Food Control 18 (2007) 1058–1062
www.elsevier.com/locate/foodcont
Estimation of dietary intakes of fumonisins B1 and B2
from conventional and organic corn
Agustín Ariño
a
a,¤
, Gloria Estopañan b, Teresa Juan b, Antonio Herrera
a
Veterinary Faculty, Department of Animal Production and Food Science, University of Zaragoza, c/Miguel Servet 177, E-50013 Zaragoza, Spain
b
Agri-Food Research and Technology Center, Avda. Montañana 930, E-50059 Zaragoza, Spain
Received 27 April 2006; received in revised form 23 June 2006; accepted 3 July 2006
Abstract
The dietary intakes of fumonisins from 60 samples of conventional and organic corn were assessed. A 13.3% of the conventional corn
samples contained fumonisin B1 and B2 at mean levels of 43 and 22 ng/g, respectively, while 10% of the organic corn samples contained
fumonisins at somewhat lower levels of 35 ng/g (FB1) and 19 ng/g (FB2). Overall, the fumonisin levels in the corn samples were much
lower than the maximum level of 2000 ng/g (as the sum of FB1 and FB2) proposed for unprocessed maize in a recent EU regulation. The
fumonisins present in conventional and organic maize are estimated to contribute with very low percentages of 0.21% and 0.17%, respectively, to the level considered at risk for human health. Based on the data exposed in this paper, the farming system is probably not of
decisive importance for the Wnal contamination of agricultural products with these mycotoxins.
© 2006 Elsevier Ltd. All rights reserved.
Keywords: Fumonisins; Organic corn; Daily intakes
1. Introduction
In the temperate climatic conditions prevailing in
Europe, Fusarium fungi are important in the cereal food
chain and can reduce crop yields and contaminate grain
with mycotoxins (SCOOP, 2003). In Aragón (Spain), maize
diseases caused by Fusarium have been reported since the
early 1980’s (Palazón & Palazón, 1982). Members of the
Gibberella fujikuroi complex (species Fusarium verticillioides, synonym of F. moniliforme) are generally regarded as
the most important colonizers of cereal grains with the ability to produce the fumonisin mycotoxins (Ariño & Bullerman, 1994; Shephard, Thiel, Stockenström, & Sydenham,
1996; Soriano & Dragacci, 2004a). Fumonisins have been
shown to be involved in leukoencephalomalacia in equine
species, associated with pulmonary oedema in pigs, and
*
Corresponding author. Tel.: +34 976 761543; fax: +34 976 761612.
E-mail address: aarino@unizar.es (A. Ariño).
0956-7135/$ - see front matter © 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2006.07.002
implicated in oesophageal cancer in humans (Visconti,
Marasas, Miller, & Riley, 1999). Fumonisin B1 is possibly
carcinogenic to humans (group 2B) by the International
Agency for Research on Cancer (IARC, 2002). The ScientiWc Committee for Food of the European Commission
(SCF, 2003) has evaluated fumonisins and established a
provisional maximum tolerable daily intake (PMTDI) of
2 g/kg body weight/day for the total of fumonisins B1, B2
and B3, alone or in combination. Also, the European Union
recently regulated fumonisins (as the sum of FB1 and FB2)
in maize-based products and unprocessed maize, so that if
no speciWc level is Wxed before 1 October 2007, maximum
levels from 200 to 2000 g/kg will apply thereafter (Commission Regulation No 856/2005).
With the steady and fast growth of the European and
US markets for organic foods there is a strong need for
quality control, including safety evaluation of the products
(Dimitri & Oberholtzer, 2006). Organic products of plant
origin are grown without the aid of chemical-synthetic
pesticides and largely without the use of readily soluble
A. Ariño et al. / Food Control 18 (2007) 1058–1062
mineral fertilizers within a diverse range of crop rotation
and extensive soil tillage. Proponents of conventional farming claim that products from organic farming may pose a
higher risk due to the presence of mycotoxins. This has not
however been conWrmed in a literature review carried out
by the Food and Agriculture Organization of the United
Nations (FAO, 2000). In a recent study, organic farming
systems showed lower rates of Fusarium ear blight infection
and lower mycotoxin contamination in winter wheat (Triticum aestivum) than conventional farming systems (Birzele,
Meier, Hindorf, Krämer, & Dehne, 2002). Occasionally,
higher mycotoxins concentrations have been measured in
organic foods than in their conventional counterparts. For
instance, in a recent comparison between conventional and
organic French foods, organic wheat and barley were more
highly contaminated by deoxynivalenol than conventional
ones, but the diVerences were not signiWcant (Malmauret,
Parent-Massin, Hardy, & Verger, 2002). In summary,
fungal attack and mycotoxin contamination in organically
and conventionally grown produce is still an extremely controversial issue (Magkos, Arvaniti, & Zampelas, 2006).
Regarding fumonisins, the Rapid Alert System for Food
and Feed of the European Union (RASSF, 2006) has
reported several alert notiWcations in conventional and
organic corn-based commodities in the last two years,
which is a cause of concern for consumers and regulatory
authorities. Also, a few research papers have compared the
levels of fumonisins in conventional and organic cornbased foods (Cirillo, Ritieni, Visone, & Cocchieri, 2003;
Paepens et al., 2005). From such results no generalizations
can be drawn except to reinforce the demand for stringent
controls and further studies including organic products.
The principles for the prevention and reduction of fumonisins should start even before harvesting, as the focal point
for the prevention of mycotoxins in cereals is the Weld
where the crops are grown. The present study was conducted to gain information on the presence of the mycotoxins fumonisin B1 and B2 in conventionally and organically
grown corn and to estimate the corresponding intakes by
consumers.
2. Material and methods
1059
himexazol 70% at 2 kg/Tm and maneb 40% at 3 L/Tm) and
insecticides and herbicides were sprayed as needed during
the vegetation period. Also, mineral fertilization of soil was
used in the conventional farms. In the organic farms, by
contrast, no pesticides and fungicides were used, and agronomic techniques included crop rotation with legumes and
alfalfa plus fertilization with compost. In addition, tilling
the soil between crop applications is indispensable in
organic farming as a weed control technique.
To prepare representative samples, up to ten subsamples
of 250 g were drawn from each lot of cereal, the subsamples
were aggregated and a single composite sample of 0.50 kg
was taken to the laboratory. The samples were stored at
¡21 °C until analyzed for mycotoxins.
2.2. Analysis of fumonisins in corn
The technique for extraction and determination of
fumonisins is based on the work by Bennett and Richard
(1994). BrieXy, 25 g of ground corn are extracted with
100 ml acetonitrile–water (1:1), Wltered through Whatman
No. 1 and the pH adjusted to 6–7. The cleanup was carried
out with Multisep 211 Fum columns (Romer Labs, Union,
MO) and the fumonisin-containing eluate was derivatized
with NDA reagent (2,3-Naphthalene dicarboxaldehyde).
Samples were injected into the LC-FLD system, a Kontron
Model 322 pump, a Model 360 autosampler, and an SFM
25 Xuorescence detector at 420 nm (excitation) and 500 nm
(emission).
The analytical method was validated in-house with
respect to precision and recovery. Blank corn samples were
spiked with FB1 and FB2 at a level of 250 ng/g by pipetting
an aliquot of standard solution onto the milled blank corn
and allowing it to dry overnight (12 h). The average recoveries and relative standard deviations (RSDr, repeatability)
obtained by the described method for FB1 and FB2 were
95.0% (RSD 4%, n D 3) and 85.0% (RSD 4%, n D 3), respectively. The performance characteristics for the analytes FB1
and FB2 were within the acceptable margins indicated in
the Commission Directive 2005/38/EC (2005). The study of
sensitivity indicated that the limit of quantiWcation (LOQ)
for FB1 and FB2 was 25 ng/g. The linear range was from
LOQ to 25xLOQ.
2.1. Origin of corn samples
2.3. Statistical analyses
Thirty samples of corn grain were selected from farms
using conventional cultivation methods, and another 30
samples were collected from organic farms. These corn
samples from various harvesting years (2001 to 2003) were
collected 1–4 weeks after harvest, October to November, at
farms of Aragon (Spain). The objective was to obtain pairs
of samples (conventional and organic) from farms at neighbouring sites. These sites diVered in agricultural practices,
fertilizers and pesticide usage, but environmental factors
such as climate and soil conditions were as comparable as
possible. In the conventional farms, the maize seeds had
been treated with fungicides (approved treatments included
The results from fumonisin analyses obtained by the
LC-FLD method were subjected to statistical analyses
(ANOVA test) according to Sachs (1978). The incidences of
samples containing fumonisins B1 and B2 (% positives) were
expressed as the percentage of samples containing levels
above LOQ (25 ng/g). The mean was calculated using onehalf the LOQ for results lower than the LOQ. A probability
value of 0.05 has been used to determine the statistical signiWcance. Calculations were performed on StatView™
SE + Graphics (Abacus Concepts, Inc. 1988, Berkeley, CA)
for Macintosh personal computers.
1060
A. Ariño et al. / Food Control 18 (2007) 1058–1062
3. Results and discussion
Fumonisin B1 was detected above the LOQ (25 ng/g) in
four samples of conventional corn (13.3%), and in three
samples of organic corn (10.0%), whereas fumonisin B2
occurred in 10% out of 30 samples of conventional corn,
and in 6.7% out of 30 samples of organic corn. The levels of
fumonisins B1 and B2 in conventional corn samples
amounted to 43 and 22 ng/g, respectively, while organic
corn samples showed somewhat lower rates of contamination, B1 35 ng/g, and B2 19 ng/g (Table 1). Considering the
positive samples, the levels of fumonisins in conventional
corn ranged from 127 to 354 ng/g (FB1) and 93 to 120 ng/g
(FB2), while in organic corn ranged from 147 to 359 ng/g
(FB1) and 60 to 153 ng/g (FB2). Overall, the fumonisin
levels in the corn samples were very low, much lower than
the maximum level of 2000 g/kg (as the sum of FB1 and
FB2) proposed for unprocessed maize in a recent EU regulation (Commission Regulation No 856/2005).
Several surveillance studies of fumonisin B1 in Spanish
market corn-based food products (Sanchis et al., 1994; Velluti, Marin, Sanchis, & Ramos, 2001) and in corn-based
feeds (Sanchis et al., 1995; Castella, Bragulat, & Cabañes,
1999) have been published, but organic corn was not
included. Regarding market corn-based foods for human
consumption (corn Xour, sweet corn, corn snacks, corn
Xakes, popcorn and toasted corn), the occurrence of
fumonisins was 16% out of 50 samples (Sanchis et al., 1994)
and 23% out of 228 samples (Velluti et al., 2001), with
calculated mean concentrations of 23.1 and 31.4 ng/g,
respectively (since authors originally reported results for
the positive samples, the total mean was re-calculated using
one-half the LOQ for negative samples for a meaningful
comparison). The prevalence is slightly higher but the
fumonisin contents are somewhat lower than those
reported in the present study, which may be probably due
to diVerent environmental conditions in the sampling years.
Therefore, the adoption of a periodic analysis of the
fumonisin levels in maize grain is recommended together
with a control system of risk factors through the use of
Good Agricultural Practices and Good Manufacturing
Practices for the prevention and reduction of Fusarium
toxins (European Commission, 2005).
In our study, the small diVerences in fumonisin concentrations between conventional and organic corn samples
were not statistically signiWcant (p > 0.05), indicating that
the farming system is probably not of decisive importance
for the Wnal contamination of agricultural products with
these mycotoxins. Similarly, the agricultural practice did
not have any signiWcant eVect on the fumonisin concentrations found in conventional and organic cornXakes from
the Belgian market (Paepens et al., 2005). A study of the
Italian market (Cirillo et al., 2003) reported that the highest
median concentration of fumonisin B1 (345 ng/g) occurred
in conventional maize-based foods (p > 0.05) while that of
fumonisin B2 (210 ng/g) appeared in organic maize-based
foods (p < 0.05). Other mycotoxins have been also subjected
to comparison between conventional and organic production systems. Thus, deoxynivalenol concentrations of conventionally grown wheat were found to be signiWcantly
higher than in organic wheat grown in Thuringia, Germany
(Döll, Valenta, Dänicke, & Flachowsky, 2002). In another
study, the levels of ochratoxin A in organically grown rye
were higher than in conventionally grown based on multiyear mean contents, though ochratoxin A levels in conventional and organic Danish wheat were very similar
(Jorgensen & Jacobsen, 2002). Finally, ochratoxin A occurrence in cereal grains from conventional and organic Polish
farms was almost the same (Czerwiecki, Czajkowska, &
Witkowska-Gwiazdowska, 2002).
The stability and persistence of fumonisins through food
processing has been reviewed by the European Mycotoxin
Awareness Network (EMAN, 2006). Dry milling of maize
results in distribution of fumonisins into diVerent milled
fractions so that concentrations in the bran, for example,
may be higher than in the original whole maize grains. In
experimental wet milling, fumonisin has been detected in
steep water, gluten, Wbre and germ, but not in the starch.
Fumonisins are quite stable and are not destroyed by
moderate heat (Castelo, Sumner, & Bullerman, 1998), however, an 80% reduction by heating at higher temperatures
has been reported (Visconti et al., 1999). However, caution
is required in assessing risk as it has been reported that
breakdown products such as ‘hydrolysed fumonisin’ may
be formed and these may be almost as toxic as the parent
compound (EMAN, 2006).
Even though there are only 30 occurrence data for each
type of corn, an estimation of dietary exposure to fumonisins from conventional and organic corn was carried out
(Table 2). In Spain, an average adult (70 kg) consumes
around 1.6 kg of corn per year (4.4 g/day), according to the
latest Food Supply and Commodity Balance Data (FAO,
2003). The mean fumonisin content of conventional corn
measured in this study was 65.1 ng/g (as the sum of FB1 and
Table 1
Descriptive analysis of fumonisins in conventional and organic corn samples
Corn type
Conventional
Organica
Total
n
a
30
30
60
Fumonisin B1
Fumonisin B2
Positive (%)
Mean
Maximum
Positive (%)
Mean
Maximum
13.3
10.0
11.7
43.2a
35.4a
39.3
354
359
359
10.0
6.7
8.3
21.9a
18.8a
20.4
120
153
153
The mean (expressed as ng/g) was calculated using one-half the LOQ for results lower than the LOQ (25 ng/g).
a
Comparison of conventional versus organic samples by ANOVA test, values with diVerent letters in a column are signiWcantly diVerent (p < 0.05).
A. Ariño et al. / Food Control 18 (2007) 1058–1062
1061
Table 2
Estimation of dietary intakes of fumonisins from conventional and organic maize
Corn type
Levels of FB1 + FB2 (ng/g)
Intake of FB1 + FB2 (ng/kg bw/day)
PMTDIa (g/kg bw/day)
% PMTDI
Conventional
Organic
Total
65.1
54.1
59.6
4.1
3.4
3.8
2
2
2
0.21
0.17
0.19
a
Provisional maximum tolerable daily intake, established by SCF (2003).
FB2). Then, the estimated daily intake of fumonisins was
4.1 ng/kg body weight/day, which is considerably lower
(0.21 %) than the PMTDI of 2 g/kg body weight/day
established by the ScientiWc Committee for Food of the
European Commission (SCF, 2003) (Table 2). Similarly,
considering the mean fumonisin content of organic corn
(54.1 ng/g), the estimated daily intake of 3.4 ng/kg body
weight/day only amounted to 0.17% of the PMTDI. Since
there is no data available on the consumption of organic
corn, the same intake of 4.4 g/day applied for conventional
maize has been used for this comparison. Furthermore, for
exposure assessment, it would be important to bear in mind
that fumonisins can be reduced from the Wrst post-harvest
treatment, from sieve process, to any process involving
water, temperature, humidity and time.
Based on the limited data exposed in this paper, the
fumonisins present in conventional and organic maize are
estimated to contribute with very low percentages of 0.21%
and 0.17%, respectively, to the level considered at risk for
human health. These estimated intakes are in the lower
range of those reported in the recent ScientiWc Cooperation
Task on Fusarium toxins in food and assessment of dietary
intake by the population of EU Member States (SCOOP,
2003). This report indicated that 46% and 42% of cerealbased food samples contained fumonisins B1 and B2,
respectively, and the range of average dietary intakes of the
sum of FB1 and FB2 for adults was between 0.1% and
14.1% (expressed as percent of PMTDI). However, higher
intakes up to 22.3% PMTDI were noted for young children.
It is well known that certain population groups are exposed
to higher intakes of fumonisins, such as people with gluten
intolerance, celiac or Dühring’s disease, vegetarians, infants
and alcohol consumers (Soriano & Dragacci, 2004b). However, in a quantitative risk assessment for fumonisins in US
corn, current dietary levels of fumonisins would not result
in renal lesions even at upper levels of exposure in high
maize eaters (Humphreys, Carrington, & Bolger, 2001).
In the neighbouring Portugal, fumonisins were detected
in 45% of 31 samples of corn and corn-based foods at mean
concentrations ranging from 64 to 995 ng/g (Lino, Silva,
Pena, & Silveira, 2006). According to data from Portuguese
Food Balance, maize consumption in 2003 reached 27.9 g
per person per day, and the authors calculated that the estimated daily intake of fumonisins was 0.14 g/kg body
weight (7% PMTDI).
The results of the present study indicated that, as far as
fumonisins are concerned, there is no scientiWcally tenable
evidence that the diVerences observed between conven-
tional and organic foodstuVs would lead to any objectively
measurable eVect on consumer health.
Acknowledgments
This research was supported by the Government of
Aragón (Spain) through Projects DGA/Grupos de Investigación Consolidados and PIP065/2005. We thank M.
Benito and J. Guilmin for their assistance in the laboratory
work, and F. Villa and the Aragonese Committee for
Organic Agriculture for the collection of samples.
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