Food Chemistry 218 (2017) 64–69

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Mycotoxin analysis of industrial beers from Brazil: The influence of

fumonisin B1 and deoxynivalenol in beer quality
Karim C. Piacentini a,⇑, Liliana O. Rocha b, Lívia C. Fontes b, Lorena Carnielli b, Tatiana A. Reis b,
Benedito Corrêa a,b
a
Biotecnology Department, University of Sao Paulo, Sao Paulo, Av. Professor Lineu Prestes 2415, Brazil
b
Microbiology Department, University of Sao Paulo, Sao Paulo, Av. Professor Lineu Prestes 1374, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Worldwide, barley is the main source of carbohydrate in the brewing process. However, corn is often used
Received 11 July 2016 as an adjunct to improve and accelerate the fermentation process. Considering that, these two substrates
Received in revised form 6 September 2016 are susceptible to fungal contamination as well as mycotoxins. The objective of the current study is to
Accepted 8 September 2016
determine the incidence of the mycotoxins deoxynivalenol (DON) and fumonisin B1 (FB1) in industrial
Available online 9 September 2016
beers.
The method applied for mycotoxin analyses included high performance liquid chromatography. The
Keywords:
mean levels for recovery experiments were 89.6% for DON and 93.3% for FB1. DON was not detected in
Beer
Adjuncts
any of the analyzed samples whereas FB1 was found in 49% of the 114 samples. The current survey
Maize demonstrated levels of FB1 contamination in industrial beer, possibly due to the addition of contaminated
Quality adjuncts. It is necessary to establish maximum levels of mycotoxins in beer in Brazil and other countries
Mycotoxins in order to reduce health risks.
Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction
Beer is a popular alcoholic beverage in the world context for
reasons that transcend social and economic aspects. In Brazil, the
beer market continues to grow every year and production reached
13.5 billion liters in 2013. In terms of national average consump-
tion, data has shown a large growth potential of 68.3 L per person
in 2014 (CervBrasil, 2014).
Worldwide, the source of fermentable sugars in industrial beer
is starch-rich cereals, mainly malted barley. Nevertheless, adjuncts
including corn, rice, unmalted barley, wheat starch, oats and sor-
ghum have been also used by the large-scale brewing industry to
provide additional sources of fermentable carbohydrates for the
yeast (Figueroa, Martínez, & Ríos, 1995; Poreda, Czarnik,
Zdaniewicz, Jakubowski, & Antkiewicz, 2014).
The brewing industry has many reasons for the application of
adjuncts including better availability on the local market, sensory
modification of the beer and, the most important, the lower price
of this product in Brazil (Dhellot & Kobawila, 2013; Glatthar,
Heinisch, & Senn, 2005). It has been proven that the use of 30%
of corn adjunct can give an 8% reduction in total production costs,
⇑ Corresponding author at: Biotechnology Department, Biomedics Science Insti-
tute, ICB III, University of Sao Paulo, Sao Paulo, SP CEP 05508-900, Brazil.
although this number may vary depending on the local prices of
raw materials and other costs of production (Baca, 2001). However,
application of adjuncts also has some disadvantages. One of the
most relevant is the contamination by fungi and the production
of mycotoxins. These will have a negative impact on the final pro-
duct, mainly because of the health problems associated with myco-
toxin contamination (Lancova et al., 2008). Several studies revealed
that barley can be contaminated by fungi (Piacentini, Savi, Olivo, &
Scussel, 2015), as well as the adjuncts used for brewing
(Kawashima, Vieira, & Valente Soares, 2007; Oliveira, Rocha,
Sulyok, Krska, & Mallmann, 2016; Queiroz et al., 2012; Van der
Westhuizen et al., 2003).
The major mycotoxins found in barley are the trichothecenes
type B group, primarily DON and its metabolites (Lancova et al.,
2008). Trichothecenes are toxins of the sesquiterpenoid metabo-
lism, produced by some species of Fusarium and other fungi in
the order Hypocreales (Rocha et al., 2015). DON is a mycotoxin lar-
gely produced by the Fusarium graminearum species complex
(FGSC) and this group is a devastating pathogen causing Fusarium
head blight in wheat and barley. DON is considered a potent inhi-
bitor of protein biosynthesis, exhibiting acute adverse effects in
animals (Rubella, Goswami, & Kistler, 2004).
Considering that corn is one of the adjuncts used for brewing,
detection of fumonisins B1 and B2 (FB1 and FB2) are expected in

http://dx.doi.org/10.1016/j.foodchem.2016.09.062
0308-8146/Ó 2016 Elsevier Ltd. All rights reserved.
 K.C. Piacentini et al. / Food Chemistry 218 (2017) 64–69
beer, as these are the most prevalent mycotoxins in this cereal and
its processed products (Matumba et al., 2014; Oliveira et al., 2016).
Fumonisins is an important mycotoxin group produced mainly by
the Fusarium fujikuroi species complex (FFSC) (Rocha et al., 2016).
Fusarium verticillioides, the major fumonisin-producing species
within the FFSC, is able to produce levels above 5000 lg/kg as
observed by many authors worldwide (Hinojo et al., 2006;
Vismer, Marasas, & Schalkwyk, 2004).
FB1 is known to cause toxicity in animals due to the inhibition
of sphingolipid metabolism and cell cycle regulation, resulting in
several adverse effects such as leukoencephalomalacia in horses
and pulmonary oedema in swine (Desjardins, 2006). It is also asso-
ciated with oesophageal cancer and neural tube birth defects in
humans (Marasas et al., 2004).
Nowadays, there is a lack of regulation for toxin levels in beer,
with maximum levels set only for raw materials (Brasil, 2011,
2013; EC No 1881/2006). However, the Scientific Committee for
Food (SCF) and FAO/WHO Joint Expert Committee on Food Addi-
tives (JECFA) (Bolger et al., 2001) indicated a tolerable daily intake
(TDI) of 1 lg/kg 1 and 2 lg/kg 1 bw for DON and FB1, respectively.
For the reasons stated above and considering that the brewing
industry in Brazil is continuing to rise, the objective of the study
was to determine the influence of the mycotoxins DON and FB1
on industrial beer quality from Brazil.
2. Materials and methods
2.1. Beer samples
A total of 114 industrial beer cans and bottles (Lager type) con-
sisting of 20 different brands and different batches were randomly
chosen to represent the main brewing industries of Brazil. These
samples were acquired from markets between September 2015
and January 2016. None of the beers had surpassed their expiry
date. Until the sample preparation, they were stored in the dark
at room temperature.
2.2. Chemicals and reagents
DON and FB1 standards were obtained from Sigma Aldrich
Chemicals (St. Louis, MO, USA). The DON stock solution was pre-
pared by dissolving 1 mg of DON in 1 ml of ethyl acetate and then
dried. The standard curve solutions were prepared from appropri-
ate dilutions of the stock solutions (200 lg/ml) with the mobile
phase acetonitrile: water (10:90) in concentrations of 0.1, 0.3,
0.6, 1.25, 2.5, 5, 10 and 20 lg/ml. A stock solution of FB1 was pre-
pared by dissolving 1 mg of FB1 in 1 ml of acetonitrile and then
dried. The standard curve solutions were prepared from appropri-
ate dilutions of the stock solution (50 lg/ml) with the mobile
phase acetonitrile:water: acetic acid (520:480:5) in concentrations
equal to 0.025, 0.05, 0.18, 0.37, 0.75, 1.5, 3 and 6 lg/ml.
For HPLC analyses, acetonitrile and methanol were obtained
from J.T Baker (Sao Paulo, SP, Brazil) and all were LC grade. Sodium
hydroxide was from Biotec (Pinhais, PR, Brazil) and the OPA
reagent (0.04 g o-ftaldialdehyde in 1 ml methanol diluted with
5 ml 0.1 M borate buffer and 50 ll of 2-mercaptoethanol) was from
Sigma Aldrich Chemicals (St. Louis, MO, USA). High-purity Milli-Q
water (18.2 MU/cm) was obtained from the Millipore Synergy sys-
tem (MA, USA).
2.3. Instruments and apparatus
The following instruments were required for analysis: high per-
formance liquid chromatography (HPLC), Shimadzu (Kyoto, Japan),
equipped with an isocratic pump, an SIL-20A autosampler, with an
65
ultraviolet–visible (UV) detector model SPD M20 and a fluores-
cence detector model RF-10AXL. The chromatographic column
used for DON was C18 reversed-phase (Synergi 4 lm particle size,
with 250  4.60 mm, length and diameter, respectively), model
Fusion-RP 80, Phenomenex (Torrance, USA). The chromatographic
column used for FB1 was C18 reversed-phase (particle size 5 lm,
with 150 and 4.60 mm), model Luna (Torrance, USA).
2.4. Extraction procedure
To perform DON analysis, the Vicam protocol DON test N°
G1005 (2013) with some modifications was used as follows: briefly
84 ml of Milli-Q water was added to 16 ml of a degassed beer sam-
ple and mixed for 10 min in the shaker at 150 rpm and then filtered
through a filter paper.
For sample cleanup and concentration, an aliquot of 1 ml of the
extract was applied to an immunoaffinity column (DON Test WB
HPLC – Vicam) at a flow rate of one drop per second. The sample
was followed by 2.5 ml of LC grade water to wash the column
and the toxin was slowly eluted with 2 ml of 100% LC grade metha-
nol. The eluate was evaporated using a heating block device at
40 °C in a gentle nitrogen stream.
FB1 analysis was performed according to the Association of Offi-
cial Analytical Chemists (AOAC) Official Methods of Analysis
995.15 (AOAC, 2005), originally developed for corn and its prod-
ucts, with some modifications. In short, the pH of craft beer sam-
ples was brought to a 5.8–6.5 range with 1 N NaOH and the
samples were filtered through qualitative filter paper. For sample
cleanup and concentration, a 50 ml aliquot of beer was applied to
a strong anion exchange SPE column (6 cm3, 500 mg 1, SAX, Phe-
nomenex, USA), previously conditioned with 10 ml of methanol,
followed by 10 ml of methanol:water (3:1). The sample was fol-
lowed by 10 ml of methanol:water (3:1) and 6 ml of methanol.
FB1 was eluted with 5 ml of methanol:acetic acid (95:5). The elu-
tion was dried in a heating block at 60 °C. The dried extract was
suspended in 300 ll of acetonitrile:water (1:1) and then was
cleaned with a syringe filter (0.45 mm, 13 mm, CA membrane).
2.5. HPLC analysis
The dry residue of DON was resuspended in 500 ll of mobile
phase acetonitrile:water (10:90, v/v). The extract (70 ll) was
injected into the LC/UV system set at a wavelength of 218 nm
and the mobile phase was delivered at a constant flow rate of
1 ml/min.
For FB1 analysis, 50 ll of the extract was transferred to a reac-
tion vessel and 50 ll of OPA reagent was added. After 60 s of reac-
tion time, 20 ll of the derived sample was injected into an LC-FLD
at 335 and 440 nm for excitation and emission, respectively. The
mobile phase was acetonitrile:water:acetic acid (520:480:5, v/v)
at a flow rate of 1 ml/min.
3. Results
3.1. Validation methods
The samples used for validation were analyzed beforehand to
ensure that they did not contain any of the studied compounds.
Afterwards, blank samples were selected for spiking and recovery
purposes. The spiking concentrations and their recoveries are
shown in Table 1 and were carried out in triplicate. The linearity
was established by the calibration curve with injections of differ-
ent standard concentrations aforementioned (0.025–6 lg/ml for
FB1 and 0.1–20 lg/ml for DON). Each standard concentration was
carried out in quintuplicate. The coefficient correlations were r2:
66 K.C. Piacentini et al. / Food Chemistry 218 (2017) 64–69
Table 1
Mycotoxin recoveries from artificially contaminated industrial beer samples.
Mycotoxin Toxin added lg/l Recovery%
DON 100 95
50 85
25 89
FB1 500 95
300 87
100 98
a
SD: standard deviation.
b
RSD: relative standard deviation.
0.995 and r2: 0.998 for FB1 and DON, respectively. Limits of detec-
tion (LODs) and quantification (LOQs) were calculated as the con-
centrations whose signal-to-noise ratios were 3 and 10,
respectively (Table 1). Finally, the retention time of FB1 was
11.2 min (Fig. 1) and of DON was 8.4 min.
3.2. Occurrence of mycotoxins
Of the 114 samples analyzed, none contained detectable levels
of DON. The descriptive analysis of the industrial beer from Brazil
is shown in Table 2.
In the current research, FB1 was detected in approximately 50%
of the samples (56 positive of 114 samples) with levels ranging
from 201.70 lg/l to 1568.62 lg/l (mean: 367.47 lg/l). The descrip-
tive analysis of the industrial beer from Brazil is shown in Table 2.
Fig. 1 represents the chromatograms of the mycotoxins DON
and FB1 in beer samples in comparison to their respective
standards.
4. Discussion
The current study demonstrated that industrial Brazilian beer
was not contaminated by DON, whereas FB1 levels were relevant.
Indeed, previous studies have shown that the transmission of
mycotoxins into the final beer will depend on crop infection, agri-
cultural practices and the technological conditions applied during
the brewing process (Kostelanska et al., 2009; Lancova et al.,
2008; Omurtag & Beyoglu, 2007). On the other hand, it has been
established that during the brewing process, DON can be either
eliminated or reduced (Lancova et al., 2008; Schwarz, Casper, &
Beattie, 1995), followed by an increase of a DON conjugate, DON-
3-glucose glucose (Kostelanska et al., 2009; Lancova et al., 2008).
These reasons may explain the non-detectable levels of DON in
industrial beer.
In general, the wheat-based beers have higher DON occurrence.
In this respect, Varga, Malachova, Schwartz, Krska, and Berthiller
(2013) and Rodríguez-Carrasco, Fattore, Albrizio, Berrada, and
Mañes (2015) showed that 78.3% of the 46 analyzed wheat beers
were contaminated by DON, with an average content of 18.4 lg/l
and maximum level of 49.6 lg/l. Also, a study proposed by the cur-
rent author demonstrated that pure malting barley beer can be
contaminated by DON, with levels ranging from 127 lg/l to
501 lg/l (mean: 221 lg/l) (Piacentini et al., 2015).
Nevertheless, a study carried out on industrial beers in coun-
tries from Europe (Belgium, Germany, Poland, Spain, UK and Ire-
land), demonstrated very low levels of DON and other
mycotoxins despite their considerable frequency (Bauer, Gross,
Gottschalk, & Usleber, 2016; Bertuzzi, Rastelli, Mulazzi, Donadini,
& Pietri, 2011).
Taking into account the FB1 contamination, the levels in the cur-
rent study could be justified with the adjunct used for the brewing
process. Several studies have shown high FBs contamination in
maize worldwide, including in Brazil (Bryła, Roszko, Szymczyk,
N SDa RSDb Recovery Mean% LOQ(lg/l) LOD (lg/l)
3 0.58 0.61 89.6 9.4 2.8
3 0.55 0.65
3 0.47 0.52
3 0.62 0.65 93.3 6.3 2.0
3 0.36 0.41
3 0.20 0.21
Jedrzejczak, & Obiedzinski, 2016; Lanza et al., 2014; Van der
Westhuizen et al., 2003). In a study carried out by Oliveira et al.
(2016), high levels of FB1 and FB2 (mean 3153 lg/kg) were found.
Also, Queiroz et al. (2012) showed that all corn samples were con-
taminated by fumonisins (FB1 and FB2), with levels ranging from
230.1 to 6450 lg/kg for both mycotoxins.
Previous studies have demonstrated that underdeveloped coun-
tries, such as Brazil, usually exports the best sources (grains) pro-
duced (Leslie & Logrieco, 2014). The medium quality grains are
for the population’s consummation and the rest, namely the worst
part of the production, is destined for the adjuncts and processed
food. This may explain the high contamination of the final product.
According to the national regulations, an amount of adjunct can
replace malted barley up to a maximum of 50% (Brasil, 1997).
Maize, which is the main available and chosen grain in Brazil to
improve and accelerate the fermentation process in the beer indus-
try, is likely to suffer contamination by FFSC, the main fumonisin-
producing lineage within the genus Fusarium (O’Donnell et al.,
2013). As a consequence of the use of maize adjuncts in the brew-
ing process, fumonisins may, therefore, potentially occur in beer
(Bertuzzi et al., 2011; Kawashima et al., 2007; Oliveira et al., 2016).
In order to exemplify this, a survey carried out by Matumba
et al. (2014) on Malawi maize-based beer showed similar results,
with high concentrations of FBs (mean = 1522 lg/l). Furthermore,
FB1 contamination was also reported in industrial beers from Eur-
ope with maximum levels of 30 lg/l, and an incidence of 97% of the
samples analyzed. Likewise, levels of FB1 (4.8–85.5 lg/l) were also
found in 43.8% of 32 beer samples in Spain (Torres, Sanchis, &
Ramos, 1998).
Furthermore, the results from this survey revealed higher FB1
contamination when compared to a previous study carried out in
Brazil on industrial beers in 2007, where 43.1% of the analyzed
samples were contaminated with levels ranging from 1 to 40 lg/l
(Kawashima et al., 2007). It is necessary to mention that fumon-
isins are known to be stable in heat processes as well as during
the fermentation (Alberts, Gelderblom, Thiel, & Marasas, 1990;
Jackson, Hlywka, Senthil, & Bullerman, 1996; Jackson, Hlywka,
Senthil, Bullerman, & Musser, 1996; Scott, Kanhere, Lawrence,
Daley, & Farber, 1995). In a research conducted by Pietri,
Bertuzzi, Agosti, and Donadini (2010), it was shown that FB1 occur-
rence in finished beer is mainly due to its high solubility in water
and to the relative heat treatment stability.
Comparing FB1 contamination found in industrial beers of this
study together with previous research carried out on craft beers
(made only from barley), it is possible to infer that the latter is
safer than the industrial beer, due to the negligible levels of FB1
found previously (Piacentini et al., 2015).
Finally, it is important to emphasize that the current Brazilian
and international regulations do not determine maximum levels
for FB1 and DON in beer. These levels can serve as a benchmark
to highlight the need for proper adjunct selection in the brewing
industry. Furthermore, the choice of good resources is not only
important because of the beer quality and brewery reputation
 K.C. Piacentini et al. / Food Chemistry 218 (2017) 64–69 67

Fig. 1. HPLC chromatograms of FB1 and DON. a. FB1 standard (750 lg/l) and contaminated beer sample (201.70 lg/l). b. DON standard (600 lg/l) and beer sample. ⁄mV,
Millivolt.
68 K.C. Piacentini et al. / Food Chemistry 218 (2017) 64–69
Table 2
Occurrence of mycotoxins (FB1 and DON) in 114 industrial beer samples.
Mycotoxin
DON
Number of negative samples 114
Number of positive samples 0 56
Range of positive samples (lg/l) – 201.70–1568.62
Mean of positive samples (lg/l) – 367.47
Method LOQ: 6.3 l/l for FB1 and 9.4 lg/l for DON.
Table 3
Mycotoxin dietary intakes estimation from
consumption.
Mycotoxin
FB1
Median (lg/l) 255
Daily average exposure (lg/kg/bw) 0.79
Tolerable daily intake (lg/kg/bw) 2
% of tolerable daily intake 39.5
but also because the raw materials must not represent any health
risk caused by FB1 exposure to consumers.
4.1. Mycotoxin dietary intakes estimation from industrial beer
consumption
Using an average adult body weight of 60 kg and the mycotoxin
occurrence data from this study, an estimation of dietary exposure
to FB1 from the industrial beer was carried out (Table 3).
The consumption of 68.3 l/year per capita, equivalent to
0.187 l/day of beer, resulted in an exposure of 0.56 lg/kg/body
weight (bw)/day for a 60 kg adult. This estimated daily intake
(DI) is lower than the provisional maximum tolerable daily intake
(PMTDI) of 2 lg/kg bw/day for FB1 stipulated by the FAO/WHO
Joint Expert Committee on Food Additives (JECFA) (Bolger et al.,
2001).
Despite the estimated daily intake being lower than the limit
established by the regulations, the presence of fumonisins in beer
should be a health concern to industry, mainly because fumonisins
are carcinogenic metabolites. In addition, FB1 has been associated
with human oesophageal cancer and neural tube birth defects in
countries where the consumption of corn is high (IPCS/WHO,
2000; Marasas et al., 1988; Soriano, González, & Catalá, 2005).
5. Conclusion
The current survey demonstrated relevant levels of FB1 contam-
ination in industrial beer, possibly due to the addition of contam-
inated adjuncts. In order to replace barley or enhance the
fermentation process, corn is often used in Brazilian beer indus-
tries because of its wide distribution and low costs in the country.
This explains the incidence of FB1 in the analyzed samples. The
results indicate the need for strategies to reduce mycotoxin con-
tamination in the raw material used for beer manufacturing as well
as to reduce FB1 contamination in the traditional beer processing
chain. Finally, maximum levels of mycotoxins in beer in Brazil
and other countries need to be established.
Financial support
The authors thank FAPESP for financial support.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
FB1 the online version, at http://dx.doi.org/10.1016/j.foodchem.2016.
09.062.
58
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