Food and Chemical Toxicology 148 (2021) 111976

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Food and Chemical Toxicology

journal homepage: www.elsevier.com/locate/foodchemtox

Review

Application of new technologies in decontamination of mycotoxins in

cereal grains: Challenges, and perspectives
Shabir Ahmad Mir a, B.N. Dar b, Manzoor Ahmad Shah c, Sajad Ahmad Sofi b,
Afshan Mumtaz Hamdani a, Carlos A.F. Oliveira d, Motahareh Hashemi Moosavi e, Amin Mousavi
Khaneghah f, **, Anderson S. Sant’Ana f, *
a
Department of Food Science & Technology, Government College for Women, M. A. Road, Srinagar, Jammu & Kashmir, India
b
Department of Food Technology, Islamic University of Science & Technology, Awantipora, Jammu & Kashmir, India
c
Department of Food Science & Technology, Government PG College for Women, Gandhi Nagar, Jammu, Jammu & Kashmir, India
d
Department of Food Engineering, Faculty of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil
e
Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences and Food Technology, Shahid
Beheshti University of Medical Sciences, Tehran, Iran
f
Department of Food Science and Nutrition, Faculty of Food Engineering, University of Campinas, Campinas, São Paulo, Brazil

A R T I C L E I N F O A B S T R A C T

Handling editor: Dr. Jose Luis Domingo Emerging decontamination technologies have been attracted considerable attention to address the consumers’
demand for high quality and safe food products. As one of the important foods in the human diet, cereals are
Keywords: usually stored for long periods, resulting in an increased risk of contamination by different hazards. Mycotoxins
Aflatoxins comprise one of the significant contaminants of cereals that lead to enormous economic losses to the industry and
Contamination
threats to human health. While prevention is the primary approach towards reducing human exposure to my­
Cold plasma
cotoxins, decontamination methods have also been developed as complementary measures. However, some
Fumonisins
Irradiation conventional methods (chemical treatments) do not fulfill industries’ expectations due to limitations like safety,
Ozone efficiency, and the destruction of food quality attributes. In this regard, novel techniques have been proposed to
Ochratoxin a food to comply with the industry’s demand and overcome conventional methods’ limitations. Novel techniques
Pulsed light have different efficiencies for removing or reducing mycotoxins depending on processing conditions, type of
Storage mycotoxin, and the food matrix. Therefore, this review provides an overview of novel mycotoxin decontami­
Trichothecenes nation technologies such as cold plasma, irradiation, and pulse light, which can be efficient for reducing my­
Zearalenone cotoxins with minimum adverse effects on the quality and nutritional properties of produce.

1. Introduction
Cereal grains occupy a vital segment in human nutrition and are
among the most crucial food commodities worldwide. Cereal grains can
be contaminated frequently by different microorganisms during har­
vesting, transportation, storage, or distribution (Fig. 1) (Hell et al., 2011;
Agriopoulou et al., 2020). Mycotoxin production frequently occurs in
hot and humid climatic conditions, which are the among the most
important factors that favour mould growth (Gebremeskel et al., 2019).
Cereal foods contamination by mycotoxigenic fungi could result in
lower quality products and potentially harmful for consumption (Neme
and Mohammed, 2017; Khaneghah et al., 2018a; El Sheikha, 2019;
Ayelign and Saeger, 2020). For this reasons, regulations for mycotoxins
in foodstuffs have been adopted worldwide. In this regard, the average
tolerable limits of common mycotoxins in cereals are 4 μg/kg of total
aflatoxins, 2 μg/kg of fumonisins, 5 μg/kg of ochratoxin A, and 750
μg/kg of deoxynivalenol (Gebremeskel et al., 2019).
Mycotoxins are the toxic secondary products of fungi that contami­
nate food commodities (Coppa et al., 2019; Vasseghian et al., 2020).
Mycotoxins show harmful effects even at low concentrations and may
present a broad spectrum of toxicity (Martins et al., 2018). Mycotoxins
can pose a severe threat to human health because of some of them
present carcinogenic, mutagenic, and genotoxic activities (Shephard,
2008; Zain et al., 2011). Once mycotoxins have been produced, their

* Corresponding author.
** Corresponding author.
E-mail addresses: mousavi@unicamp.br (A. Mousavi Khaneghah), and@unicamp.br (A.S. Sant’Ana).

https://doi.org/10.1016/j.fct.2021.111976
Received 25 October 2020; Received in revised form 27 December 2020; Accepted 31 December 2020
Available online 8 January 2021
0278-6915/© 2021 Elsevier Ltd. This article is made available under the Elsevier license (http://www.elsevier.com/open-access/userlicense/1.0/).
S.A. Mir et al.
degradation is hard to be achieved due to their physical and chemical
stabilities (Thanushree et al., 2019; Vasseghian et al., 2020). Therefore,
in addition to the public health impact, mycotoxin contamination of
cereal grains may result in significant economic losses (Khaneghah et al.,
2018b).
Different strategies like appropriate grain handling after harvest and
proper storage practices are key in managing mycotoxins’ production
(Khaneghah et al., 2018b, 2018c). However, these practices will not be
effective once the mycotoxins were formed. Several mycotoxin decon­
tamination strategies have been evaluated throughout the years (Sar­
rocco and Vannacci, 2018; Neme and Mohammed, 2017; Shanakhat
et al., 2018; Javanmardi et al., 2020; Khaneghah et al., 2020a,b). Most
of the approaches tested for mycotoxin degradation were based on
conventional techniques such as thermal treatments, which have not
successfully destroyed these contaminants while maintaining their
properties (Grenier et al., 2014; Pankaj et al., 2018; Mokhtarian et al.,
2020). Given this, novel techniques to decontaminate cereal grains have
been demanded. While these methods should never replace preventive
measures to avoid fungal contamination/growth and mycotoxin pro­
duction, their development can be integrated strategies to reduce con­
sumers’ exposure to mycotoxins.
Novel techniques like cold plasma (Dasan et al., 2016; Mir et al.,
2016; Wielogorska et al., 2019), irradiation (Aziz et al., 2007; Shah
et al., 2014), ozone processing (Tiwari et al., 2010; Savi et al., 2014),
biological methods (Ji et al., 2016; Zhou et al., 2017; Ismail et al., 2018)
are exploited for degradation of mycotoxins in the food industry (Fig. 2).
These novel technologies potentially result in less adverse effects on the
nutritional properties, quality attributes, and sensory characteristics of
grains (Roohi et al., 2020) (Table 1). These technologies have consid­
erable scope for use in the grain industry for the decontamination of
mycotoxins. Therefore, this review provides an overview of the novel
mycotoxin decontamination technologies, the range of efficiency for
reducing mycotoxins potentially present in cereal grains.
2. Main mycotoxins in cereal grains
Once mycotoxins contaminate cereal grains in the field or during
storage, they will likely be found on the consumer’s plate (Luo et al.,
2018). The commonly detected and worldwide controlled mycotoxins in
cereal grains are the aflatoxins, ochratoxins, fumonisins, zearalenone,
and deoxynivalenol ingestion can lead to acute or chronic effects in
consumers (Ostry et al., 2017).
Fig. 1. Factors influencing the growth of toxigenic fungi and the occurrence of mycotoxins in the supply chain of cereal grains.
2
Food and Chemical Toxicology 148 (2021) 111976
2.1. Aflatoxin
Aflatoxins are highly toxic mycotoxins released mostly by Aspergillus
flavus and A. parasiticus (Campagnollo et al., 2016). There are various
types of aflatoxin identified, including aflatoxin B1, aflatoxin B2, afla­
toxin G1, and aflatoxin G2 (Murphy et al., 2006; Udomkun et al., 2017).
Many food products are affected by aflatoxins, such as cereal grains,
spices, oilseeds, nuts, and meat. Cereal grains, including wheat, rice, and
maize, are frequently affected by the Aspergillus spp. (Khaneghah et al.,
2018a; Jedidi et al., 2018; Rushing et al., 2019). The occurrence of af­
latoxins in the grain is mainly due to the high moisture content at har­
vest time, inappropriate drying, and grain storage (Bumbangi et al.,
2016). Aflatoxins are carcinogenic, teratogenic, and mutagenic (Richard
2007; Ismail et al., 2018).
2.2. Ochratoxin
Ochratoxin is produced mainly by Aspergillus and Penicillium species,
notably A. ochraceus and P. verrucosum (Perrone et al., 2017;
Sánchez-Montero et al., 2019). In grains, this type of contamination
mainly occurs during postharvest storage (Majeed et al., 2018; Khane­
ghah et al., 2019a,b). The growth of toxigenic fungi and mycotoxins’
production, like ochratoxins, is influenced by the grains’ moisture
content and storage temperature, among other factors (Bayman, 2006).
Ochratoxin occurs in different types of foods, mainly in maize and
wheat, also occurring in dried fruits and grapes (Zhihong et al., 2015:
Majeed et al., 2018; Heshmati et al., 2020). Ochratoxin A is the most
toxic among the ochratoxin family produced by Aspergillus spp. and
Penicillium spp. (Ciconova et al., 2010). Ochratoxin A primarily damages
the kidney and liver due to its toxicity. It is nephrotoxic, teratogenic, and
carcinogenic for human health (Clark and Snedeker, 2006).
2.3. Fumonisin
Fusarium, especially F. verticillioides, produces this type of mycotoxin
(Chen et al., 2018).). Fumonisin has been characterized as A, B, C, and P.
Among fumonisin B, FB1, FB2, and FB3 are the most abundant, with FB1
being the most toxic fumonisin (Kamle et al., 2019). Maize is one of the
common grains associated with the contamination with this type of
mycotoxin (Fandohan et al., 2005; Atukwase et al., 2009). Fumonisins
sometimes occur in rice, wheat, barley, and sorghum (Cendoya et al.,
2018). High temperature and damage by insects mainly lead to
S.A. Mir et al. Food and Chemical Toxicology 148 (2021) 111976

Fig. 2. Conventional and novel techniques for mycotoxin decontamination.

2.5. Deoxynivalenol
Table 1
Pros and cons of decontamination technologies.
Deoxynivalenol, also known as vomitoxin, is commonly produced by
Decontamination Cons Pros F. culmorum and F. graminearum in the field and/or postharvest storage
technology
(Shah et al., 2018). Deoxynivalenol is abundantly observed in wheat,
Cold Plasma Up-scaling challenges No chemical residue maize, barley, rice, oats, and rye (Richard, 2007; Neme and Mohammed,
Poor penetration of active Non-thermal nature 2017; Khaneghah et al., 2018b). Deoxynivalenol production usually
components Retention of quality
properties of food
occurs due to wet weather and high moisture level at harvest time
material (Wegulo, 2012). Deoxynivalenol is found to affect gut morphology
Irradiation Lipid and vitamin oxidation, Effectively destroy (Pestka, 2010) and is found to induce headaches, diarrhea, nausea,
Formation of off-flavor mycotoxins abdominal pain, and fever (Sobrova et al., 2010).
Color changes of food products Non-thermal nature
High capital cost
Ozone Efficiency depends on the grain No toxic residues 2.6. Techniques for mycotoxins decontamination in grains
properties and moisture Environmental
Oxidation of lipids, degradation friendly
of some vitamins and phenolic Minimally affect the
The fungal growth, which leads to the formation of mycotoxins,
compounds quality properties of cannot be avoided entirely. Therefore, many techniques have been
Leads to the changes in color grains developed to reduce mycotoxin levels (Milani et al., 2014; Kaushik,
Pulse Light Only surface decontamination Cost-effective 2015). The first approach that should be applied to control the myco­
Treatment efficiency depends on Nonthermal technique
toxins or fungal growth is to follow proper pre-and postharvest practices
food material properties like Does not leave any
matrix and thickness of food residues on food (Sarrocco and Vannacci, 2018). The harvested grains may be contami­
material, composition, and type material nated through handling, transport, and storage (Amirahmadi et al.,
of mycotoxin 2018). Sometimes inoculum is already present in the transport facility
Biological methods Not easy to select nontoxigenic Environmental and storage structures. Proper environmental conditions of inoculum
biocompetitive microorganisms friendly
Long time required to Leaves no toxic
lead to the rapid growth of microbe and ultimately causing grain loss
detoxification residues (Benbrook et al., 2005). Moreover, postharvest operations and grains
High-efficiency conditions are more critical, influencing the storage behavior and
Natural ingredients Strong aroma of some natural Environmental occurrence of various types of microbial contamination in grains (Neme
ingredients friendly
and Mohammed, 2017). Many unit operations with specific technical
Complicated procedures for Leaves no toxic
preparing natural ingredients residues purposes may also reduce mycotoxin levels in cereals, such as milling
and dehulling. Nonetheless, reducing mycotoxin levels is not their pri­
mary aim, technologies that reduce mycotoxins’ concentration, and
contamination by this type of fungi. The coexistence of fumonisins oc­ consequently, human exposure is demanded.
curs in the field, which depends on the agroclimatic conditions. More­
over, high moisture of grains during storage also favors the growth of
2.7. Conventional decontamination techniques
these fungi. Fumonisins usually affect the kidney, liver, pancreas,
gastrointestinal tract, and animals’ blood cells (Marasas et al., 2004;
Mycotoxin content in grains is moderately removed by cleaning and
Alizadeh et al., 2012).
milling operations. The higher mycotoxin level is usually concentrated
in the outer layer of the grain removed by milling or dehulling process
2.4. Zearalenone
(Cheli et al., 2013; Tibola et al., 2016; Khaneghah et al., 2018c). How­
ever, some percentage of mycotoxins remains with the milled grain,
Zearalenone is produced by Fusarium species, particularly by
which affects its quality. The primary practice which influences the
F. roseum and F. moniliforme (Guo et al., 2019). Usually, zearalenone
growth of mycotoxins in grains is storage management. Appropriate
producing fungi infect maize. In addition to that, other cereal crops like
storage parameters like moisture, humidity, and temperature control the
oats, barley, wheat, and rice (Sangare-Tigori et al., 2006; Marques et al.,
microbial growth and production of mycotoxins (Walker et al., 2018;
2008). Zearalenone is usually produced in the field but increases under
Guoliang et al., 2020). These procedures are applicable to prevent the
storage conditions with moisture higher than 30% (Rai et al., 2019).
growth of molds and mycotoxin formation. However, once the myco­
Literature reported that zearalenone adversely affects animals’ repro­
toxins occurred in the grains, it cannot be controlled by these strategies.
ductive functions (Bennour et al., 2009). Due to its high thermal sta­
Various chemicals such as hydrogen peroxide, citric acid, lactic acid,
bility, zearalenone, like other mycotoxins, is hard to remove entirely
propionic acid, and ozonated water are used to decontaminate food
during various processing operations (Chilaka et al., 2018).
grains (Grenier et al., 2014). Treatment with chemicals leads to the
conversion of mycotoxins into less toxic compounds. Lactic acid resulted
in the conversion of AFB1 into less toxic products identified as AFD1 via

3
S.A. Mir et al. Food and Chemical Toxicology 148 (2021) 111976

hydrolysis of the lactone ring (Jubeen et al., 2020). Different bases like Table 2
ammonia and hydrated oxide may also be used in grains to reduce Influence of gamma irradiation on mycotoxins.
mycotoxins like the aflatoxins. In addition to that, glycerol and calcium Type of Type of Dose % reduction of Reference
chloride mixture have also been exploited for reducing the level of mycotoxin grain (kGy) mycotoxins
mycotoxins. The decontamination of AFB1 by citric acid primarily leads AFB1 Maize 2 68.9 Aquino et al.
to the formation of the β-keto acid structure, catalyzed by an acidic (2005)
medium (Fig. 3). The process is followed by hydrolysis of the lactone AFB2 Maize 2 97.6 Aquino et al.
ring, which involves the formation of AFD1 derived from the decar­ (2005)
AFB1 Maize 0.5–6 74 Aziz et al.
boxylation of the lactone ring-opened form of aflatoxin B1. The AFD1 (2004)
shows lower mutagenic activity than AFB1, with a decrease in 18 fold Ochratoxin A Maize 0.5–6 51 Aziz et al.
toxicity (Méndez-Albores et al., 2005). Chemical decontamination (2004)
techniques are used in the cereal industry due to easy availability and Zearalenone Maize 0.5–6 78 Aziz et al.
(2004)
cheap source. However, some chemical decontamination techniques are
Fumonisin B1 Wheat 5 97 Aziz et al.
not permitted for grains by various world health organizations (Luo (2007)
et al., 2018). Chemicals such as organic acids also increase grain mois­ Fumonisin B1 Maize 5 87 Aziz et al.
ture content and penetrate the endosperm (Sabillon et al., 2017). (2007)
Furthermore, residual chemicals and limited effects also create problems Fumonisin B1 Barley 5 100 Aziz et al.
(2007)
for the use of these chemicals for decontamination. However, even AFB1 Wheat 8 69 Mohamed et al.
though used, these conventional methods were forced to discover and (2015)
use novel technologies for decontamination of mycotoxins from food AFB1 Rice 8 65 Mohamed et al.
grains. (2015)
AFB1 Corn 10 81 Ghanem et al.
(2008)
2.8. Novel decontamination techniques AFB1 Corn 8 60 Mohamed et al.
(2015)
The conventional techniques used for degradation of the mycotoxins
in cereal grains demanded a considerable requirement for novel tech­
may negatively affects grain’s quality properties up to some extent
nologies, which will be useful, environmentally friendly, and cost-
(Ghanem et al., 2008; Lung et al., 2015).
effective. Any novel technique used should decrease the mycotoxin
Braghini et al. (2009) demonstrated the effect of different doses of
load on cereal grains without affecting grain quality, nutritional, and
irradiation on Alternaria alternata inoculated on cereal grains. The re­
sensory characteristics. The critical novel techniques for decontamina­
sults indicated that 5 kGy is effective in controlling the growth of
tion of cereal grains are discussed as follows.
microbe. However, 10 kGy inhibited the growth of Alternaria
completely. Aziz et al. (1997) observed that an irradiation dose of 6 kGy
2.8.1. Irradiation
eliminates the fungal flora in wheat grain. In another study, Aziz et al.
Irradiation has been extensively used for the decontamination of
(2007) evaluated gamma irradiation’s influence on Fumonisin B1 in
food for centuries. However, innovative applications have been pro­
different grains like maize, wheat, and barley. The results showed that
posed using irradiation for degradation of mycotoxins involving the
irradiation doses of 5 kGy inactivated the fumonisin B1 about 100% in
exposure of food to ionizing energy (Mohamed et al., 2015). The indirect
barley, 96.6% in wheat, and 87.1% in barley grain. Another author,
effects like free radical reaction due to water and other components’
Aquino et al. (2005), observed that 10 kGy of irradiation dose eliminates
radiolysis resulted in the mycotoxin degradation by irradiation (Aquino
the presence of AFB1 and AFB2 in maize. However, Farag et al. (2004)
et al., 2005; Lung et al., 2015). Irradiation processing has been utilized
observed that gamma irradiation at a higher dose (20 kGy) eliminates
effectively for controlling the contamination of grains by toxigenic fungi
76% of AFB1 in the yellow type of maize. Authors reported in various
like Aspergillus, Fusarium, and Penicillium species (Table 2) (Aziz et al.,
studies that different doses of irradiation are sufficient to destroy my­
2007; Calado et al., 2014). Different irradiation doses are applied for a
cotoxins as per the type of grain and mycotoxin. However, the myco­
significant reduction of fungal growth from different cereal grains.
toxin percentage was found to be decreased with increasing irradiation
Irradiation treatment for food purposes is regarded as safe for dosages of
dose.
up to 10 kGy (Schmidt et al., 2018). However, the irradiation process

Fig. 3. Mechanism of detoxification of AFB1 by citric acid (Adapted from Jubeen et al., 2020).

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S.A. Mir et al. Food and Chemical Toxicology 148 (2021) 111976

Hassan and Aziz (1998) studied gamma irradiation on aflatoxins in
maize at different moisture levels. The aflatoxin production decreased
with an increase in the irradiation dose and was negligible at 4 kGy.
Mycotoxin degradation efficiency not solely depends on the dose of
gamma irradiation treatment, but the moisture level of treated samples
also plays a vital role in degradation. The effect is due to the radiolysis of
water, which produces highly reactive radicals that lead to the degra­
dation of mycotoxins (Aziz et al., 2004; Wang et al., 2011; Schmidt et al.,
2018). Similar results were observed by Mehrez et al. (2016) while
studying mycotoxins’ degradation stability. The degradation of myco­
toxins irradiated with 8 kGy at 16% moisture content was significantly
higher than the moisture content of 11%.
removes about 66% of aflatoxin B1 and Fumonisin B1 in maize grain.
During plasma treatment, the mycotoxin degradation depends on
mycotoxin’s molecular structure, nature of plasma chemistry, and
interaction of reactive species with toxins (Misra et al., 2019; Gavahian
and Cullen, 2020). The proposed degradation mechanism by
plasma-induced degradation of aflatoxin is given in Fig. 4. Literature
reported that aromatic structures observed in mycotoxins decrease the
degradation efficiency of plasma treatment. The effectiveness of plasma
processing depends on operating factors like the voltage, frequency,
exposure time, and gas composition. Moreover, the detoxifying efficacy
of cold plasma depends on the food material matrix (Wang et al., 2015;
Shi et al., 2017a,b).

2.8.2. Cold plasma 2.8.3. Ozone treatment

Cold plasma is potentially exploited in various areas in the food in­ Ozone leads to potential applications in the food industry as a
dustry. Cold plasma is one of the novel techniques widely used to disinfectant (Trombete et al., 2017; Pandiselvam et al., 2018). Ozone is a
decontaminate cereal grains (Table 3). The mycotoxin observed in food strong oxidant employed to eliminate the mycotoxins from food grains
material is degraded by reactive species such as O, O3, OH, NO, and NO2 (Table 4) (Mendez et al., 2003; Savi et al., 2020). Ozone treatment is one
generated by the cold plasma. The reactive species generated by cold of the potential alternatives for conventional decontamination tech­
plasma attack mycotoxin molecules’ chemical bonds, resulting in their niques, which leaves no toxic residues and is environmentally friendly
degradation or conversion to other products (Misra et al., 2019). This (Pandiselvam et al., 2018). However, the ozone technique’s cost is
technique offers high inactivation of mycotoxins at 5–30 ◦ C without relatively high due to the sophisticated decontamination technology
affecting the quality attributes than conventional/traditional techniques (El-Desouky et al., 2012; Greene et al., 2012; Luo et al., 2014). The
(Mir et al., 2016; Wielogorska et al., 2019). This technology showed degradation of aflatoxin by ozone begins with an electrophilic attack on
promising applications by retaining the nutritional and sensory prop­ the C8–C9 double bond of the furan, leads to the formation of primary
erties, thus maintain the quality properties of cereal grains (Mir et al., ozonides followed by rearrangement into derivates of monoxide like
2020; Mohammadi et al., 2020). However, cold plasma efficiency de­ aldehydes, ketones, and organic acids (Diao et al., 2013; Pankaj et al.,
pends on mycotoxins’ structure, grain characteristics, and surface (Luo 2018). The ozonolysis pathway aflatoxin B1 is given in Fig. 5. Ozone is
et al., 2018). used in the gases, or aqueous form reduces the microbial load from
Selcuk et al. (2008) used the cold plasma technique to induce different types of cereal grains (Wu et al., 2006; Savi et al., 2015). Ozone
Aspergillus spp. and Penicillium spp. on grain surfaces. This non-thermal has been reported to degrade the common mycotoxins found in grains
technique reduced the fungal infection to below 1% without affecting like aflatoxins B1, B2, G1, G2, fumonisin B, ochratoxin A, patulin, and
the seed quality. Maize grains were treated with atmospheric plasma zearalenone. (Kottapalli et al., 2005). Ozone treatment degrades the
contaminated with Aspergillus flavus and A. parasiticus spores. After mycotoxins or leads to chemical modifications and reduces their activity
plasma treatment, a significant reduction of fungal spores was observed. (Tiwari et al., 2010). McKenzie et al. (1997) reported that aflatoxin B1 is
Moreover, the study also showed that plasma technology’s fungicidal rapidly degraded by ozone into new products that are non-toxic or
effect is associated with modification in the spore surface morphology having lower toxicity.
and loss of spore (Dasan et al., 2016). Shi et al. (2017a,b) studied at­ The main advantage of ozone treatment is that it affects the quality
mospheric cold plasma’s effect on aflatoxin degradation in corn. Afla­ properties of food grains minimally. Decontamination of mycotoxins in
toxin rapidly degraded at different time intervals of plasma treatment. grains by ozone processing depends on many factors such as the con­
Wielogorska et al. (2019) explored the use of cold atmospheric plasma to centration of ozone, treatment temperature, time of exposure, ozone
decontaminate mycotoxins in maize. The treatment time of 10 min flow rate, moisture, pH, and surface roughness of the grain (Tiwari et al.,
2010). There is also the increased efficiency of the ozone process in
aqueous media compared to the gaseous phase due to moisture. Raila
Table 3 et al. (2006) used ozone treatment to decontaminate wheat grain at
Effect of cold plasma treatment on mycotoxins. different moisture content. The ozone treatment efficiently reduces the
Type of Treatment Type % reduction Reference contamination in wheat grains at higher moisture levels. Moisture im­
mycotoxin of of proves ozone treatment efficiency because water solubilizes ozone and
grain mycotoxins increases the contact between grain and ozone gas. In another study,
AFB1 Helium gas with 0.5 Maize 65 Wielogorska Young (1986) observed the reduction of mycotoxins in corn during
and 0.75% of oxygen, et al. (2019) moist conditions. Prudente and King (2006) observed the reduction of
exposure time 10 92% of aflatoxin levels in corn. Ozone is efficiently applied to eliminate
min, frequency 20
kHz
aflatoxin and citrinin from wheat grains using different gas (Savi et al.,
Fumonisin Helium gas with 0.5 Maize 64 Wielogorska 2014). The mycotoxin AFB1, which is the more toxic among aflatoxins, is
B1 and 0.75% of oxygen, et al. (2019) highly reduced by ozone treatment. The temperature of grain and time
exposure time 10 during treatment affects the efficiency of ozone for the degradation of
min, frequency 20
mycotoxins. The higher degree of temperature and treatment time in­
kHz
Aflatoxin Treatment time 1 Maize 62 Shi et al. creases the efficiency during ozone processing (Proctor et al., 2004).
min, humidity 40%, (2017) However, there are particular challenges associated with ozone treat­
modified atmosphere ment. Ozone treatment efficiency depends on factors like the type of
65% oxygen30% grain, treatment time, and moisture, which affects its efficacy during
CO2/5% N2
Aflatoxin Treatment time 10 Maize 82 Shi et al.
application. Moreover, ozone treatment also induced lipids’ oxidation,
min, humidity 40%, (2017) degradation of some vitamins and phenolic compounds, and color
modified atmosphere changes (Deng et al., 2020).
65% oxygen30%
CO2/5% N2

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S.A. Mir et al. Food and Chemical Toxicology 148 (2021) 111976

Fig. 4. Proposed mechanisms for plasma-

induced degradation of aflatoxin B1. AFB1:
Aflatoxin B1(C17 H13O6; MW: 313); P1:
Product 1 (C16H17O6; MW: 305); P2:
Product 2 (C17H15O7; MW: 331); P3:
Product 3 (C14H13O5; MW:261); P4: prod­
uct 4 (C14H11O6; MW:275); P5: Product 5
(C17H13O7; MW: 329); P 6: Product 6
(C19H19O8; MW: 375); I1: Intermediate
product1 (C16H13O6; MW: 301); I2: Inter­
mediate product 2 (C19 H15O8; MW: 371)
(Adapted from Gavahian and Cullen, 2020).

2.8.4. Pulsed light

Table 4
Pulse light is one of the promising tools used for the decontamination
Effect of ozone treatment on mycotoxins.
of grains (Table 5). It is a potential alternative to traditional technologies
Type of Treatment (gaseous Type % reduction Reference without significantly affecting the quality of grain. However, pulse light
Mycotoxin state) of of
has a low ability to penetrate the grain and decreases the germination
grain mycotoxins
percentage of seeds used for sprouting (Maftei et al., 2013). The
Deoxynivalenol Ozone Wheat 64.3 Trombete
decontamination efficiency of pulse light is due to the broad spectrum of
Aflatoxins concentration 60 48 et al. (2017)
mg/L for 300 min
UV light, short flashes, and peak power (Wang et al., 2016; John and
AFB1 Ozone gas Wheat 94.6 Savi et al. Ramaswamy, 2018). Pulse light is a cost-effective and non-thermal
concentration 60 (2015) technique that does not leave any residues on food material. Many
μmol/mol, food material factors like matrix and thickness of food material,
exposure time 180
composition, and type of mycotoxin could influence pulsed light treat­
min
AFB2 Ozone gas Wheat 84.5 Savi et al. ment (John and Ramaswamy, 2018).
concentration 60 (2015) Pulse light processing conditions strongly affect treatment efficiency
μmol/mol, and depend on the number of pulses used for treatment, power of pulses,
exposure time 180 and distance from lamp to sample during treatment (Abuagela et al.,
min
AFG1 Ozone gas Wheat 80 Savi et al.
2019). Maftei et al. (2013) applied the pulse light for the decontami­
concentration 60 (2015) nation of wheat grain. The grains were treated with pulse light treatment
μmol/mol, up to 40 flashes of fluence of 0.4 J/cm2 per pulse, with an overall energy
exposure time 180 release ranging from 6.4 to 51.2 J g− 1. The pulse light showed the
min
efficient microbial reduction (4 log cycles) at higher doses (51.2 J g− 1).
AFG2 Ozone gas Wheat 81 Savi et al.
concentration 60 (2015) Wang et al. (2016) studied the influence of pulse light treatment on the
μmol/mol, degradation of aflatoxins B1 and B2 in rough rice. Rice samples were
exposure time 180 treated with 0.52 J/cm2/pulse for different times of 20, 40, 60, and 80 s
min at room temperature. Pulse light treatment of the 80s reduces the AFB1
Deoxynivalenol Ozone gas 60 Wheat 100 Savi et al.
μmol/mol, (2014)
(75%) and AFB2 (39.2%). The aflatoxin B2 was less susceptible to
exposure time 120 degradation by pulse light treatment than aflatoxin B1. The variation in
min these mycotoxins’ degradation capacity is due to the molecular struc­
Fungal spores 0.33 mg of ozone (g Wheat 97 Wu et al. tures’ difference, which affects photodegradation efficiency.
sample)− 1 min− 1 (2006)
In another study, Zenklusen et al. (2018) applied the pulse light
Fusarium Ozone treatment of Barley 36 Kottapalli
11 and 26 mg/g for et al. (2005) treatment on malted barley. Maximum reduction of A. carbonarius and
15 min A. flavus were observed after 5–15 s of treatment time. Chen et al. (2019)
AFB1 Time: 5–40 min; Corn 88 Luo et al. used the intense pulsed light for deoxynivalenol decontamination in raw
Ozone (2014) and germinated barley. Pulsed light potentially degraded the deoxy­
concentration
40–90/L
nivalenol in barley after a treatment time of 180 pulses in the 60s.
AFB1 Time: 5–40 min; Wheat 97 El-Desouky However, pulsed light technology has certain limitations. Pulse light is
Ozone et al. (2012) effective in surface decontamination due to its limited penetration ca­
concentration pacity. Moreover, it also negatively affects the quality of heat-sensitive
20–40/L
food materials (Deng et al., 2020).

2.8.5. Biological methods

Biological methods are becoming popular among consumers due to

6
S.A. Mir et al. Food and Chemical Toxicology 148 (2021) 111976

Fig. 5. (a): First ozonolysis pathway of aflatoxin B1 in acetonitrile solution (Adapted from Diao et al., 2012). (b): Second ozonolysis pathway of aflatoxin B1 in
acetonitrile solution (Adapted from Diao et al., 2012).

2.8.6. Natural ingredients

Table 5
Natural ingredients from different sources such as spices, herbs, and
Effect of pulse light treatment on mycotoxins.
plants are used mostly in powdered form to decontaminate mycotoxins
Type of Treatment Type of % reduction of Reference while they would not leave any residual toxicity observed in various
mycotoxin grain mycotoxins
synthetic chemicals used for decontamination (Shanakhat et al., 2015).
AFB1 Pulse light Rice 75 Wang et al. From this viewpoint, chemical compounds in natural ingredients could
treatment of 0.52 (2016)
be considered as chemically-based approaches for mycotoxin decon­
J/cm2/pulse for
80s tamination (Ismail et al., 2018). The anti-mycotoxigenic efficiency of
AFB2 Pulse light Rice 39.2 Wang et al. natural ingredients depends on active constituents such as phenolic
treatment of 0.52 (2016) acids, alkaloids, quercetin, terpenes, tannins, and volatile compounds
J/cm2/pulse for (Sultana et al., 2015). Essential oils from aromatic plants showed the
80s
Deoxynivalenol 180 pulses for 60 s Barley 35.5 Chen et al.
potential detoxifying capacity against aflatoxin in sorghum grain. These
(2019) essential oils contain particular components like eugenol and iso­
thiocyanates, which possess detoxifying capacity against mycotoxins
(Komala et al., 2012; Hontanaya et al., 2015). The neem leaves were
promising results showing efficient decontamination of mycotoxins. It is found to be a potential detoxifying agent against aflatoxins during
an eco-friendly technique that does not leave any residue. Numerous long-time storage for maize, wheat, and rice (Sultana et al., 2015).
biological agents like bacterial strains, molds, and yeasts have shown However, the pungent aroma of some natural ingredients may restrict
promising results to degrade or bind the mycotoxins biologically (Fuchs their applications in food material.
et al., 2008; Luo et al., 2018). The microorganisms used for mycotoxin Nowadays, there is a potential demand for plant extracts for various
decontamination must have high-efficiency and cost-effectiveness, applications in the food industry. Plant extracts from different sources
without producing any undesirable substance in food material. More­ have been reported to have the ability to degrade the mycotoxins
over, these microorganisms did not negatively influence grain quality (Ponzilacqua et al., 2019). Plant extracts show a promising approach
(Khaneghah et al., 2017; Fashandi et al., 2018). These microorganisms and are effectively used to prevent fungal growth and accumulation of
are applied at different grain production stages, like during preharvest mycotoxins in food grain. Kalagatur et al. (2018) reported that the
or postharvest stages, to control the mycotoxins. The effect is mediated combined effect of essential oil and gamma irradiation was highly effi­
through the competition for substrate and inhibitory metabolites’ pro­ cient in controlling the mycotoxin production by F. graminearum in
duction (Kabak and Dobson, 2009). Biological detoxification also in­ maize grains.
volves enzymatic degradation or modification of toxins resulting in a
decrease in potential toxicity. Common microorganisms for detoxifying 3. Conclusion
the aflatoxins are lactic acid bacteria, Bacillus licheniforms, B. subtilis, and
Saccharomyces cerevisiae. (Cho et al., 2010; Campagnollo et al., 2015; Possible mycotoxin contamination risks associated with cereal grains
Ismail et al., 2018). Some Rhizopus spp. have also been tested for remain a foremost concern of the industry and a severe threat to human
decontamination of mycotoxins due to their mycotoxin binding capac­ health. However, the traditional techniques used for control of myco­
ity. Simultaneously, the microbial cells can adsorption the aflatoxin toxin spoilage of cereal grains reduce the toxin load, with negative im­
from the food, by physically bound to the toxin due to adherence to the plications on the qualities of the grain and environmental impacts. To
bacterial cell wall (Gonçalves et al., 2017). The adsorption capacity of mitigate the limitations of the traditional techniques, novel decontam­
bacterial and yeast enables the use of enterosorbents to decrease my­ ination technologies like ozone, cold plasma, and irradiation have
cotoxins’ bioavailability (Kabak and Dobson, 2009; Zhou et al., 2017). shown promising results while used for the degradation of mycotoxins.
Novel technologies efficiently degrade the mycotoxins without

7
S.A. Mir et al.
significantly affecting the quality properties. Moreover, each technology
showed varied efficiency at optimized processing conditions, which also
depends on food material properties. Besides, biological techniques
based on the degradation or removal of mycotoxins by microbes like
bacteria and yeast have shown the potential prospect. Each technology
is having some advantages while using for detoxifying the mycotoxins.
More studies are required to ensure that these novel techniques provide
efficient mycotoxin degradation without compromising grain quality.
CRediT authorship contribution statement
Shabir Ahmad Mir: Conceptualization, Methodology, Writing -
original draft. B.N. Dar: Software, Formal analysis. Manzoor Ahmad
Shah: Validation, Investigation. Sajad Ahmad Sofi: Software, Re­
sources. Afshan Mumtaz Hamdani: Visualization, Investigation. Car­
los A.F. Oliveira: Writing - review & editing. Motahareh Hashemi
Moosavi: Writing - review & editing. Amin Mousavi Khaneghah:
Validation, Writing - review & editing, Supervision. Anderson S. San­
t’Ana: Validation, Writing - review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have influenced the work
reported in this paper.
Acknowledgments
Amin Mousavi Khaneghah would like to thank the support of
Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)
(Grant #2018/15432-7). A. S. Sant’Ana acknowledges the support from
National Council for Scientific and Technological Development for
financial support (Grants: #302763/2014-7 and #305804/2017-0).
This study was financed in part by the Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.
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