissue histomorphology.

Improved growth, serum biochemistry indices, antioxidant and liver enzymes.

Abdel-Tawwab et al. (2020)

Abdel-Tawwab et al. (2021)

Sadeghietal.(2020)

Khalafallaetal.(2022)

Abdelhiee et al. (2020)

Fangetal.(202)

Conclusions

Numerous mechanisms have been introduced to remove or reduce mycotoxins in aquaculture before or after the animals are exposed to them

Chemical approaches entail the application of chemical compounds such as ozone, sodium hydroxide, ammonia, and different acids, which are mainly used to prevent mycotoxin formation in feed.

Although chemical methods are effective in combating mycotoxins, they result in harmful effects since they leave residues and adversely affect the test and appearance of the meals.

Physical approaches involve mycotoxins with various methods like cleaning, UV lights, sorting, and sequestering or adsorbing agents. The latter, in particular, has become a magnet for many studies, and its effectiveness has been demonstrated.

Nevertheless, one major drawback of the physical approach is the poor adsorption capacity. Thus, combining different mineral adsorbing agents might be beneficial, but future research investigating this is necessary.

The microbiological approach is associated with implementing commensal bacteria, fungi, the enzymes they produce, and plant-based feed additives.

Plant-based feed additives are also highly recommended as they contain essential oils, herbs, spices, and other vital extracts that are effective to some extent in combating mycotoxins.

Microbes are inexpensive, eco-friendly, and most importantly, very efficient at degrading or adsorbing mycotoxins. However, compounds produced when mycotoxins are degraded may not be safe, and little is known about how such products may affect animals, a concern of the microbiological approach.

For this reason, studies aiming to discover the methods, dosage, time length of microbiological detoxification, and the safety of microbe-produced products are deemed necessary.

Future studies should also focus on the synergistic effects of methods from different approaches, such as physical (mineral adsorbing agents) and microbiological (microbes, enzymes, or plant-derived feed additives) on mycotoxin removal in aquaculture.

Most of the existing literature on mycotoxins is associated with aflatoxins, apparently because of their frequency of incidence. Still, other classes of mycotoxins in aquaculture are misrepresented in the literature. Therefore, future studies should explore different types of mycotoxins, their formation, effects, and mitigation strategies.

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