Animal Feed Science and Technology: W.-X. Peng, J.L.M. Marchal, A.F.B. Van Der Poel

Animal Feed Science and Technology 237 (2018) 129–153
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Animal Feed Science and Technology

journal homepage: www.elsevier.com/locate/anifeedsci
Review article
Strategies to prevent and reduce mycotoxins for compound feed

T
manufacturing
⁎
W.-X. Penga, J.L.M. Marchalb, A.F.B. van der Poela,
a
Animal Nutrition Group, Wageningen Institute of Animal Sciences, WIAS, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The
Netherlands
b
ForFarmers, Kwinkweerd 12, 7241CW Lochem, The Netherlands
AR TI CLE I NF O AB S T R A CT
Keywords: Mycotoxins are the secondary metabolites of fungi, especially moulds. They have over 300 types
Mycotoxins and can be easily produced ubiquitously by moulds. Many mycotoxins have been found to be
Prevention toxic to most farmed animals through the diets. With the globalization of feed ingredient trade
Reduction and the rapid climate changes, occurrence of mycotoxins become increasingly difficult to be
Feed additives
predicted. Thus, the unnoticeable mycotoxin hazards can directly impact the animal production
Compound feed
systems. Preventing or minimizing mycotoxins in feed ingredients has become an important topic
from the aspect of feed manufacturing industry. The aim of this literature review is to summarize
the effective strategies for feed manufacturers to minimize the mycotoxin hazards. Prevention
methods, including pre-harvest field management and post-harvest storage management, are still
the most effective strategies, since mycotoxins are hardly to be eliminated once they are present
in the ingredients. Moreover, mycotoxin reducing effects of several feed manufacturing tech-
nologies are also reviewed. In this review, the mycotoxin reducing methods are mainly cate-
gorized into 4 methodologies: physical methods, thermal methods, chemical methods, and my-
cotoxin controlling feed additives. The first three methodologies mainly focus on how to reduce
mycotoxins in feed ingredients during processes, while the last one on how to compensate the
adverse impacts of mycotoxin-contaminated diets in animal bodies. The results showed that most
of the methods reviewed show evident mycotoxin reducing effects, but of different consistencies.
On the other hand, many practical factors that can affect the feasibility of each method in
practical manufacturing are also discussed in this review. In conclusion, mycotoxin prevention
management and the processing stage of cleaning and sorting are still the most efficient strategies
to control mycotoxin hazards in current feed manufacturing.
1. Introduction
1.1. Overview: mycotoxins
Mycotoxin contamination is one of the most severe threats to modern feedstuff manufacturing and animal husbandry. Modern
academic detection of mycotoxins started in 1961, when mass mortality of turkeys occurred in England and then aflatoxin was
discovered and accused as the culprit (Richard, 2007). In following decades, more mycotoxins and their toxicities were gradually
discovered, and some mass health problems recorded before 1960s were retrospectively found related to mycotoxins (Richard, 2007).
⁎
Corresponding author.
E-mail address: thomas.vanderpoel@wur.nl (A.F.B. van der Poel).
https://doi.org/10.1016/j.anifeedsci.2018.01.017
Received 6 November 2017; Received in revised form 15 January 2018; Accepted 16 January 2018
0377-8401/ © 2018 Elsevier B.V. All rights reserved.
W.-X. Peng et al. Animal Feed Science and Technology 237 (2018) 129–153
Table 1
Brief information of some concerned mycotoxins (Hussein and Brasel, 2001; Richard, 2007; Streit et al., 2012).
Mycotoxin Main origin Host crop Main adverse effects
Aflatoxin Aspergillus flavus Wheat Decreased feeding performance, acute damage in organs, carcinogen and sudden death
A. parasiticus Barley
Maize
Peanut
Deoxynivalenol Fusarium species Wheat Impaired feeding performance, immune-suppressive,
Barley
Oats
Maize
Zearalenone Fusarium species Maize Little acute toxicity, disorder of female estrus and reproduction, smaller litter size and weak piglets
Wheat
Barley
Sorghum,
Rye
Fumonisin F. proliferatum Maize Carcinogen to humans, pulmonary oedema in swine and leukoencephalomalacia in horses
F. verticillioides Sorghum
Rice
Ochratoxin A A. ochraceus Maize, kidney and liver damage, immune suppression, infant deformity
Penicillium viridicatum Raisins
P. cyclopium Barley
Soy
Coffee
T-2/HT-2 F. sporotrichioides Corn Inhibition of protein synthesis, disruption of DNA and RNA synthesis
F. poae Wheat
Barley
Oats
Rice
Rye
Modern animal feed/human food manufacturing suffers from increasing risks of mycotoxin contamination, since mould infection can
occur in almost all sectors involved, from crop cultivation in the field to the storage and logistics of finished commodities. Compared
to those man-made toxins such as pesticides, preservatives and some feed/food additives, mycotoxins, as a group of natural toxins,
are more difficult to be controlled because of the absence of standardized management and sufficient toxicological data (Berthiller
et al., 2013).
‘Mycotoxin’ refers to a group of toxic compounds which are produced by fungi and are toxic to vertebrates and other animals in
low concentrations, which excludes fungi-originated chemical compounds respectively threatening bacteria (categorised as ‘anti-
biotics’) and plants (categorised as ‘phytotoxins’). In addition, general discussion of mycotoxicology tends to focus on unnoticeable
toxic compounds produced by moulds and exclude mushroom poisons, which threaten animals or human mainly through avoidable
accidental ingestions (Bennett and Klich, 2003). Thus, discussion on mycotoxin contamination is highly related to issues of mould
infection. One mould species can produce different mycotoxins, and on the other way one mycotoxin can be produced by different
mould species. Currently, most concerned mycotoxins are mainly synthesized by five fungal genera: Alternaria, Aspergillus, Clados-
porium, Fusarium and Penicillium (Bryden, 2012). Several dangerous mycotoxins that are frequently detected are introduced in this
part (Table 1).
1.2. Most detected mycotoxins in feed manufacturing
1.2.1. Aflatoxin
Among mycotoxins, aflatoxin (AFL) is the most notorious one, not only because it is the first mycotoxin discovered that lead to
animals’ mass mortality, but also due to its current high adverse effects on human and animal health. The major aflatoxins consist of
aflatoxin B1, B2, G1 and G2, and they are mainly synthesized by Aspergillus flavus or Aspergillus parasiticus. Aflatoxin B1 (AB1) is listed
as a severe carcinogen by World Health Organization (WHO). Aflatoxin M1, a metabolic in ruminants of B1 appearing in animal
tissues and fluids (such as milk and urine), has also raised special attention for its residual levels in milk products. Aflatoxins have
been observed to be immunosuppressive, teratogenic and mutagenic to animals. In addition, aflatoxins can impair the intestines and
decrease the feed intake of animals and animals’ growth performance (Richard, 2007), which have been supported by several long-
term studies (Bailey et al., 2006; Dersjant-Li et al., 2003; Han et al., 2008).
1.2.2. Deoxynivalenol
Deoxynivalenol (DON) is the most detected mycotoxin in the ingredients for feed/food production (Richard, 2007; Wu et al.,
2007). DON is mainly produced by Fusarium, like F. graminearum, F. crookwellense and F. culmorum (Eckard et al., 2011). Grains of
some common crops, including wheat, barley, oats and maize, are common hosts of these fungi. Rachis of maize, which can be
applied as silage feed material, could also suffer from attack of these fungal. Symptoms of fungal attacks occurring in maize rachis are
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mainly the rots, which, however, are hardly distinguishable from those resulting from insects’ or other animals’ attack (Eckard et al.,
2011). This can lead to the ignorance of mycotoxin hazards in silage feed production. DON is one of the least acutely toxic compounds
among trichothecenes (Binder, 2007), which makes its chronic toxicity relatively difficult to be diagnosed. The immunosuppressive
effect is the most observed chronic disadvantage of DON. Among livestock, the pig is particularly sensitive to DON in the diet. Pigs
may vomit soon after they swallow DON, and vomiting can acutely reduce feed intake and growing performance (Richard, 2007). As
indicated by Pestka (2007) levels of already 50 μg/kg body weight can cause vomiting where Bryden (2012) associates dietary levels
of 2–20 mg/kg in the feed with feed refusal and vomiting, respectively. DON metabolism and accumulation in pig body occurs very
soon after the DON contaminated diet is consumed (Danicke et al., 2004). Different from aflatoxin, DON is much less possible to be
transferred into animal-originated food (Richard, 2007).
1.2.3. Zearalenone
Zearalenone (ZEN) is a frequently detected mycotoxin also synthesized by Fusarium fungi like F. graminearum or F. culmorum, and
it usually co-occurs with DON. Most ZEN contamination is observed in maize, but wheat, barley, sorghum and rye are also potential
hosts. Generally, ZEN shows little acute toxicity to animals. Because of its structural similarity to estradiol, ZEN can chronically affect
the reproductive performance of female animals. For example, ‘fake estrus’ of female animals (especially swine) is a potential
symptom of ZEN poisoning (Binder, 2007). Other main symptoms include precocious development of mammae in young gilts and
preputial enlargement in young barrows. From the productive aspect, small litter size and weak piglets are the most notorious
consequences when ZEN interferes with reproduction of older swine. Comparatively, chickens are more tolerant to this toxin (Fink-
Gremmels and Malekinejad, 2007).
1.2.4. Ochratoxin A
Ochratoxin A (OTA) is primarily produced by Aspergillus ochraceus and Penicillium verrucosum (Richard, 2007). This toxin occurs in
storage environment more than in the field. It usually occurs in raisins, barley, soy products and coffee at low level (Richard, 2007).
Adverse consequences of consuming OTA mainly include organ damage, immune suppression and infant deformity. In body, kidney
suffers most from OTA, including the symptoms of vascular lesions, renal haemorrhages, renal lymph nodes enlargement and so on
(Stoev et al., 2002). OTA was accused of being responsible to the once-sensational ‘mycotoxic porcine nephropathy (MPN)’ in 1970s
(Stoev et al., 2002), and it also had been suspected to have resulted in the human Balkan endemic nephropathy (BEN) occurring in
the 1950s (Pfohl-Leszkowicz and Manderville, 2007). OTA is easy to accumulate in organs due to its low metabolizing velocity in
animal bodies, and thus human food originating from these organs also have the risks of OTA accumulation.
1.2.5. Fumonisins
Fumonisin (FN) covers a group of relatively newly discovered mycotoxins (mainly fumonisin B1, fumonisin B2 and fumonisin B3),
produced primarily by F. verticillioides and F. proliferatum. Corn is the major commodity affected by this group of toxins and their
occurrence also has been found in sorghum and rice. Consuming fumonisin can lead to tumors growing in lung, liver and kidney of
rodents and pigs (Richard, 2007). One distinguishable problems of fumonisin is that it can interfere with the sphingolipid metabolism
of horses and foster tumour growth in their brains, and this is quite an unusual pathogenic pattern compared to other mycotoxins.
1.2.6. T2/HT-2
T2 and its derivate HT-2 are also produced by Fusarium, especially F. sporotrichioides. Since mutual transformation between T-2
and HT-2 is frequent under natural conditions, they are often combined as one detecting unit in analytical detections. T-2 and HT-2
have been found to occur in crops including corn, wheat, barley, oats, rice, rye and in temperature ranging from 6 to 24 °C. A 4-year
(2002–2005) survey on barleys and oats at harvest in England showed that 16% of the samples were contaminated by high H-2 and
HT-2 (average combined concentration > 1000 mg/kg), where DON concentrations were quite low (∼300 mg/kg) in the same
survey (Scudamore et al., 2007). T-2 toxin can inhibit protein synthesis, and this can lead to even disruption of DNA and RNA
synthesis. Among the farm animals, poultry is quite sensitive to it.
1.3. Growing impacts of mycotoxins on animal production system
Different mycotoxins could contaminate many crop species. Among these crops, some are quite important as both human food and
animal feed, like maize, wheat, and barley. For example, maize is quite susceptible to various fungi, including A. flavus, A. parasiticus,
F. graminearum, F. verticillioides, Penicillium spp., and Diplodia maydisand. Thus, maize could be easily contaminated by aflatoxins,
DON, ZEN, Fumonisins etc. (Reddy et al., 2009). In recent years, mycotoxin hazard becomes a worldwide increasing problem in
human food or animal feed production. One three-year survey (2009–2011) (Rodrigues and Naehrer, 2012) tested 7049 ingredient
samples (corn, soybean, soybean meal, wheat, dried distillers grains with solubles and finished) from America, Europe or Asia, 81% of
which were contaminated by at least one of the target mycotoxins (aflatoxin, ZEN, DON, FUM and OTA). Among the samples, corn
suffered the highest frequency of mycotoxin contamination, and soybeans or soybean meals met less problems.
In the context of modern feed manufacturing, the occurrence of mycotoxins may become more complicated through the frequent
international trade of ingredients
Legislative or certificating organisations around the world have been trying to establish maximum levels of mycotoxins in
feedstuffs (Cheli et al., 2014). For example, European Commission (EC) published maximum levels of several mycotoxins in the EU.
The mycotoxins targeted are: AB1, DON, ZEN, OTA, FB1 + B2 and T-2 + HT-2 (Table 2). All these maximum levels are low, and some
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Table 2
Regulated and recommended maximum levels of mycotoxins in feed materials set by the European Commission (moisture content: 12%).
Mycotoxin Products Regulated maximum level Guidance Value (mg/kg,

(mg/kg, or ppm) or ppm)
Aflatoxin B1a All feed materials 0.02

Complete feedingstuffs for dairy animals 0.005
Complete feedingstuffs for calves and lambs 0.01
Complementary and complete feedingstuffs for cattle, sheep and goats 0.02
(except complementary feedingstuffs for dairy animals, calves and lambs)
Complementary and complete feedingstuffs for adult pigs and poultry 0.02
DONb Maize by-products 12
Other cereals and cereal products 8
Complementary and complete feedingstuffs except for: 5
-complementary and complete feedingstuffs for pigs 0.9
-complementary and complete feedingstuffs for calves (< 4 months), lambs 2
and kids
ZENb Maize by-products 2
Other cereals and cereal products 3
Complementary and complete feedingstuffs for piglets and young sows 0.1
Complementary and complete feedingstuffs for sows and fattening pigs 0.25
Complementary and complete feedingstuffs for calves, dairy cattle, sheep 0.5
(including lamb) and goats (including kids)
OTAb Cereals and cereal products 0.25
Complementary and complete feedingstuffs for pigs 0.05
Complementary and complete feedingstuffs for poultry 0.1
Fumonisin B1 + B2b maize and maize products 60
Complementary and complete feedingstuffs for pigs, horses, rabbits and pet 5
animals
Complementary and complete feedingstuffs for fish 10
Complementary and complete feedingstuffs for poultry, calves (< 4 months), 20
lambs and kids
Complementary and complete feedingstuffs for adult ruminants 50
(> 4 months) and mink
c
T-2 + HT-2 Oat milling products (husks) 2
Other cereal products 0.5
Compound feed, with the exception of feed for cats 0.25
a
European Commission (2002).
b
European Commission (2006a).
c
European Commission (2013).
of them are lower because of special toxicological backgrounds. For example, maximum level of AB1 in feedingstuffs for dairy animals
is set lower than that in other feeding strategies because of the concern that AB1 in cattle bodies can be transferred into AM1 in milk.
Another example is that the maximum levels of DON and ZEN are set lower because pigs are more sensitive to them. On the other
hand, some mycotoxins, having different distinct forms, are detected as one compound in EC legislatives. For example, the reasons
can be the easy transformation between forms (T-2 and HT-2) or the similar toxicities and appearing frequency (FB1 and FB2). In
addition, EU laws and legislations against mycotoxins are advancing as the accumulation of toxicological studies increase. For
example, EC maximum level of T-2 + HT-2 was recently set in 2013, after their toxicological studies had been performed for decades
(EC, 2013).
Establishment of legal maximum concentrations of mycotoxins does not mean that mycotoxins at low concentrates are safe. Small
amounts of mycotoxins can also interrupt the normal cellular functioning, and even result in cell deaths and accumulative patho-
logical changes (Table 3). Moreover, low levels of mycotoxins in diets can lead to subclinical problems which is less evident,
Table 3
Cascade of cellular events due to the cytotoxicity of several mycotoxins (Riley, 1998; Bryden, 2012).
Mycotoxin Cascade of cellular events
Aflatoxin Metabolic activation → DNA modification → cell deregulation → cell death/transformation (metabolic activation → disruption of
macromolecular synthesis → cell deregulation → cell death (apoptotic))
Deoxynivalenol Inhibition of protein synthesis → disruption of cytokine regulation → altered cell proliferation → cell death/apoptosis?
Fumonisins Sphinganine N-acyltransferase → disrupted lipid metabolism → cell deregulation → cell death/apoptosis (disrupted delta-6-desaturase
activity → disrupted fatty acid and arachidonic acid metabolism → cell death)
Ochratoxin Disruption of phenylalanine metabolism → reduced Phosphoenolpyruvate carboxykinase (PEPCK) → reduced glyconeogenesis → cell death
(metabolic activation → inhibition of protein/DNA synthesis → apoptosis?) (altered membrane permeability → disrupt calcium
homeostasis → cell deregulation → cell death)
Zearalenone Cytosolic oestrogen receptor → estrogenic response → disruption of hormonal control → ?
T-2 Inhibition of protein synthesis → ? → cell death (apoptotic?) (Transient Ca2+ elevation → endonuclease activation → apoptosis)
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including a slight decrease of feed intake and growth, nutrient utilization and (re)productive performance (Bryden, 2012).
Climate change is also fostering mycotoxin hazards. Different fungal strains show preference to specific environments. For ex-
ample, some Aspergillus flavus strains can prosper and produce aflatoxin under low humidity while other Aspergillus flavus strains not
(Magan et al., 2011). Thus, acute climate changes can contribute to changes of mycotoxin distribution. One recent example is the
increasing A. flavus infection and aflatoxin contamination during summer in Southern Europe, where these problems were uncommon
when summers used to be less hot and dry (Streit et al., 2012). On the other hand, the climate changes indirectly influence mycotoxin
accumulation by influencing other local biological factors. For example, draught was associated with increasing insect attack on
maize (Miller, 2008), and these broken kernels usually contain higher mycotoxins (Jouany, 2007).
The update of toxicological studies also helps to refresh the comprehension towards mycotoxins. For example, it was believed that
mycotoxins hazards are much less severe to ruminant animals, but recent studies turned down this concept. This outdated concept
was based on the physiological fact that rumen can degrade several mycotoxins, like OTA, DON and ZEN. However, aflatoxins and
fumonisins have recently been found much less degradable in the rumen than expected (Fink-Gremmels, 2008). Diverse feed re-
sources, including concentrate feed, silage commodities, and natural pasturing, also increase potential dietary mycotoxin hazards to
cattle (Fink-Gremmels, 2008). On the other hand, ensiling was once believed a good process to eliminate fungi and mycotoxins
because of its high moisture, low pH and low oxygen concentrate environment (Eckard et al., 2011). However, Penicillium, one
recently noticed mycotoxigenic mould, has been found able to prosper under the environment of ensiling. Mycotoxins produced by
Penicillium mainly include cyclopiazonic acid (CPA), patulin (PAT), mycophenolic acid (MPA), and roquefortine C (ROC). PAT and
ROC have been observed to cause acute mycotoxicoses in cattle, including paralysis, abortion and even death, but MPA results in less
acute symptoms like immunosuppression (Mansfield et al., 2008). In 120 maize silage samples randomly collected by Mansfield et al.
(2008) from all around US, contamination frequency of these mycotoxins is quite high: 60% (ROC), 42% (MPA), 37% (CPA), and 23%
(PAT).
Since mycotoxin hazards, accompanying fungal infection, could occur ubiquitously, strategies against mycotoxins should cover a
long chain from crop cultivation to feed manufacturing. In the following parts of this review, these strategies are introduced.
2. Prevention strategies against mycotoxin contamination
2.1. Pre-harvest prevention
Pre-harvest mycotoxin prevention strategies are mainly performed during the phase of crop cultivation in the field. Based on
plant-fungus interaction patterns, toxigenic fungi are classified into four categories (Miller, 2008): 1) fungi as plant pathogens (e.g.
Fusarium graminearum); 2) fungi that produce mycotoxins on aging or stressed plants (e.g. Aspergillus flavus on maize); 3) fungi that
colonize the crop and potentially contaminate the post-harvested commodity (e.g. Aspergillus flavus in subtropical maize); 4) fungi left
over in the soil or decaying plant materials which potentially invade newly planted crops or their commodity (e.g. Aspergillus flavus
on many commodities). These interaction patterns lead to the prevention methodologies.
First, different strains of one crop species can show different effects on fungal resistance and mycotoxin control, which is mainly
determined by genotypes (Brandwagt et al., 2000; Miedaner et al., 2001; Gao et al., 2007). Thus, crop breeding is a logical meth-
odology to relieve crops from mycotoxin contamination. However, practical effects of breeding still have many limitations to
overcome. For example, Fusarium head blight (FHB), which usually occurs to corn, is a severe disease caused by Fusarium infection,
and infected plants usually contain high Fusarium mycotoxins. Wounds on plant body, which usually result from insects, crucially
foster this infection. Thus, the trait resistant to both fungal infection and insect wounds are crucial for breeding works of plants’
mycotoxin resistance (Mesterhazy et al., 2012). However, the mycotoxin resistant trait is strongly limited by environment, and its
heritability is also limited (Massman et al., 2010), which greatly bothers the breeding work. Generally, current development of hybrid
breeding for mycotoxin resistance has been left far behind the rapid growing of academic mycotoxin knowledge (Mesterhazy et al.,
2012).
Cultivation management also takes a crucial role in pre-harvest mycotoxin control. Crop rotation with proper species, like wheat
and legumes, is effective to control mycotoxin contamination (Richard, 2007). Proper practice of soil cultivation, like ploughing,
minimum tillage, no-tillage technology, also contributes to the removal or isolation of the infected crop residues, which decrease the
mycotoxin risks invading new cultivated crops (Richard, 2007). Proper sowing date is highly recommended since a delay could
increase the risks of DON accumulation (Eckard et al., 2011). On the contrary, improper supplies of water and nutrition can foster the
soil stress, which fosters mycotoxin accumulation (Richard, 2007).
Preventing the attacks from other organisms, like insects and other animals, is also important, since these attacks can directly
interfere with plants’ resistance capacity towards mycotoxins. Even though the utilization of pesticides or fungicides is rarely ac-
cepted by some developed farming concepts, these fungi controlling products could contribute to mycotoxin prevention. For example,
it was found that crops from organic farms potentially contain six times as much OTA as compared to the crops from conventional
farms (Czerwiecki et al., 2002, reviewed by Pfohl-Leszkowicz and Manderville, 2007).
Rapid developing of information technology has led to mathematical models for regional mycotoxin prediction on field scale.
However, compared to the developed models for predicting crop diseases, models for mycotoxin occurrence are still in their infancy
because of the relatively low accuracy (Miller, 2008). Since dynamics between mycotoxin occurrence, climate factors and other
biological factors remain unclear, these modelling systems still have high uncertainty to overcome (Magan et al., 2011).
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2.2. Post-harvest prevention
Post-harvest management is also crucial to decrease the mycotoxin hazards, since harvested grains lack much defending ability
compared to entire plants. Storage is one crucial stage for the post-harvest prevention of mycotoxins. Storage of harvested grains
forms a man-made ecosystem, with the dynamics of various biotic (grain, bacteria, yeast, fungi etc.) and abiotic factors (water, air,
temperature, etc.). Among these factors, temperature and humidity are crucial for the fungal infection and mycotoxin contamination.
When the humidity is high at 17–20%, DON concentrations can increase significantly due to activity of Fusarium spores (Birzele et al.,
2000). Keeping a low moisture in storage environments is crucial for controlling the level of fungi and mycotoxins. Generally, a water
activity less than 0.7 can efficiently eliminate mould spoilage (Magan et al., 2003), but insufficient drying of grains before storage can
significantly decrease the mycotoxin eliminating effects of dry storage environment.
Biotic factors, like bacteria and other microbes, also foster the mycotoxin problems in storage. The break-in of these organisms
could be due to the impaired tightness of storage, but unnoticed organisms can also sneak into grains before storage. Insect is a
common example of biotic factors impairing the bio-dynamics in storage ecosystem. Different from microbes, insects can survive a
much broader range of temperature and humidity. Activities of insects can produce metabolite heat and water, which form so-called
‘hot spots’ inside the grain heap. These spots can soon provide a suitable environment for fungal growth (Magan et al., 2003). Thus,
keeping insects or similar biotic factors from storage environment is a necessary method for food and feed hygiene and safety.
3. Physical removal of mycotoxins by feed manufacturing technologies
It is insufficient to overcome mycotoxin problems only by prevention strategies. To deal with mycotoxin contaminants which are
present in feedingstuffs, more strategies have to be taken into account. One classic example of these strategies was ‘dilution’, which
means to mix the contaminated materials with clean feed ingredients to achieve a mixture whose mycotoxin concentrations can be
legally low. However, ‘hot spot’ hazard, which means a partial high toxicity in the feed materials, was then found to threaten
consumers’ health. Another typical strategy was to assign the contaminated materials to the livestock species which were thought to
have a higher mycotoxin resistance, like ruminants. In recent years, however, this method has also been found dangerous since these
animals have been found not as resistant to mycotoxins as having been expected (Part 1). Currently, both these methods are pro-
hibited in the European Union (EC, 2006b).
As required by European Commission (2006b), cereal grains should meet the legal and recommended levels of mycotoxins
(Table 2) before entering the ‘first-stage processing’, which means ‘any physical or thermal treatment, other than cleaning, sorting
and drying’. Nevertheless, feedingstuffs with legally low mycotoxin levels might still be threatening to consumers (Alassane-Kpembi
et al., 2013; Streit et al., 2013). Thus, reducing mycotoxin concentrations as low as possible becomes a crucial task for compound feed
manufacturers. This part 3 focuses on several methodologies that can physically remove from feedingstuffs.
3.1. Cleaning and sorting
Generally, cleaning means to remove external materials like large foreign trash and dust, and sorting means to pick out the
inferior kernels from the healthy ones. These unwanted materials can decrease feed quality and even impair the consumers’ health, as
well as attract toxigenic fungi. Moreover, cleaning and sorting practices are expected to reduce concentrates of mycotoxins to a low
level in respect to EU requirements, which gives high importance to the mycotoxin reducing effects of cleaning and sorting.
One traditional sorting method is hand sorting, which means to pick out the inferior grains by human labour. This method is based
on the visible abnormalities of kernels, like smaller size, mould spots or colour changes, which could be associated with higher
possibility of mycotoxin contamination (Kabak et al., 2006). Effectiveness of this traditional method is highly dependent on the
experiences of workers, and it can be only performed in small-scale production situations. Another traditionally applied sorting
method to reduce mycotoxins is wet sorting. Main mechanism of wet sorting is to remove the buoyant of kernels in liquid, based on
their different densities. These lighter fractions contain at least within one batch more mycotoxins since their decreased densities
could be involved with fungal activities in kernels (Huff, 1980, Huff and Hagler, 1982, 1985).
Several articles on mycotoxin reducing effects of these traditional methods were published. Matumba et al. (2015) compared the
mycotoxin reducing effects between hand sorting and water flotation. In their study, hand sorting helped to increase the safety of
products by eliminating over 90% of all kinds of target mycotoxins (aflatoxins, fumonisins, DON etc.), and in comparison, the
reducing effects of liquid flotation were highly varied (32–78%) between mycotoxins (Table 4). Types of solutions could be crucial for
the wet sorting’s mycotoxin reducing effects by removing contaminated parts without specificity. For example, Huff and Hagler
(1985) observed that liquid flotation with 30% sucrose solution could decrease DON concentration by 76.7% in a maize sample with
6 ppm initial DON, while flotation with water could only reduce that by 11.7% in a backup sample (Table 4), even though similarly
large differences between solutions were not repeatedly observed in other samples of the same study. In another study (van der
Westhuizen et al., 2011), the mycotoxin reducing effects of simple washing by water were examined, but limited effects were
observed, which was much inferior to the effects of hand sorting in the same study (Table 4).
The traditional cleaning and sorting methods introduced above, however, are inapplicable in large-scale manufacturing situa-
tions, for their low efficiency and high costs. The authors recognize however, that these methods provide valuable information what
can be achieved, especially since the fast advances of image processing and computer power will make this economical achievable in
the near future.
In large-scale feed manufacturing, cleaning and sorting are highly mechanized, which usually combine several mechanical
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Table 4
Mycotoxin reducing effects of cleaning and sorting processes.
Samples Conditions Mycotoxin Reduction (%) Mass Loss (%)
a,b
Wheat Air screen cleaner gravity separator DON 74.7 28.0
Wheatb,c Air screen cleaner gravity separator DON 88.9 32.9
Oatd,e Air separator T-2/HT-2 48.3 ± 44.7f
Maizeg Liquid flotation (brine solution)q Aflatoxin 73.4 ± 2.1f 3.4
Liquid flotation (water) DON 11.7 3.4
Liquid flotation (30% sucrose) DON 76.7 7.5
Maizeh Water flotation NIV 57.3 6.4
DON 60.4
3-AcDON + 15-AcDONi 32.3
Aflatoxin B1 62.6
Aflatoxin B2 64.2
Aflatoxin G1 55.9
Aflatoxin G2 68.2
FB1 74.3
FB2 77.8
FB3 67.0
Hand sorting NIV 95.4 14.3
DON 96.3
3-AcDON + 15-AcDONi 95.7
Aflatoxin B1 98.7
Aflatoxin B2 96.0
Aflatoxin G1 99.2
Aflatoxin G2 97.7
FB1 92.1
FB2 95.7
FB3 91.6
Maizej Hand sorting FB1 + FB2 + FB3i 71 ± 18f 2.5 ± 0.5f
Maizej,k Washing for 5 min 5 ± 8f
Washing for 10 min 13 ± 12f
Washing for 30 min 12 ± 33f
Washing for 60 min 9
Wheatl Sieving, scouring and polishing DON 49.8, 45.4, 46.7 & 52.7m
NIV 100 n
HT-2/T-2 100n,o
Durum wheatp Sieving machine DON 22.6 ± 10.5f
a
Wheat cultivar BRS Parrudo.
b
Tibola et al. (2016).
c
Wheat cultivar BRS 374.
d
Schwake-Anduschus et al. (2010).
e
Samples cover 4 cultivars from 10 cultivating sites.
f
Mean ± Standard deviation based on 24 different samples.
g
Huff and Hagler (1985).
h
Matumba et al. (2015).
i
Different mycotoxins were merged as one index.
j
van der Westhuizen et al. (2011).
k
Inferior maize grains had been discarded by hand sorting.
l
Lancova et al. (2008).
m
DON reduction respectively for 4 samples with different initial DON concentrations: 909, 108, 92 and 2985 (μg kg−1).
n
Mycotoxin concentrations in cleaned samples were lower than the limit of detection.
o
Not all uncleaned samples contained targeted mycotoxins.
p
Visconti et al. (2004).
q
‘Each sample was stirred for 2 min in a saturated sodium chloride solution (brine solution, d-1.2)’.
equipment, including air separators, sieves, gravity separators and indented cylinders. Alike the wet flotation, the mechanical sorting
is mainly based on the lower density of potential infected grains. Several authors have studied the mycotoxin decontaminating effects
of these mechanical methods (Lancova et al., 2008; Visconti et al., 2004; Tibola et al., 2016; Schwake-Anduschus et al., 2010). In the
study of Tibola et al. (2016), mechanical cleaning was observed with general good DON decontaminating effects in wheat, but
difference occurred between wheat cultivars (74.7 and 88.9% respectively). Moreover, some articles also focused on those less
commonly occurred mycotoxins, like NIV and T-2/HT-2. Lancova et al. (2008) observed that almost 100% of NIV and T-2/HT-2 were
eliminated through cleaning machine (including the process of Sieving, scouring and polishing). However, in the study of Schwake-
Anduschus et al. (2010), the cleaning by air separator was observed to result in high variation (2.3–100%) in T-2/HT-2 reduction, and
this may be partly due to the high diversity of the cultivars and places of origin of these oat samples (4 cultivars from 10 cultivating
sites) (Table 4).
135
Table 5
Mycotoxin reducing effects of dehulling processes.
Samples Conditions Mycotoxins Reduction (%) Mass loss (%)
a b
Maize 11% Moisture Aflatoxin B1 + B2 + G1 + G2 93.4 20
Aflatoxin B1 88.8
20% Moisture Aflatoxin B1 + B2 + G1 + G2b 91.4
Aflatoxin B1 89.8
Oatc 4 cultivars from 10 locations T-2 88.3 ± 14.2d
HT-2 100
Maizee Wooden mortar and pestle NIV 71.8 29
DON 62.9
3-AcDON + 15-AcDONb 51.6
Aflatoxin B1 87.8
Aflatoxin B2 91.9
Aflatoxin G1 94.1
Aflatoxin G2 94.4
FB1 85.2
FB2 90.3
FB3 88.9
a
Siwela et al. (2005).
b
Different mycotoxins were merged as one index.
c
Schwake-Anduschus et al. (2010).
d
Mean ± Standard Deviation.
e
Matumba et al. (2015).
3.2. Dehulling
In feed manufacturing, dehulling is a mechanical process to remove the outer layer of the grains. This process is widely used for
cereals, legume seeds and oilseeds with outer fibrous compositions (Rios et al., 2009a). Dehulling also helps to increase the fineness of
subsequent milling products, such as flour and semolina (Cheli et al., 2013). The removed hulls can be re-utilized to meet some
livestock’s nutritional requirements for fibres. From the aspect of feed hygiene and safety, this removal can incidentally decrease the
contaminants attached to the outer layer, including fungi and mycotoxins.
Several studies on the mycotoxin detoxification effect of dehulling process have been published. In their results, the mycotoxin
contents in the dehulled feed materials have been significantly decreased (Table 5). Dehulling could be performed with different
tools. For example, Siwela et al. (2005) studied the aflatoxin reduction in maize through ‘a dehuller’; Schwake-Anduschus et al.
(2010) studied the T-2/HT-2 reduction in oat by laboratory huller; Matumba et al. (2015) applied traditional dehulling with wooden
mortar and pestle to examine mycotoxin reduction in maize. These studies indicated that many factors, including crop species, crop
cultivars and processing duration, could crucially influence the mycotoxin reducing effects of dehulling process. Moreover, Rios et al.
(2009a) proposed two curved-line models to explain the relationship between dehulling duration, grain mass loss and the remaining
DON proportions in two wheat samples: the first model (Fig. 1) indicated the grain mass loss percentage (Y axis) against duration (X
axis), and the second model (Fig. 2) indicated the remaining DON percentage (Y axis) against the grain mass loss percentage (X axis).
For example, it could be observed that 20 min’ milling process reduces about 20% grain mass (Fig. 1), which takes away about 60%
DON (Fig. 2). Similarly, House et al. (2003) also proposed a similar curving line between grain loss mass and remaining DON
percentage in barley (Fig. 3). In this study, high reduction (e.g. 65%) of DON was observed with 15% mass loss within a very short
dehulling duration (15 s), and 1.5 min seemed long enough to eliminate 90% of DON, but with a mass loss of 40% (Table 6).
Fig. 1. Relationship between dehulling duration (min) and percentage of grain mass loss in two durum wheat grain samples with different initial DON concentrations
(A1 presents the first sample which contains 382 mg kg−1 initial DON; A2 presents the second sample which contains 4203 mg kg−1 initial DON) (Rios et al., 2009a).
136
Fig. 2. Relationship between percentage of grain mass loss and proportions of remaining DON in two durum wheat grain samples with different initial DON con-
centrations (A1 presents the first sample which contains 382 mg kg−1 initial DON; A2 presents the second sample which contains 4203 mg kg−1 initial DON) (Rios
et al., 2009a).
Fig. 3. Relationship between percentage of remaining grain mass and proportions of remaining DON in barley samples (House et al., 2003).
Table 6
Effects of dehulling duration on grains’ mass loss and mycotoxin reduction.
Sample Mycotoxin Dehulling duration Reduction Mass loss
a
Durum Wheat DON 5 min 45% 10%
10 min 60% 20%
30 min 70% 35%
Barleyb DON 15 s 66% 15%

45 s 82% 26%
90 s 90% 40%
a
Rios et al. (2009b).
b
House et al. (2003).
3.3. Milling
Milling is a process to physically break grains into smaller particles. The application of this process is based on that milled
fractions of different sizes usually contain different main nutrients. For example, large granules (20 μm) of milled pea seeds contain
mainly starch particles, when small particles (1–3 μm) of these milled seeds are protein-rich (Pelgrom et al., 2013). Thus, milled
fractions of different sizes are usually separately preserved for manufacturing different products. In practical situations, the air
separator equipped within typical milling machine is for separating fractions with different densities, and these fractions can be
collected for further manufacturing.
Logically, milling processes can only redistribute the existing mycotoxins into different fractions, rather than to eliminate or
deactivate these toxins. Since the outer layer of kernels is easier to be contaminated than inner parts (Lancova et al., 2008), milling is
expected to result in lower mycotoxin concentrations in fractions from grains’ inner parts (e.g. flour or semolina) compared to that in
initial grain samples, meanwhile higher mycotoxin levels in those fractions originating from outer layer (e.g. brans and shorts) (Cheli
et al., 2013). While in highly contaminated grains, high mycotoxin levels could also be observed in the finest fractions originating
from endosperm. Rios et al. (2009b) studied the distribution of DON in the milled fractions of two French durum wheat samples with
different initial DON concentrations (382 and 4204 mg kg−1, Table 7). In this study, samples were successively milled by two types of
137
Table 7
Redistribution of mycotoxins in milled durum wheat samples of different initial contaminating levels (Rios et al., 2009b).
Sample A1: initial DON concentration before milling: 382.0 ± 9.7 mg kg−1
Mill fraction Yield (%) DON (%) Concentration (mg kg−1) Change rate (%) CV (%)
Total semolina 76.4 40.8 199.3 ± 62.0a

−47.8 b
31.1
Total break flours 3.2 4.8 637.3 ± 166.7a +66.8b 26.2
Total reduction flours 3.7 3.5 374.8 ± 56.1a −1.9b 15.0
Total bran & shorts 16.8 50.8 908.5 ± 478.0a +137.8b 52.6
Sample A2: initial DON concentration before milling: 4203.5 ± 202.7 mg kg−1
Mill fraction Yield (%) DON (%) Concentration (mg kg−1) Change rate (%) CV (%)
Total semolina 75.9 49.6 3015 ± 632.6a −78.4b 21.0

Total break flours 3.3 3.7 5623 ± 1890.4a +33.8b 33.6
Total reduction flours 4.2 4.1 4467 ± 1164.0a +6.3b 26.1
Total bran & shorts 16.6 42.6 9087 ± 4279.5a +116.2b 47.1
a
b
Change rate indicates the mycotoxin concentration in milled fractions compared to that in initial unprocessed samples. ‘+’ represents the increase of con-
centration, and ‘−’ represents the decrease.
rolls (‘break rolls’ and ‘reducing rolls’), and then different milled fractions were collected for mycotoxin tests. In both samples, the
fraction ‘bran and shorts’ were observed to contain high proportions of the total DON (50.8% and 42.6%), but this did not signal that
the removal of this fraction was sufficient to overcome the mycotoxin hazard, since the finest fraction ‘total semolina’ still maintain
high DON proportions (40.8% and 49.6%). Similar results were observed in the study of Lancova et al. (2008), which was performed
on 4 wheat samples of different initial mycotoxin contamination levels (909, 108, 92 and 2985 mg kg−1 respectively). The results
indicated that 50–65% of total initial DON were removed with brans and rests (shorts, losses etc.), but certain proportions of total
DON remained in the break flour (10–22%) and the reducing flour (24–28%). Visconti et al. (2004) also observed about 47% of total
DON in unprocessed durum wheat samples were distributed to milled semolina fraction.
However, these proportions of redistributed mycotoxins were only about the ‘amount’ of mycotoxins, which indeed are much less
crucial than mycotoxin concentrations. Thus, mycotoxin redistributing effects of the milling process could be interpreted from the
aspect of mycotoxin concentrations again. In the study of Rios et al. (2009b), DON concentration in semolina fraction show large
reduction (by 47.8% and 78.4 respectively in two samples), regardless that nearly half of initial DON was left in this fraction
(Table 7). Similarly, good mycotoxin reduction of mycotoxin concentrations was also showed in the fine milled fractions in other
studies (Lancova et al., 2008; Visconti et al., 2004). More rigorously, Tibola et al. (2015) studied samples with different initial DON
levels, and found that mycotoxin reduction in fine milled wheat fractions decreased with the grains’ initial contaminating level
increasing. In this study, untreated samples were classified, based on different levels of initial DON contamination (A:498.8 mg kg−1,
B: 746.5 mg kg−1, C: 1225.0 mg kg−1, D: 2747.5 mg kg−1 and E: 5985.0 mg kg−1). The results of this study showed that DON
concentrations in finished flour decreased with these initial concentrations increased (42.1%, 33.6%, 35.8%, 21.5% and 10.4%)
(Table 8). In addition, low levels of ZEN co-occurred in sample D and E in this study, and milling seemed efficient enough to eliminate
them in finished flours.
3.4. Summary of physical removal methods
In this part, mycotoxin reducing effects of several feed manufacturing processes (cleaning, sorting, dehulling and milling) have
been introduced. In all these processes, mycotoxins are mainly decreased due to the physical separation rather than chemical and
biological deactivation, and thus they are classified as ‘physical removal methods’. Cleaning and sorting is first line methodology to
remove contaminants, including mycotoxins in grain samples. In the reviewed studies, hand sorting showed highest mycotoxin
reducing effects since 70%–99% of different mycotoxin types were reduced (Matumba et al., 2015; van der Westhuizen et al., 2011).
Liquid flotation methods also showed good mycotoxin reducing effects, especially when an optimal solvent is supplied (Matumba
et al., 2015). However, these two methods are rarely applied in practical manufacturing situations because of high extra costs. In
comparison, reducing effects of cleaning machines (e.g. air separator, sieving machine) are various. Some studies declared to observe
high DON reduction (Tibola et al., 2016), while some others observed low DON reducing effects (Visconti et al., 2004). High variation
might be easier occur when targeted mycotoxin types usually occur with relatively low concentrations, like T-2/HT-2 and 3-
AcDON + 15-AcDON (Schwake-Anduschus et al., 2010; Matumba et al., 2015). Mass loss during cleaning and sorting is another
highly concerned topic in manufacturers’ eyes, since high mass loss might imply high financial loss. Most of the reviewed studies
observed mass loss lower than 8%, but high mass losses were also observed. For example, mass loss of hand sorting method studied by
Matumba et al. (2015) was 14%, and the study of Tibola et al. (2016) observed up to 33% mass lost. The high variation in hand
sorting methods’ decontaminating effects could be due to the inconsistent subjective judgment of workers. Tibola et al. (2016) also
declared it difficult to explain the high mass loss in their results, since it was impossible to record accurate mass balance of each step
138
Table 8
Average DON and ZON concentrations in unprocessed wheat and milled fractions, and the change rate of mycotoxin concentrations in milled fractions compared to
unprocessed wheat (Tibola et al., 2015).
Mill fraction Yield (%) DON ZEN
−1
Concentration (mg kg ) Change rate (%) Concentration (mg kg−1) Change rate (%)
−1a
Sample A: initial DON concentration before milling: 498.8 ± 29.3 mg kg
Finished flour 43.9 288.7 ± 4.2a −42.1b
Bran 626.3 ± 207.0a +25.6b
Sample B: initial DON concentration before milling: 746.5 ± 70.7 mg kg−1a

Finished flour 42.0 495.8 ± 36.1a −33.6b
Bran 870.0 ± 175.2a +16.5b
Sample C: initial DON concentration before milling: 1225.0 ± 90.0 mg kg−1a

Finished flour 43.2 787.0 ± 36.1a −35.8b
Bran 1752.5 ± 234.8a +43.1b
Sample D: initial DON concentration before milling: 2747.5 ± 140.8 mg kg−1a (with 27.6 ± 1.8 mg kg−1a ZEN co-occurring)
Finished flour 42.6 2157.5 ± 79.3 −21.5b NDc
Bran 3415.0 ± 212.1 +24.3b 62.6 ± 42.8a +127.2b
−1a −1a
Sample E: initial DON concentration before milling: 5985.0 ± 260.6 mg kg (with 38.7 ± 6.5 mg kg ZEN co-occurring)
Finished flour 40.1 5360.0 ± 331.4a −10.4b NDc
Bran 7407.5 ± 534.6a +23.8b 61.2 ± 158.2a +58.2b
a
b
Change rate indicates the mycotoxin concentration in milled fractions compared to that in initial unprocessed samples. ‘+’ represents the increase of con-
centration, and ‘−’ represents the decrease.
c
ND: Below the limit of quantification (< 20 mg kg−1).
in a continuous processing system.

Dehulling and milling processes also showed good mycotoxin reducing effects in reviewed studies. However, these two meth-
odologies have an obvious limitation: their mycotoxin reducing effects must give way to their main functions for feed manufacturing.
One evident example is the relationship between dehulling processing duration, remaining mass and remaining mycotoxin (House
et al., 2003; Rios et al., 2009b). Longer processing duration could lead to lower remaining mycotoxin, but processing duration is
always set stable in practical manufacturing situations in respect to production standards. On the other hand, milling process was
effective to reduce mycotoxin concentrations in fine mill fractions (e.g. semolina), but this does not mean that mycotoxin hazards
could be ignored in other mill fractions (e.g. break flours and reducing flours), which are commonly utilised for feed manufacturing.
In the study of Rios et al. (2009b), these mill fractions even contained higher mycotoxin concentrations compared to the raw samples.
Meanwhile, increased initial contaminating levels of grains also limit the reducing rate of these physical removal methods (Tibola
et al., 2015), so rejecting highly contaminated samples is a logical choice for feed manufacturers.
4. Thermal processes for mycotoxin reduction
Thermal processing has been widely utilized in feed manufacturing. It helps to increase feed quality by deactivating some mi-
crobes like Salmonella or transforming kernels’ physicochemical properties. In addition, anti-nutritional factors in cereals and legume
seeds can be significantly inactivated through thermal process (Qin et al., 1996). In this part, mycotoxin-reducing abilities of several
thermal processes are introduced.
4.1. Dry heating
Many mycotoxins are thermally resistant. For example, decomposing temperature of aflatoxins can be as high as 280 °C, and other
mycotoxins also have high thermal resistance (Table 9). Nevertheless, mycotoxin reducing effects of dry heating process were ob-
served in some studies. These effects are highly influenced by different factors, including processing duration, temperature and form
of processed grain samples. Yumbe-Guevara et al. (2003) studied the reduction of DON, NIV and ZEN in barley through superheating.
Table 9
Decomposing temperatures of some mycotoxins (Kabak, 2009).
Mycotoxins Decomposing temperature (∘C)
Aflatoxins 268–269
Ochratoxin A 169
DON 151–153
ZON 164–165
Fumonisins 100–120
139
Fig. 4. Effects of heating time and temperature on DON, NIV and ZEN reduction in: A) Standard solution; B) Naturally contaminated barley powder; C) Naturally
contaminated barley kernels. ○ 140 °C; ◆ 150 °C; ■ 160 °C; ▲ 180 °C; ◇ 200 °C; ● 220 °C (Yumbe-Guevara et al., 2003).
In this study, different processing temperatures and sample forms (standard solution, barley powder and barley kernels) were pre-
pared. As shown in the results, mycotoxins in some treatment groups were quite resistant, but reducing effects of superheating also
occurred to other groups and showed positive association with both temperature and processing time (Fig. 4). Moreover, this study
supported that sample particle size distribution influences the mycotoxin reducing effects of heating, since the barley powder in this
study achieved better mycotoxin reduction compared to the whole kernel samples (Fig. 4).
4.2. Superheated steam
Superheated steam is another effective thermal technology in feed/food manufacturing. Compared to conventional thermal
processing, superheated steam could bring less oxidation loss and higher energy efficacy to the manufacturing (Anto et al., 2014). An
effect of this technology is to bring high friability to kernels, which saves the time and energy in subsequent milling process. What
should be pointed out is that superheated steam technology may have drying effects to the samples even though high moisture is
involved. For example, prolongation of processing time at high temperature could dry the materials, while at low temperature it
might bring higher moisture to the samples (Pronyk et al., 2006). Besides this, depending on processing conditions (temperature and
moisture), starch will gelatinise.
Pronyk et al. (2006) studied the DON reducing effects in wheat kernels by using a superheated steam process. The results of this
study showed that the detoxifying effects of superheated steaming were positively associated with the processing duration and steam
temperature (experimental range: 110–185 °C). Speed of steam is a crucial interfering factor specifically for superheated steaming.
Fig. 5 was quoted from this study and clearly illustrates that linear results were hardly achieved in the reducing effects in DON
contaminated wheat when these factors (processing duration, steam temperature and speed) were all integrated. For example, high
steam temperature (185 °C) with sufficient processing time can reduce DON concentration by up to 50%, while no significant re-
duction effect was brought by most of the lower temperature groups (< 135 °C). So far, the reducing effects of superheated steam on
other mycotoxins, such as AFL, ZEN etc., are still in need.
4.3. Extrusion cooking
Extrusion cooking is a process that combines high-speed shearing and superheated steaming within a short time. This processing
step is usually applied to produce snack foods for humans, or pet food and fish diets. During this process, feed or food ingredients
successively experience physical powdering, super heating forming and cooling. Thus, several physical and chemical transformations
occur to the processed samples, including starch gelatinization, protein denaturation and microbial count reduction (Castells et al.,
2005). Several studies on mycotoxin reducing effects of extrusion cooking observed in samples with different initial contaminating
levels were published (Castells et al., 2006a,b) and targeted mycotoxins cover aflatoxins, fumonisins, DON and ZEN etc. (Table 10).
Higher processing temperatures during extrusion lead to a higher reduction of mycotoxins (Buser and Abbas, 2002; Katta et al., 1999;
Table 11; Figs. 6 and 7) but temperatures of 160° product temperature may have a negative effect on protein quality after extrusion.
With many influencing factors involved, the effects of extrusion detoxification indeed are less constant. For example, a study by
Castells et al. (2006a) showed that higher aflatoxin concentration unexpectedly occurred in the rice meal sample which was
140
Fig. 5. DON concentration in wheat samples treated by superheated steam respectively at: a) 185 °C, b) 160 °C, c) 135 °C, d) 110 °C. Two steam velocities were
supplied: 1.3 m/s and 0.65 m/s (Pronyk et al., 2006).
processed at higher temperature, even when other variables (residence time and initial moisture) were controlled (Fig. 8).
Extrusion cooking is a promising process for mycotoxin reduction, since it combines different processing methodologies including
shearing, making available the inner part of the grains, and heating (Bullerman and Bianchini, 2007). Moreover, the radicals formed
during the extrusion cooking (Ullsten et al., 2006; Schaich, 2002; Schaich and Rebello, 1999) may also have an effect on the
breakdown of mycotoxins.
4.4. Irradiation
Irradiation technologies are applied in feed and food industry usually because of their high efficiency to eliminate the micro-
organisms and other potential pathogens infecting the grains. Irradiation contains two types: non-ionizing radiation and ionizing
radiation. The non-ionizing radiation has a long wavelength and does not contain enough energy to ionize the atoms or molecules.
Radio, microwave and infrared ray are heat producing examples of non-ionizing radiation. Ionizing radiation is a by-product when
unstable atoms try to reach stability by giving out energy or mass or both, and it has short wavelength and high energy. With the
concern of radioactive contamination, only selected types of ionizing radiations are legally applicable in food or feed manufacturing
with detailed regulations in Europe, like gamma-radiation, X-rays and electron beams (EC, 1999a; EC, 1999b).
Both heating and hydrolysis are the main mechanisms involved with the mycotoxin reduction by irradiation. Heating effects of
irradiation methods were directly provided by high doses and long exposing time, and thus mycotoxin reducing effects of irradiation
are directly affected by these factors. A study performed by Herzallah et al. (2008) is quite informative. In this study, the non-ionizing
treatments (microwave and sunlight), which provides lower energy, showed much less efficient to reduce mycotoxins in chicken feed
samples, compared to gamma ray. Also, increase of exposing time of each treatment showed better reducing effects in the same study
141
Table 10
Publications on the mycotoxin decontamination effects of extrusion process (Not all authors provided the duration of process).
Mycotoxin Sample Type of extruder Additives Reduction (%)
FB1 Corn flour a

Single-screw None 66–92
Corn flourb Slot hot extruder None 26
Alkali-cooked corn flourc Twin-screw None 0–99
FB2 Corn flourb Slot hot extruder None 32
AFB1 Corn flourd Single-screw Control 45
0.3% Ca(OH)2 74
0.5% Ca(OH)2 85
0.75% H2O2 63
1.5% H2O2 64
3% H2O2 72
AFM1 Corn flourd Single-screw Control 20
0.3% Ca(OH)2 51
0.5% Ca(OH)2 82
0.75% H2O2 61
1.5% H2O2 74
3% H2O2 73
DON Corn floure Not reported Control 95–99.5
Na2S2O5
Wheat kernelsf Twin-screw NaHSO3 42–92
ZEN Corn gritsg Twin-screw None 66–83
OTA Wheat mealh Twin-screw None 8.3–42.2
Barley meali Single-screw None 17.5–86.5
a
Piñeiro et al. (1999).
b
De Girolamo et al. (2001).
c
Cortez-Rocha et al. (2002).
d
Elias-Orozco et al. (2002).
e
Cazzaniga et al. (2001).
f
Accerbi et al. (1999).
g
Ryu et al. (1999).
h
Scudamore et al. (2004).
i
Castells et al. (2006b).
Table 11
Effects of different processing temperature (°C) during extrusion on aflatoxin reduction (%)a in cottonseed (Buser and Abbas, 2002).
Processing temperature (°C) Remaining aflatoxin (ppb) Reduction (%)
104 182 ± 44 72.0 ± 6.7

132 137 ± 34 78.9 ± 5.2
160 117 ± 21 82.0 ± 3.2
a
Initial concentration: 650 ppb.
(Table 12). On the other hand, the hydrolysis effect of irradiation, where free radicals appear to reduce mycotoxins, occurs more
easily in aqueous conditions (He et al., 2010). For example, O’Neill et al. (1993) observed that DON and its derivative 3-A-DON in dry
maize kernels showed high stability even at 50 kGy (Gy is the SI unit of absorbed radiation) of gamma irradiation, while 5 kGy was
sufficient to drastically reduce these toxins in the aqueous solution (Fig. 9). In another study (Stepanik et al., 2007), evident dif-
ference of DON reducing effects between wet distillers grains (wet condition, Fig. 10), distillers solubles (wet condition, Fig. 11) and
distillers dried grain and solubles (dry condition, Fig. 12).
4.5. Summary of thermal methods for mycotoxin reducing
Mycotoxin reducing effects of four thermal methodologies were introduced in this part. Apart from high temperature, some other
different functions involved could contribute to mycotoxin reduction, like hydrolysis in irradiation technologies and kernel de-
formation in extrusion cooking. Like physical removal methods, thermal methods should have little specificity for mycotoxins, but the
practical reduction could still be affected by different thermal sensitiveness between mycotoxins. For example, aflatoxin B1 has
relatively high sensitiveness to gamma irradiation, and is thus easier to eliminate, compared to other mycotoxins (O’Neill et al.,
1993).
Some disadvantages of irradiation technologies could limit their promotion. First, extra costs conducted by manufacturers and the
public concern on chemical safety of ionizing irradiation are still limiting their application in food/feed manufacturing (Calado et al.,
2014). Second, negative nutritional changes could result from the irradiation treatments. For example, Ghanem et al. (2008) ob-
served a significant drop of oil content in the crop samples (including corn, pistachios, and peanuts) after gamma irradiation de-
graded existing mycotoxins, and the oil loss increased with higher gamma doses. Unsaturated bonds in fat can also be attacked by
142
Fig. 6. Fumonisin B1 reduction (%) in extruded corn cereal, with the presence of salt (%), barley malt (%) and sucrose (%). S = salt, M = malt (Castells et al., 2009).
Fig. 7. Effect of temperature during extrusion cooking on fumonisin B1 concentration in corn grit samples with different initial FB1 concentrations (Katta et al., 1999).
irradiation, which leads to changes in taste (D’Ovidio et al., 2007). Some vitamins (especially vitamin C, E, K and thiamin) and
proteins are also sensitive to irradiation (D’Ovidio et al., 2007). Third, whether mycotoxin ‘reduction’ is real ‘detoxification’ is still
doubtful, since thermal treatments could transfer mycotoxins into some undetectable derivatives with unknown toxicities. In con-
clusion, thermal technologies are not that ideal for mycotoxin reduction in feed manufacturing.
5. Chemical methods for mycotoxin reduction
Some chemicals are effective to reduce the mycotoxins. Generally, chemical methods have some advantages in mycotoxin re-
duction, including high reducing efficiency and relatively low cost. Different mechanisms are involved with the mycotoxin reducing
effects of these chemical methods, including alkalization, oxidation, reduction, hydrolysis, hydration and conjugation (He et al.,
2010). However, most of these chemical methods have been concerned due to consumers’ health. Currently, application of chemical
treatments for mycotoxin reduction has been banned in feed/food materials by European Commission (2006b). In this review, only
two main chemicals (ammonia and ozone application) are discussed. One typical chemical with mycotoxin reducing effects is am-
monia. The other chemical is ozone, which is famous for the super oxidizing ability. In practice, both products are in either liquid or
gas form, and could be applied because of their excellent effects to eliminate zoonotic bacteria in feedstuffs (Tajkarimi et al., 2008;
McKenzie et al., 1998).
143
Fig. 8. Effects of extrusion processing with different processing temperature (°C), residence time (s) and initial moisture (A and B) on aflatoxin B1 reduction in rice
meal (Castells et al., 2006a). Five bars of different colours represent different residence times (second); ‘A’ represents the samples initially with 24% moisture, and ‘B’
represents the samples initially with 27% moisture.
Table 12
Effects of different irradiation types on AB1 reduction.
Sample Irradiation Dose (kGy) Duration Reduction (%)
a 60
Wheat bran Co gamma ray 4 52.9
6 75.5
10 86
Corna 4 31.2
6 72.1
10 84.2
Barleya 4 45.0
6 66.2
10 89.9
Peanuta 4 8
6 28.5
10 58
Coconut agarb Electron beam 5 75.5
Chick feedc 60
Co gamma ray 5 6.3–10.5
10 12.8–21.9
15 18.3–37.3
Microwave 4 min 3.6–14.9
8 min 7.1–28.6
10 min 21.2–33.3
Sunlight 3h 39.8–42.3
9h 49.9–56.4
30 h 60.4–75.5
a
Ghanem et al. (2008).
b
Rogovschi et al. (2009).
c
Herzallah et al. (2008).
These two chemicals were also applied for mycotoxin decontamination. One in vitro study (Young et al., 2006) found that aqueous
ozone is highly effective to reduce pure trichothecene mycotoxins (including DON, 3ADON, 15ADON, T2, HT2 etc.) under laboratory
conditions, and the reducing effects were positively related with the applied amount of ozone, which is related to both the con-
centration of ozone and the exposing time. In situ mycotoxin reducing effects of these chemicals were also supported by studies, and
their decontaminating effect can be influenced by many factors. First, they can be influenced by the initial mycotoxin contaminating
degree. In the study of Savi et al. (2014), ozone successfully reduced DON level in wheat pericarp by 86.6% within 30 min, but was
144
Fig. 9. Different degradation effects on DON by gamma irradiation in dry maize or aqueous solution (O’Neill et al., 1993).
Fig. 10. Effect of electron beam with different doses on DON concentrations in wet distillers grains (Stepanik et al., 2007).
Fig. 11. Effect of electron beam with different doses on DON concentrations in distillers solubles (Stepanik et al., 2007).
much less efficient to reduce the DON in wheat endosperm. Since endosperm originates from the inner parts of grains, the rich lipid in
that parts could be a reason to grasp this lipo-soluble toxin firmly (Table 13).
On the other hand, levels of heat and moisture during the chemical treatment may be positively associated with the effects of
145
Fig. 12. Effect of electron beam with different doses on DON concentrations in distillers dried grain and solubles (Stepanik et al., 2007).
Table 13
Effects of ozone and ammonia treatments on mycotoxin reduction.
Mycotoxins Samples Chemicals Duration (min) Moisturec (%) Temperature (°C) Reduction (%)
DONa Wheat pericarp Ozoned 30 86.6

60 86.6
120 100
Wheat endosperm Ammoniae 30 20.8
60 34.0
120 100
Aflatoxin B1b Ground corn Ammoniaf 60 12 40 64.9
16 40 93.1
60 12 25 17.5
12 121 99.8
a
Savi et al. (2014).
b
Weng et al. (1994).
c
Initial moisture of samples.
d
In the gaseous form.
e
Gaseous NH3 (%2).
f
Aqueous NH4OH (2%).
these treatments. For example, In the study of Weng et al. (1994), higher initial moisture in ground corn largely increase the
reduction of aflatoxin B1 by aqueous NH4OH. In the same study, aqueous NH4OH could decrease aflatoxin B1 by 99.8%, while only
17.5% aflatoxin B1 was eliminated at 25 °C (Table 13). Third, chemicals show different detoxifying effects when targeting different
mycotoxins. For example, ammonia (either gas or liquid) shows good effects to reduce aflatoxins in samples, but is less effective to
deal with Fumonisins and DON (Jouany, 2007).
Feeding experiment also supported the detoxifying effects of these chemical treatments. An in vivo study on broiler chicks by
Allameh et al. (2005) observed that the adverse effects of aflatoxin-contaminated maize could be controlled after the ammonia
treatment (vapours with 1% ammonia), and the growth performance, organ conditions and the serum biochemical parameters of
chicks fed with the treated diet were comparable to the control group which was fed with uncontaminated grains. The compensating
effects of ozone were also observed in another in vivo study, where turkeys were fed with aflatoxin-contaminated corn (McKenzie
et al., 1998).
These chemical treatments for decontaminating mycotoxins also have their limitations. First, the toxicities of the mycotoxin
metabolites resulting from these chemical treatments are still threatening, since, for example, some intermediate compounds ori-
ginating from aflatoxin B1 treated by ozone or ammonia, including aflatoxin D1 and aflatoxin ozonide, could still have toxicity
(Tiwari et al., 2010; McKenzie et al., 1998) (Fig. 13). Second, these chemical treatments may change the quality of materials. These
changes include surface oxidation, colour changes, impaired taste, reduced germination energy, and extra energy could be required in
following milling processing (Tiwari et al., 2010). In the study of Savi et al. (2014), germination capacity of wheat grains was reduced
by 12.5% after 180 min of ozone exposure compared to the untreated grains, but no similar impairment was observed in the samples
whose exposure lasted for 120 min. Since chemical treatments for mycotoxin reduction in food or feed materials have been banned,
studies on chemicals’ mycotoxin reducing effects were gradually less published in this century (He et al., 2010).
6. Biotransformation of mycotoxins
Apart from the inorganic or organic binding agents introduced above, mycotoxin controlling ability of some microbes was also
noticed. These methods use biologically transformation to reduce or eliminate mycotoxins as reviewed by He et al. (2010) and
146
Fig. 13. General chemical transformation flow chart of aflatoxin B1 treated by ammonia or ozone (McKenzie et al., 1998).
Vanhoutte et al. (2016).

He et al. (2010) summarize the following advantages of biotransformation:
– specificity towards less or non-toxic ingredients

– mild reaction conditions (temperature; pH)
– application under aerobic and anaerobic conditions
– potential application of detoxifying enzymes
Some microbes can turn mycotoxins into less toxic or non-toxic derivatives by transforming their physical and chemical char-
acteristic. These materials were usually isolated from natural sources, like crop tissues, soil, and in vivo microbial (Heinl et al., 2010).
One example is the reductive de-epoxidation of trichothecenes of microbes in the hindgut of pigs and poultry. In this process, the
transformation of epoxide groups, which determines the toxicity of trichothecenes, leads to less toxic products (Wu et al., 2007).
These natural detoxifying microbes occurring in animal GI tracts seem to be adaptive. For example, DON or NIV could not be
detoxified in animals which have never been exposed to trichothecenes before (Karlovsky, 2011).
However, these microbes may function well only when their strict environment requirements are met. For example, the bacteria
that can detoxify trichothecenes by de-epoxidating are observed to be active only under anaerobic environment (Karlovsky, 2011).
Some enzymes involved in detoxification need NADPH (Hassan et al., 2017) or other co-factors which limit their practical application
as an enzyme solution.
This situation makes the application of these microbes as animal feed additive quite complicated. Thus, biological feed additives
can represent alternative detoxification methods but are still in their infancy and need breakthroughs.
7. Mycotoxin-binding by feed additives
In 2009, the European Commission extended their definition of ‘feed additives’ to include materials that ‘suppress or reduce the
absorption of mycotoxins, promote the excretion of mycotoxins or modify their mode of action and thereby mitigate possible adverse
effects of mycotoxins on animal health’ (EC, 2009). Academic studies on feed additives to reduce mycotoxins in feed were performed
long time ago. Unlike the physical removal, thermal or chemical methods which focus on how to reduce mycotoxins in the in-
gredients during the feed manufacturing stage, these feed additives were designed to reduce the potential adverse effects of my-
cotoxins after the feed is ingested by animals. Main mycotoxin-restricting mechanisms involved with these additives include: 1)
physically binding the mycotoxins and thus decreasing the gastrointestinal absorption of mycotoxins; 2) inactivating mycotoxins; 3)
modifying animals’ enzymes to transform mycotoxins into some less toxic metabolites or improve animals’ defence against mycotoxin
(Meissonnier et al., 2009). Below, mycotoxin restricting effects of several feed additive products are introduced.
7.1. Inorganic binding agents
Binding agents are a group of feed additives which function to block the absorption of mycotoxins in gastrointestinal tracts of
animals by physically binding these toxins. Main examples of inorganic binders for mycotoxins include hydrated sodium calcium
aluminosilicates (HSCAS), activated coat (AC), montmorillonite clays (MC), etc. (Avantaggiato et al., 2005). Absorbing effects of
these inorganic binding agents are based on the physical and chemical structures of both the agents and the mycotoxins, and these
binding agents usually have their own specific repertoire of target mycotoxins. For example, AFL, which contain polar functioning
147
Table 14
Body weight, feed conversion rate (FCR) and mortality of chicks1,2,3 from 0 to 6 weeks old, provided with 4 different diets (Bailey et al., 2006).
Diet Weight (g) FCR Mortality (%)
Phase 1: week 1–3

Aflatoxin (3600 ppb) 330.1d 2.05a 16.5a
Aflatoxin (3600 ppb) + MC 338.7c 1.95a 13.0a
Control 732.6a 1.33b 3.5b
Control + MC 701.3b 1.33b 6.0b
Phase 2: week 4–5

Aflatoxin (3600 ppb) 566.4c 1.91a 15.2a
Aflatoxin (3600 ppb) + MC 759.8b 1.72b 6.9b
Control 1134.9a 1.66b 1.6c
Control + MC 1028.1a 1.68b 0.5c
Phase 3: week 6
Aflatoxin (3600 ppb) 318.9c 2.32a 9.2a
Aflatoxin (3600 ppb) + MC 424.5b 2.18ab 4.2b
Control 550.3a 2.08ab 0.5c
Control + MC 592.8a 1.98b 1.1bc
Cumulative for 6 weeks
Aflatoxin (3600 ppb) 1215.5c 2.01a 36.0a
Aflatoxin (3600 ppb) + MC 1565.0b 1.89b 22.5b
Control 2417.8a 1.65c 5.5c
Control + MC 2376.2a 1.65c 7.5c
a–d
Values with a different superscript within a column differ significantly (P < 0.05).
1
All values represent the average of 10 pens.
2
MC = montmorillonite clays.
3
The added MC is 0.5% of the total feed.
groups, are easier to be absorbed by MC than the non-polar ZEN and OTA (Kabak et al., 2006). Among these inorganic binders,
bentonite (an absorbent aluminium phyllosilicate clay) receives the support from European Commission (2013, No 1060/2013) as an
effective feed additive to bind mycotoixns, especially aflatoxins.
An ideal mycotoxin binding agent should: 1) be harmless to the animal health and productive performance, 2) rapidly produce
stable detoxified mycotoxin-absorbent complex before mycotoxins enter the blood, 3) be effective to different mycotoxin con-
centrates under various environments of the entire GI tract, 4) be environment-friendly after excreted out of animal bodies (Jard
et al., 2011). Roughly, these agents can be divided into two groups, inorganic and organic, based on their physicochemical char-
acteristics. A long-term study (Bailey et al., 2006) on the protecting effects of dietary calcium montmorillonite clays (MC) was
performed on chicks for the entire 6 weeks after hatchery (first 3 weeks as ‘new-born’, then 2 weeks as ‘grower’ and last 1 week as
‘finisher’) (Table 14). Four diet types were set: A) diet contaminated with 3600 ppb of aflatoxin; B) diet contaminated with 3600 ppb
of aflatoxin, and containing 0.5% MC; C) control diet without aflatoxin contamination; D) diet without aflatoxin contamination, but
containing 0.5% MC. In this experiment, both the health statue and the growth performance were analysed through recording several
parameters, including mortality, feed intake, body weight gain, and weights of some organs. In the comparison of groups offered with
diet A and B, MC showed limited effects to reduce the mortality of new-born chickens poisoned by aflatoxin, but the weight in group
B was still higher than that of group A, which indicated the compensating effects of MC. Compared to the youngest chicks, the
compensating effects on the weight gain and mortality reduction became greater in older chicks. On the other hand, the MC diet
seemed to reduce the weight gain of new-born chicks, even though this adverse effect became less evident in the older chicks.
Moreover, the drastically increased weight of (both A and B) finisher’s liver, kidney and spleen indicated that MC failed to protect
these organs from the high level of aflatoxin (much higher than EU requirement, Table 2) in this experiment (Table 15). In similar
studies, activated coat failed to prevent weaning pigs from the poisoning of fumonisin B1 (Piva et al., 2005), and the diatomaceous
earth (DE) also failed for boilers fed aflatoxin contaminated diets (Modirsanei et al., 2008). Results of these experiments indicate that
the effects of inorganic binders are limited.
Table 15
Relative weights of organs in bodies of sacrificed finisher chicks (Bailey et al., 2006).
Relative weight (%) Aflatoxin Aflatoxin + MC Control Control + MC
Liver 4.56a 4.00b 1.90c 1.96c

Kidney 1.50a 1.11b 0.56c 0.60c
Spleen 0.22a 0.2 a 0.12b 0.12b
a–c
values with a different superscript within a row differ significantly (P < 0.05).
148
Table 16
Aflatoxin B1 binding abilities of strains of yeasta and lactic acid bacteriab (Shetty and Jespersen, 2006).
Isolates Quantity of mycotoxin binding strains
Percentage of binding
< 15 15–39 40–59 ≥60
Yeasta Saccharomyces cerevisiae 1 8 3 3

Candida krusei 4 5 1 1
Saccharomycodes ludwigii 0 0 1 0
Lactic acid bacteriab Lactobacillus plantarum 0 0 4 1

Lactobacillus fermentum 0 0 0 1
Selangorensis 4 1 0 0
a
For all the yeast strains, 108 cells were incubated in 1 ml of PBS containing 5 mg of aflatoxin B1 for 72 h at 25 °C.
b
For all the lactic acid bacteria strains, 109 cells were incubated in 1 ml of PBS containing 5 mg of aflatoxin B1 for 72 h at 25 °C.
7.2. Organic ‘binding agents’
Some organic materials also work effectively to ‘bind’ mycotoxins. One of the earliest organic binders dealing with mycotoxins
might be the extractions from some fibre-rich plants (e.g. oat and alfalfa) (Jouany, 2007). Currently, the most noticed organic binder
now is the yeast cell wall. Even though earlier researchers had noticed that live yeast Saccharomyces cerevisiae can effectively suppress
adverse effects of some mycotoxins (e.g. aflatoxins) in animals (e.g. chicks) (Stanley et al., 1993), the earliest in vitro study which
found the mycotoxin binding function of cell wall of yeast Saccharomyces cerevisiae was performed by Devegowda and colleagues in
1998, as reviewed by Jouany (2007).
Shetty and Jespersen (2006) performed a laboratory study on the aflatoxin B1 binding abilities of isolates from different yeast or
lactic acid bacteria strains (Table 16). In their study, one group of isolates from western African maize, Saccharomyces cerevisiae were
observed with best effect to bind over 60% of aflatoxin, but other strains performed much less effective.
Apart from the simple physical absorbing effects, some other mycotoxin controlling mechanisms are also involved with these
organic ‘binders’. For example, major fractions of dry yeast cell wall are two polysaccharides: β-D-glucan and α-D-mannan, and the
mycotoxin binding function is directly involved with β-D-glucan (Kogan and Kocher, 2007; Jouany, 2007). Apart from binding
mycotoxins, these polysaccharides also supply other effects to control mycotoxins’ harm in animal bodies, including modulating
immune activities and binding gastrointestinal bacterial pathogens (Kogan and Kocher, 2007). Meissonnier et al. (2009) specifically
studied the immuno-modulating effects of glucomannan of dry yeast cell wall. In this study, weaned pigs were exposed to different
levels of aflatoxin B1 or T-2 for 28 days. The glucomannan added for some diet groups evidently decreased the severity of liver
damages and delayed the impairing of immune reactions. Main mechanisms could be that dietary glucomannan stirred the pro-
liferation of immune enzymes and immunoglobulin G, even though these protective effects might be relatively limited.
7.3. Summary
With the banning (EC, 2006a,b) of chemical mycotoxin-decontaminating methods in feed manufacturing, safer methodology for
mycotoxin controlling in feed are needed in recent decades. Mycotoxin binding agents are gradually noticed in this context. Different
from other methodologies, binding agents mainly function when mycotoxin contaminated diets are ingested by animals. Thus, the in
vivo effects of these additives are crucial. These binding agents are roughly classified as ‘inorganic’ and ‘organic’ ones. Inorganic
binders were found to have effects to compensate the impacts of mycotoxins in animal diets, and they have been widely noticed and
partly applied by local farmers because of their low costs and high operability. Organic binding agents may have other positive
functions, like binding other pathogens and improving animal’s immunity, which indirectly help to control mycotoxin hazards.
These feed additives also have some disadvantages. Generally, efficacy of the inorganic products is usually low. With both low
costs and low efficacy, these inorganic binders are sometimes added into feed at large amount by farmers, which may decrease the
total nutritional values of feed (Karlovsky, 2011). In addition, they could bind other nutritional factors like vitamins and trace
elements, bringing nutritional imbalance to animals. Some binders, like clay, show low toxicity in animals. They might also contain
other negative effects like interrupting nutrient metabolisms, and impairing animal organs. Relatively low natural degradation of
inorganic binders also leads to ecological problems after they are excreted out of animals. Even though the organic feed additives
could exclude the disadvantages of the inorganic ones, highly varied inner environments (e.g. pH) of animal GI tracts can greatly
affect the efficacy of these biological treatments (Karlovsky, 2011).
In conclusion, feed additives for mycotoxin detoxifying through binding are useful in current animal feed practice but still less
from ideal.
149
8. Discussion
8.1. Limitations of current strategies
Despite these strategies have been observed to be effective for mycotoxin controlling, several problems and limitations of some of
them are still need overcoming.
First, an evident limitation is the heterogeneity observed in different studies. One type of heterogeneity is the experimental
conditions. For example, several studies noticed that some experimental conditions could affect the mycotoxin reducing effects of
extrusion cooking, including type of processing machine (Castells et al., 2005), crop breeds and places of origin (Schwake-Anduschus
et al., 2010; Tibola et al., 2016), presence of special ingredients (e.g. sugar, salt) during processing (Castells et al., 2009). Never-
theless, most studies reviewed usually neglected to emphasize the potential impacts of these variables. The other heterogeneity is the
initial contaminating levels of feedstuffs. Mycotoxin contamination mainly accumulates on the surface or shallow parts of a single
kernel, but contamination may also occur in deeper parts when the level of fungal activity rises. Take Fusarium graminearum, when
this mycotoxigenic mould infects cereal grains, the brush hair at the kernel’s tip is the most rapid entrance, which is followed by quite
a slow development into deeper parts, and the endosperm is the eventual target (Skadsen and Hohn, 2004). Among the reviewed
studies, some on the mycotoxin redistributing effects of milling noticed the impact of different levels of initial contamination and
grant it as an experimental variable (Rios et al., 2009b; Tibola et al., 2015), while others did not focus on this variable.
The second limitation is the unclear toxicity of mycotoxin derivatives. One typical problem is the ‘masked mycotoxin’. Generally,
this term ‘masked mycotoxin’ covers those mycotoxin derivatives which are undetectable by some conventional analytical methods,
because of their changed structure compared to the parent toxins (Berthiller et al., 2013). Masked mycotoxins can result from feed/
food processing. For example, amount of deoxynivalenol-3-D-glucopyranoside (D3G) increases after malting of barley grains
(Berthiller et al., 2013). Also, thermal treatments could transfer DON into masked mycotoxins, like D3G (Kostelanska et al., 2011). On
the other hand, one mycotoxin can be transferred into various ‘masked mycotoxins’, which increases the uncertainty of food or feed
safety. For example, through conjugation, DON occurring in some crops can be transferred into less toxic D3G, while through
acetylation DON can be turned into 3-acetyl-DON (3ADON) and 15-acetyl-DON (15ADON) (Berthiller et al., 2013). Till now, more
and more ‘masked mycotoxins’, originating from DON, ZEN, T-2, HT-2, fumonisins, OTA, etc., have been gradually discovered
(reviewed by Berthiller et al., 2013). This issue of the unknown toxicological information brings some warnings to the current
knowledge of mycotoxin reduction. First, the mycotoxin reducing effects of some methodologies should be examined again, espe-
cially thermal and chemical methods, which could produce the toxic derivatives from common mycotoxins. Second, current legal
systems on food/feed safety might not take the new toxicological development into account. For example, α-zearalenol (α-ZEL), a
much less detectable derivate of ZEN, can result in more severe estrogenic effect than its precursor, but no current regulation has been
proposed to control its presence in food or feed processing (Urraca et al., 2004).
The final problem discussed is the limited applicability of some reviewed mycotoxin controlling methods in practical feed
manufacturing. Typical examples include the banning of the chemical methods and ionizing irradiation, which shows distinguishable
mycotoxin reducing effects, but raises public concern towards the safety of treated food/feed materials. Furthermore, costs of my-
cotoxin reducing strategies are always an important factor considered by manufacturers. High costs of some methods, like liquid
flotation and hand sorting, directly restrict their applicability in large scale manufacturing situations. Advances in automation and
digital processing could in the future help to make this a viable option. For those strategies that are applicable in feed manufacturing,
their mycotoxin reducing effects may interfere with the desired product quality. For example, the mycotoxin reducing effects of
dehulling could be increased when longer duration takes away more outer parts of seeds or hulls, but duration of dehulling is set,
based on the time requirements of production, a reason why mycotoxin reducing effects of dehulling could be marginalized. Due to
similar logics, mass loss of materials is a crucial factor to judge the applicability of cleaning and sorting methods, since low mass loss
could indicate low economic loss. For example, the high mass loss (> 28%) in one reviewed study could bring high extra costs and
thus be less acceptable from the aspect of feed manufacturers, regardless of the high mycotoxin reducing effects (> 74%) (Table 4,
Tibola et al., 2016).
Detoxification methods by using biotransformation agents certainly have future possibilities on the condition they are well
identified for their degradative ánd detoxification effects. This means that they have to be examined at the same time for the toxicity
of their metabolites. Multiple mycotoxin degradation should have a priority in research, since agents claiming mycotoxin detox-
ification are not always effective against other, non-related mycotoxins (Vanhoutte et al., 2016). The same authors invite researchers
to examine the biodegradation of mycotoxins by microorgansims.
8.2. Recommendations
With the comprehensive consideration achieved through this review, several recommendations for feed manufacturers to control
mycotoxin hazards could be proposed.
First, physical removal strategies are the most recommended, because they contribute to reducing the existing fungi and my-
cotoxins of little specificity, and less tend to result in the synthesis compared to chemical and thermal methods. Among the physical
methods, cleaning and sorting is necessary in most situations because of its function to eliminate not only mycotoxin but also other
contaminants. In comparison, dehulling may be more narrowly applicable, since they can only function on limited range of seed
species like legumes, and these seeds are relatively less contaminated by mycotoxins. As introduced above, the milling process is only
to redistribute mycotoxins into different mill fractions. Even though this process could result in low mycotoxin concentrations in the
150
finest fractions, the mycotoxin hazards could be still shrouding other mill fractions like brans, which are often reutilized for animal
feed products. Thus, potential mycotoxins in these by-products should be examined.
Second, thermal methods generally show limited mycotoxin reducing effects, and is less recommended than physical removal
methods. The costs of different thermal methods are highly diverse, which could be an important factor influencing the applicability
of each thermal method in practical manufacturing. Cheap methods, like IR, seem less effective towards mycotoxins, while some
methods showing evident mycotoxin controlling effects, like gamma irradiation, are costly. In addition, it is still doubtful whether the
‘decreased’ mycotoxins are transferred into undetectable toxic derivatives, like masked mycotoxins.
Third, chemical treatments (not meaning enzymatic), without doubts, are banned by legislatives. In comparison, mycotoxin
reducing effects of some feed additive products seem more promising, especially after some of these products were officially included
as ‘feed additives’ (EC, 2013). Some in vitro studies supported their potential to detoxifying contaminated feedstuffs, but their actual
functions in animal bodies still need more proof.
Generally, these products’ mycotoxin controlling effects are generally low and inconsistent. It is also challenging for them to
function well through the complicated inner environments of GI tracts with little harm to the animals (Le Thanh et al., 2016). The
first results to detoxify DON in vivo are promising (Starkl et al., 2015).
9. Conclusions
Among the different mycotoxin reducing methods, we should not declare that one individual method is unconditionally effective
to eliminate mycotoxin contamination in crops or to prevent the consequent impacts on animal health. The prevention strategies and
cleaning and sorting methods are widely applied because they work as first-line barriers to free the materials from various con-
taminants, including mycotoxins. However, mycotoxin reducing effects of other feed manufacturing technologies, like milling, de-
hulling and thermal methods, could be inconsistent and limited by various practical conditions. In addition, the evident reducing
effects of some physical removal methods requires the costs of high grain mass loss, which could be a dilemma from the aspect of
practical manufacturing. Feed additive products specifically against mycotoxins are promising but still in their babyhood, since in
vitro functioning of some products are inconsistent, and their in vivo functioning need more proof.
As for biotransformation, understanding the reaction for the detoxification of mycotoxins, attention in research on the toxicity of
transformation by enzymes and their end-products (He et al., 2010; Vanhoutte et al., 2016) should emphasize the possibilities of the
use of micro-organisms or enzymes towards safe properties in animal feed ingredients.
Thus, this literature review generally agrees with the discussion of Jouany (2007): ‘Prevention strategies are essential, since it is
impossible for other technologies to completely decontaminate the mycotoxin-contaminated feed samples once they are present’.
Conflict of interest statement
No conflict of interest.
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Animal Feed Science and Technology 237 (2018) 129–153

Contents lists available at ScienceDirect

Animal Feed Science and Technology

Strategies to prevent and reduce mycotoxins for compound feed

1.1. Overview: mycotoxins

Mycotoxin Main origin Host crop Main adverse eﬀects

1.2. Most detected mycotoxins in feed manufacturing

1.3. Growing impacts of mycotoxins on animal production system

Mycotoxin Products Regulated maximum level Guidance Value (mg/kg,

Aﬂatoxin B1a All feed materials 0.02

Mycotoxin Cascade of cellular events

2. Prevention strategies against mycotoxin contamination

2.1. Pre-harvest prevention

2.2. Post-harvest prevention

3. Physical removal of mycotoxins by feed manufacturing technologies

3.1. Cleaning and sorting

Samples Conditions Mycotoxin Reduction (%) Mass Loss (%)

Samples Conditions Mycotoxins Reduction (%) Mass loss (%)

Sample Mycotoxin Dehulling duration Reduction Mass loss

Barleyb DON 15 s 66% 15%

Total semolina 76.4 40.8 199.3 ± 62.0a

Total semolina 75.9 49.6 3015 ± 632.6a −78.4b 21.0

3.4. Summary of physical removal methods

Mill fraction Yield (%) DON ZEN

Sample B: initial DON concentration before milling: 746.5 ± 70.7 mg kg−1a

Sample C: initial DON concentration before milling: 1225.0 ± 90.0 mg kg−1a

in a continuous processing system.

4. Thermal processes for mycotoxin reduction

4.1. Dry heating

Mycotoxins Decomposing temperature (∘C)

4.2. Superheated steam

4.3. Extrusion cooking

Mycotoxin Sample Type of extruder Additives Reduction (%)

FB1 Corn ﬂour a

Processing temperature (°C) Remaining aﬂatoxin (ppb) Reduction (%)

104 182 ± 44 72.0 ± 6.7

4.5. Summary of thermal methods for mycotoxin reducing

5. Chemical methods for mycotoxin reduction

Sample Irradiation Dose (kGy) Duration Reduction (%)

DONa Wheat pericarp Ozoned 30 86.6

Vanhoutte et al. (2016).

– speciﬁcity towards less or non-toxic ingredients

7. Mycotoxin-binding by feed additives

7.1. Inorganic binding agents

Diet Weight (g) FCR Mortality (%)

Phase 1: week 1–3

Phase 2: week 4–5

Relative weight (%) Aﬂatoxin Aﬂatoxin + MC Control Control + MC

Liver 4.56a 4.00b 1.90c 1.96c

Isolates Quantity of mycotoxin binding strains

< 15 15–39 40–59 ≥60

Yeasta Saccharomyces cerevisiae 1 8 3 3

Lactic acid bacteriab Lactobacillus plantarum 0 0 4 1

7.2. Organic ‘binding agents’

8.1. Limitations of current strategies

Conﬂict of interest statement

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