Mini-review

Received: 16 September 2008 Revised: 19 November 2008 Accepted: 19 November 2008 Published online in Wiley Interscience: 6 January 2009

(www.interscience.wiley.com) DOI 10.1002/jsfa.3491

The fate of mycotoxins during thermal food

processing
Bulent Kabak∗

Abstract
Mycotoxins are considered to be heat-stable molecules. Because of their toxic effects, information about their stability in
thermal processes and potential inactivation procedures is needed. Numerous reports in the literature over a number of years
have described the fate of mycotoxin during thermal food processing, including cooking, boiling, baking, frying, roasting and
pasteurization. This review focuses on the effects of various thermal treatments on mycotoxins, while the fate of mycotoxins
during extrusion processing, which is one of the most important technologies employed in the food industry, will also be
reviewed.

c 2009 Society of Chemical Industry

Keywords: mycotoxins; thermal food processing; extrusion; detoxification

INTRODUCTION the moisture content, pH and ionic strength of food, among other
Mycotoxins are fungal secondary metabolites that are known factors, play a significant role in the degree and extent of toxin
for severe toxic effects on vertebrates and which are produced degradation.6,7 The effects of various thermal treatments on the
by many important phytho-pathogenic and food spoilage fungi, most important mycotoxin groups will be now be reviewed.
including Aspergillus, Penicillium, Fusarium and Alternaria species.
The Food and Agricultural Organization (FAO) has estimated Aflatoxins
that up to 25% of the world’s food crops are significantly
Aflatoxins have high decomposition temperatures, ranging from
contaminated with mycotoxins.1 From both a public health and
237 to 306 ◦ C.7 Even though aflatoxins are highly stable to dry heat-
agronomic perspective, the most significant mycotoxins include
up temperatures (melting point of 268–269 ◦ C), some attempts
the aflatoxins, ochratoxin A (OTA), fumonisins, deoxynivalenol
have been made to inactivate aflatoxins in various food products. It
(DON or sometimes called vomitoxin) and zearalenone (ZEA).2
has been reported that temperatures above 150 ◦ C are required to
However, there has been much recent interest among researchers
attain partial destruction of the toxin.6 Cooking and/or processing
in other mycotoxins such as moniliformin (MON), patulin, T-2 and
of feed has been shown to result in reductions of up to 41%
HT-2 toxin. These toxins can be formed not only during the growth
in aflatoxins B1 (AFB1 ) and B2 (AFB2 ) levels.8 In addition, either
of the crop but also during storage, as a result of bad storage
boiling or frying maize grits has been shown to lead to an average
conditions or during treatment of the products before they enter
of 28% and 34–53% reduction in AFB1 levels, respectively.9 The
the market. Failure to prevent fungal growth and toxin production
reduction of aflatoxin contamination in rice has been evaluated,
in the field or in storage will inevitably lead to a health risk to
during normal cooking and cooking with excess water, with
the consumer, together with often quite severe economic losses.
reductions of up to 89% of the initial toxin levels present being
It is therefore very important to know the stability of the various
reported.10 It has been suggested that the presence of moisture
mycotoxins during various thermal food-processing processes.
in foods helps in opening the lactone ring in AFB1 , allowing the
The application of heat to cook and preserve products is the basis
formation of a terminal carboxylic acid, which then undergoes
of all thermal processes. Thermal treatments currently employed
a heat-induced decarboxylation.6 In another study, Park et al.11
include ordinary cooking, boiling, baking, frying, roasting, canning
reported that the cooking of naturally contaminated rice with
and extrusion.3 Among these processes, extrusion processing,
AFB1 causes an average 34% reduction in AFB1 levels. Even further
which is receiving increasing interest, will be critically reviewed
reduction (78–88%) can be achieved following pressure cooking.
separately in this paper.
with reductions in aflatoxin-induced mutagenic potential ranging
from 68% to 78%.12
THERMAL PROCESSING The traditional nixtamalization (alkaline-cooking) process in-
volving cooking and steeping maize, which is used to manufacture
Most mycotoxins are heat-resistant within the range of conven-
tional food-processing temperatures (80–121 ◦ C), so little or no
reduction in overall toxin levels occurs as a result of normal
∗ Correspondence to: Bulent Kabak, Department of Food Engineering, Hitit
cooking conditions such as boiling and frying, or even following
University, TR-19030, Corum, Turkey.
pasteurization.4,5 The initial level of contamination, the type and
E-mail: [email protected]
concentration of the mycotoxin, the heating temperature together
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with the time employed, the degree of heat penetration as well as Department of Food Engineering Hitit University, TR-19030, Corum, Turkey

J Sci Food Agric 2009; 89: 549–554 www.soci.org

c 2009 Society of Chemical Industry
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tortillas in Latin America, has been shown to result in the elimina- OTA in wheat was evaluated by Boudra et al.,31 who showed that
tion of 51.7%, 84.5% and 78.8% of the aflatoxin content of tortilla, at 100 ◦ C there was no change after 40–160 min of dry heating,
tortilla chips and maize chips, respectively.13 In another report, whereas upon wet heating at the same temperature over 50% of
this traditional nixtamalization process reduced levels of AFB1 by OTA was destroyed after 120 min. Additionally, pressure cooking
94% and AFB1 -8,9-dihydrodiol by 93%.14 beans in water resulted in up to a 84% reduction in OTA.32 The
Roasting is considered one of the most effective methods of cooking of rice in excess water resulted in a 86% reduction in OTA
reducing aflatoxin levels in certain commodities, such as peanuts levels, while an average of 83% loss was observed during normal
and coffee in particular, with average reductions in the aflatoxin cooking.10
content of peanuts ranging from 45% to 83% following dry The thermal decomposition products of OTA have also been
roasting being reported.15 Pluyer et al.16 have reported that oven described; at high temperatures (250 ◦ C), partial isomerization
roasting of naturally contaminated peanuts at 150 ◦ C for 30 min of OTA at the C3 position takes place during the roasting
causes a 30–45% reduction in aflatoxin levels, with 48–61% process of coffee beans, resulting in the formation of a less
reduction in AFB1 levels in artificially contaminated peanuts being toxic diastereomer.24 In another report, two fluorescent products
achieved under the same conditions. These differences can be have been observed on heating OTA at higher temperatures
explained by the increased availability of aflatoxins in spiked (200–250 ◦ C) in dry wheat samples.33 It should be remembered,
samples to degradation by heat. In another study, Yazdanpanah however, that the disappearance of OTA does not necessarily
et al.17 reported that the roasting of pistachio nuts at 90, 120 and mean an absence or indeed a decrease in toxicity risk, as the
150 ◦ C for 30, 60 and 120 min reduced the aflatoxin content of decomposition product(s) may be just as dangerous as the parent
nuts by levels ranging from 17% to 63%, depending on the time OTA molecule itself.29
and temperature of the roasting as well as initial level of toxin
contamination. It has also been reported that the presence of ionic Fumonisins
salts causes an increase in the levels of aflatoxin degradation that Fumonisins are also fairly heat-stable (up to 100–120 ◦ C) and there-
can be achieved by heat treatments. For example, 38%, 41.5% and fore survive many of the commonly used thermal processes.3,34 In
47.6% degradation of AFB1 in unsalted and 20 g kg−1 and 50 g one of the first fumonisin stability studies, Alberts et al.35 showed
kg−1 in salted peanuts has been achieved by traditional roasting that boiling of Fusarium verticillioides culture material for 30 min
at 150 ◦ C for 30 min, respectively.18 Similar results have been did not result in a reduction in the overall levels of fumonisin
obtained by roasting coffee beans. Soliman19 reported reductions B1 (FB1 ) present. In another study conducted by Maragos and
in aflatoxins in coffee beans ranging from 42.2% to 55.9% following Richard,36 the pasteurization of milk spiked with 50 ng mL−1 FB1
the roasting process, depending on the type and temperature of and fumonisin B2 (FB2 ) at 62 ◦ C for 30 min did not lead to signif-
roasting. In a study conducted by Ogunsanwo et al.,20 seeds dry- icant reductions in the fumonisin levels in the milk. Additionally,
roasted at 140 ◦ C for 40 min resulted in 58.8% and 64.5% reductions the nixtamalization of maize was not effective in reducing FB1
in AFB1 and AFG1 , while those roasted at 150 ◦ C for 25 min resulted levels in maize materials and the hydrolysis product, hydrolyzed
in 68.5% and 73.3% reductions in AFB1 and AFG1 , respectively. fumonisin B1 (HFB1 ), was still toxic.37 However, the toxicological
The effects of heat treatments on the stability of aflatoxin significance of hydrolyzed fumonisins in foods is not yet clear,
M1 (AFM1 ), the monohydroxylated derivative of AFB1 , have also with HFB1 being reported to inhibit ceramide synthase in vitro less
been tested. Purchase et al.21 observed that a 32% reduction in effectively than FB1 , suggesting that HFB1 may potentially be less
AFM1 can be achieved by pasteurization at 62 ◦ C for 30 min. In toxic in vivo.34
another report, the heating of milk, depending on the conditions The effects of processing time (10–60 min) and temperature
employed, can cause a decrease in the AFM1 content of the milk (100–235 ◦ C) on the stability of FB1 and FB2 in aqueous buffered
of between 12% and 35%.22 solutions at pH 4, 7 and 10 have shown that both compounds
are least stable at pH 4, followed by 10 and 7. Decomposition
Ochratoxin A begins at or above 150 ◦ C, and at >175 ◦ C more than 90% of
The thermal stability of OTA is of particular interest to the coffee FB1 and FB2 was lost after a 60 min treatment, regardless of
industry. OTA has a melting point of 169 ◦ C and there have been pH.38,39 In addition, Scott and Lawrance40 showed that heating
a number of conflicting reports involving the effect of roasting of dry and moist maize meals at 190 ◦ C for 60 min caused in the
on OTA levels in coffee. It has been reported that roasting at range of 60–80% reductions in fumonisin levels, while almost
200 ◦ C for 10–20 min resulted in only a 0–12% reduction in OTA 100% of the available toxin was degraded following baking at
levels in the dried whole beans,23 while Studer-Rohr et al.24 have 220 ◦ C for 25 min. In another report, baking maize muffins spiked
shown that roasting (150 ◦ C, 2.5 min) of naturally contaminated with 5 mg kg−1 FB1 at 175 and 200 ◦ C resulted in 16% and 28%
green beans or beans which have inoculated with Aspergillus reductions in toxin levels, respectively, whereas the frying of tortilla
ochraceus resulted in only small reductions in OTA levels. On the chips at 190 ◦ C for 15 min caused a 67% reduction in fumonisin
other hand, Blanc et al.25 reported that up to 80% of the OTA levels.41 In similar work, Castelo and co-workers observed that
present in coffee was destroyed during the industrial roasting the roasting of maize meal samples which were either artificially
process, with other studies reporting that roasting coffee led to a (5 µg g−1 of FB1 ) or naturally contaminated, at 218 ◦ C for 15 min,
mean reductions of between 66.5% and 90% in OTA levels.26 – 28 In resulted in a complete loss of fumonisins.42
other studies Suárez-Quiroz et al.29 reported that roasting green During food processing, it is known that fumonisins can bind
coffee naturally contaminated with OTA (0.4 µg kg−1 ) resulted in to various components within the food matrix or react with
the complete loss of OTA, whereas reduction to a maximum of other ingredients within the food such as reducing sugars. For
82.9% was observed in green coffee artificially contaminated with example, the incubation of FB1 with D-glucose results in the
53.2 µg kg−1 OTA. In another study, thermal treatment of liquorice formation of N-carboxymethyl-FB1 .43 The four primary products
at 150 ◦ C for 60 min did not reduce its OTA content.30 The effect of the FB1 -reducing sugars reaction have been characterized as N-
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of temperature and moisture conditions on the decomposition of methyl-FB1 , N-carboxymethyl-FB1 , N-(3-hydroxyacetonyl)-FB1 and

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N-(2-hydroxy, 2-carboxyethyl)-FB1 by nuclear magnetic resonance Moniliformin

and electrospray mass spectroscopy.44 The reaction of FB1 with Overall, MON displays heat stability which is similar to or greater
reducing sugars such as D-glucose or D-fructose at 65 ◦ C for 48 h than other Fusarium mycotoxins such as DON and FB1 .59 In stability
appears to block the primary amino group FB1 thereby preventing studies, heating ground maize and ground wheat containing MON
FB1 -induced toxicity of rat and swine cell tissue cultures.43,45 – 48 at a level of 1 µg g−1 at 50, 100 and 150 ◦ C for 0.5–2 h resulted
It should also be noted that fumonisin concentrations in in moderate levels of decomposition, with, for example, 55% of
cooked products might in fact actually underestimate the the toxin remaining in the maize following treatment at 100 ◦ C
products’ potential toxicity because of the formation of unknown for 0.5 h.60 Better results were, however, subsequently reported
biologically active fumonisin decomposition products or so called for MON, where the percentage of MON reduction was correlated
‘hidden’ fumonisins. ‘Hidden’ fumonisins have been described as positively with increasing temperature and pH, with heating at
fumonisins that are bound to sugar, such as the aforementioned pH 10 resulting in a major reduction in toxin levels, i.e. 99%
reducing sugars, or other components in food matrices during degradation at 175 ◦ C after 60 min.61 Similarly, complete (100%)
cooking/processing or which are present in the raw material prior reduction of MON was observed when a naturally contaminated
to processing34 and that cannot be detected by conventional maize sample containing 1.4 µg g−1 of MON was used in a pilot-
methods.49 For example, Kim et al.50 reported that hidden scale alkaline cooking and tortilla-manufacturing process.62 In
fumonisin contamination could be detected in all the cornflake stark contrast, however, in a very extensive study Pineda-Valdes
samples they analyzed, even in those with no detectable fumonisin et al.59 reported that MON was relatively heat-stable under the
levels. conditions tested for baking, autoclaving, frying, roasting and
The milling process appears to result in the differential extrusion, showing stability comparable to or in some cases even
distribution of fumonisins in different milling fractions, leading greater than other Fusarium mycotoxins. Roasting maize meal at
ultimately to an increase in toxin concentrations in some products 218 ◦ C for 15 min had the most significant effect (44.6%) on the
and a decrease in others.34 This is clearly evident from a recent reduction of MON, whereas autoclaving creamed maize at 121 ◦ C
study in which the redistribution of 16 different Fusarium toxins for 65 min resulted in only a 10% reduction in MON levels. The
during commercial dry milling of maize was reported. Toxins were mechanism of heat-induced destruction of MON and whether or
either not detected at all or their content was low in raw and not this heat treatment reduces the toxicity of MON still remain to
tempered maize, grits and two types of flour, whereas markedly be established.63
higher toxin concentrations were found in screenings, bran, germ
or germ meal.51
Patulin
Deoxynivalenol Patulin has a melting point of 111 ◦ C64 and it is more stable
DON is a very stable compound, with a melting point of to thermal degradation in the pH range 3.5–5.5, with lower pH
151–153 ◦ C, and thermal processing is known not to destroy values leading to greater stability.65 There are conflicting reports
or significantly reduce DON levels.52 On the other hand, when in the literature concerning the thermal stability of patulin. It has
higher temperatures are used some reductions may be achieved. been reported that approximately 90% degradation of patulin can
For example, the cooking of spaghetti and noodles prepared from be achieved by heat treatment at 105 ◦ C for 29 h,66 while in a
wheat has been shown to reduce DON levels by 47%.53 In a very second study the pasteurization of apple cider at 60–90 ◦ C for 10 s
extensive study, Samar et al.54 have reported reductions in the resulted in only an 18.8% reduction in patulin levels.67 Finally in
levels of DON of more than 66%, 43% and 38%, after frying at 169, a third study heat treatments of 90 and 100 ◦ C for 20 min were
205 and 243 ◦ C, respectively, in flour artificially contaminated with reported to lead to patulin degradation levels of 18.8% and 26%,
260 µg kg−1 DON. Similarly, reductions in DON concentrations of respectively, while heating samples to 70 and 80 ◦ C during an
up to 52% have been achieved in grain by employing superheated evaporation process resulted in 9.4% and 14.06% reductions in
steam at 185 ◦ C for 6 min.55 The effects of various heat treatments patulin concentration, respectively, after 20 min.68
at differing pH values on DON degradation have been evaluated
by Wolf and Bullerman.56 While DON levels were unaffected by
heat treatments of 100–120 ◦ C at pH 4.0 and 7.0, heat treatments EXTRUSION PROCESSING
of 120 ◦ C for 30 min or 170 ◦ C for 15 min led to the complete The effects of one of the most recent food-processing op-
degradation of DON at pH 10. Since none of the potential thermal erations – extrusion processing – on the destruction of various
decomposition products of DON are known, coupled with the mycotoxins have also been tested by several investigators. Dur-
fact that no toxicity studies have been done on these products ing extrusion cooking, the raw material is subjected to high
of DON, there is currently no clear evidence that the observed temperature, high pressure and severe shear forces. Two major
thermal instability of DON ultimately results in the detoxification types of extruders are used in the food industry: single-screw
of DON-contaminated foods or feeds. and twin-screw extruders.34 The destruction of mycotoxins dur-
ing extrusion processing is largely dependent on several factors,
Zearalenone including extruder temperature, screw speed, moisture content
ZEA is a chemically stable compound with a melting point of of the extrusion mixture and residence time in the extruder.3 The
164–165 ◦ C.57 On one hand it has been reported that ZEA can effects of the different extrusion parameters on the destruction of
survive heat treatments of 120 ◦ C for 4 h,5 while on the other mycotoxins are summarized in Table 1.
complete reduction of ZEA has been observed in aqueous buffer In a study conducted by Scudamore et al.,69 the factors residence
solutions heated for less than 30 min at 225 ◦ C, regardless of the time, temperature and moisture affected the loss of OTA during
pH of the solution.58 Additionally, it has been reported that the extrusion of contaminated wholemeal wheat flour, whereas screw
potential estrogenic activity of breakdown products of ZEA can be speed had very little effect under the same test conditions. At
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reduced in bread during processing.4 200 ◦ C and a residence time of 40 s, approximately 30–40% of

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Table 1. The fate of mycotoxins during extrusion processing

Initial level Type of Barrel Screw speed Moisture Reduction
Mycotoxin (µg g−1 ) Raw material extruder temperature (◦ C) (rpm) content (%) (%) References

AFB1 0.05 Maize flour n.r. 150, 180 120 15, 30 10–25 72
AFB1 0.49 Maize flour Single-screw 87 35 n.r. 46 14
AFB1 0.63–0.97 Rice meal Single-screw 140, 170, 200 40–150 24, 27, 30 65–95 73
AFB2 0.11–0.39 Rice meal Single-screw 140, 170, 200 40–150 24, 27, 30 58–94
AFG1 0.27–0.38 Rice meal Single-screw 140, 170, 200 40–150 24, 27, 30 79–95
AFG2 0.08–0.14 Rice meal Single-screw 140, 170, 200 40–150 24, 27, 30 51–95
AFM1 0.4 Maize flour Single-screw 87 35 n.r. 20 14
OTA 0.01, 0.04 Wheat flour Twin-screw 116–136 200–252 30 11–39 69
OTA 0.01, 0.04 Wheat flour Twin-screw 157–196 352–401 17.5 8–35
OTA 0.01 Wheat flour Twin-screw 168–201 300 17–25 21–31
OTA 0.05 Wheat flour Twin-screw 183–200 302 18–26 28–42
FB1 5 Maize grits Twin-screw 120, 140, 160 142 18, 22, 26 31–68 71
FB1 5 Maize grits Twin-screw 14, 160, 180, 200 160 26 34–95 74
DON 4 Maize grits Twin-screw n.r. 140 22 53 75
DON 5.47 Dry dog food Single-screw 100 29 22 21
DON 5 Maize flour n.r. 150, 180 120 15, 30 95–99.5 72
MON 5 Maize grits Twin-screw 140, 160, 180 142 18, 22, 26 27 59
ZEA 4.4 Maize grits Twin screw 120, 140, 160 n.r. 18, 22, 26 66–83 70

n.r., not reported.

the OTA was broken down at wholemeal flour moisture values concentration of toxin added, variations in sample source and/or
between 17% and 25%. In another study, focusing on ZEA, it environmental factors.
has been reported that extrusion cooking of maize grits led to In conclusion, although most mycotoxins are moderately heat-
reductions in toxin levels ranging from 77% to 83%, 74% to 83% stable, varying degrees of destruction can be achieved with the
and 66% to 77% at 120, 140 and 160 ◦ C, respectively.70 Overall, the use of high-temperature processing. Most of the data indicate
use of the mixing screws resulted in slightly higher levels of ZEA that baking, frying, roasting, extrusion and microwave heating
reduction (66–83%) than the use of non-mixing screws (65–77%). cause reductions in mycotoxin levels in different food materials.
This is in agreement with the study of Castelo et al.,71 who reported It is important to note, however, that the amount of reduction
that extrusion cooking achieved higher levels of apparent FB1 loss is highly dependent on cooking conditions, such as temperature,
when the extruder was equipped with mixing (30–68%) screws time, water and pH, as well as the type of mycotoxin and its
than with non-mixing screws (16–50%), since both the residence concentration in the food or feed matrix. Further studies on the
time and shear rate are higher than when extruding with mixing toxic effects of the potential breakdown products of mycotoxins
screws. Additionally, Cazzaniga et al.72 reported higher than 95% to various biological systems are also clearly required before the
reductions in DON levels in maize flour by extrusion cooking at apparent losses/reductions in toxin levels observed during food
150–180 ◦ C, whereas 10–25% reduction was observed in AFB1 processing can be directly equated with an overall loss in toxicity.
in maize flour under similar conditions. In one of the most
recent studies, extrusion cooking was reported to reduce aflatoxin
content, which ranged from 51% to 95% depending on the type
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