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Ochratoxin A in conventional and organic cereal

derivatives: a survey of the Italian market, 2001–02
a a b a a a
R. Biffi , M. Munari , L. Dioguardi , C. Ballabio , A. Cattaneo , C. L. Galli & P.
a
Restani
a
Toxicology Laboratory , Department of Pharmacological Sciences, University of Milan , via
Balzaretti 9, I-20133 Milan, Italy
b
Istituto di Ingegneria Agraria , University of Milan , via Celoria 2, I-20133, Milan, Italy
Published online: 20 Feb 2007.

To cite this article: R. Biffi , M. Munari , L. Dioguardi , C. Ballabio , A. Cattaneo , C. L. Galli & P. Restani (2004) Ochratoxin A
in conventional and organic cereal derivatives: a survey of the Italian market, 2001–02, Food Additives & Contaminants, 21:6,
586-591, DOI: 10.1080/02652030410001687708

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 Food Additives and Contaminants, Vol. 21, No. 6 (June 2004), pp. 586–591
Ochratoxin A in conventional and organic cereal
derivatives: a survey of the Italian market, 2001–02
R. Biffi{, M. Munari{, L. Dioguardi{, C. Ballabio{,
A. Cattaneo{, C. L. Galli{ and P. Restani{*
{Toxicology Laboratory, Department of Pharmacological Sciences,
University of Milan, via Balzaretti 9, I-20133 Milan, Italy
{Istituto di Ingegneria Agraria, University of Milan, via Celoria 2,
I-20133, Milan, Italy
Downloaded by [University of California, San Francisco] at 23:06 22 February 2015
(Received 8 October 2003; revised 23 February 2004;
accepted 23 February 2004)
Ochratoxin A is a mycotoxin produced mainly by
Penicillium verrucosum and Aspergillus ochraceus.
Although typically considered a cereal contaminant, it
has also been detected in dried fruit, nuts, meat and
derivatives. To estimate the quantity of ochratoxin A
that might be ingested by Italian consumers from
these foods, 211 cereal derivatives (flours and bakery
products) were analysed by high-performance liquid
chromatography. Products were from conventional
and organic agriculture and from integrated pest
management agriculture. All commercial flours and
derivatives examined contained ochratoxin A at
concentrations very much below the legal limit
(3
g kg
1): the highest value, 0.816
g kg
1, was
detected in a sample of spelt whole flour from organic
agriculture. In many samples, the ochratoxin content
was below the limit of detection; only rarely did values
exceed 0.5
g kg
1. In baby foods, four samples were
above the particularly restrictive Italian legal limit of
0.5
g kg
1. Although some significant differences were
found between samples from conventional and organic
agriculture when some product categories were exam-
ined (namely, baby foods as semolina and rice creams),
no important difference was found between the two
types of agricultural practice when all types of cereal
derivatives were considered together.
Keywords: ochratoxin A, mycotoxins, cereals,
organic agriculture
* To whom correspondence should be addressed.
e-mail: patrizia.restani@unimi.it
Food Additives and Contaminants ISSN 0265–203X print/ISSN 1464–5122 online # 2004 Taylor & Francis Ltd
http://www.tandf.co.uk/journals
DOI: 10.1080/02652030410001687708
Introduction
Ochratoxin A (CAS no. 303-47-9) is a secondary
metabolite produced mainly by Penicillium verruco-
sum and Aspergillus ochraceus (Harwig et al. 1983,
Chelkowski et al. 1987, Frisvad and Lund 1993).
Usually considered a cereal contaminant (Jørgensen
et al. 1996, Scudamore and MacDonald 1998,
Scudamore et al. 1999), its presence has been also
reported in coffee (Tsubouchi et al. 1988, Jørgensen
1998), beer (Payen et al. 1983, Jørgensen 1998), dried
fruits (Ozay and Alperden 1991), wine (Zimmerli and
Dick 1996) and nuts (Cooper et al. 1982). Some
studies showed that ochratoxin A contamination is
mainly associated with storage (Moss 1996,
Scudamore et al. 1999); suitable post-harvest con-
ditions (temperature and moisture) are important to
prevent the growth of the fungi and the production of
the mycotoxin.
Human exposure to ochratoxin A has been shown
in several European countries by demonstrating its
presence in blood and milk (European Commission
1996).
Ochratoxin A causes renal toxicity, nephropathy,
renal cancer and immunosuppression in several
animal species, and independent clinical studies
(Radovanovich 1991, Tanchev and Dorossiev 1991,
IARC 1993) have linked exposure to ochratoxin A to
human Balkan endemic nephropathy.
Although there is insufficient evidence of a carcino-
genic effect in humans, the International Agency for
Research on Cancer has classified ochratoxin A as a
possible human carcinogen based on data in experi-
mental animals (IARC 1993).
At its 56th meeting, the Joint FAO/WHO Expert
Committee on Food Additives concluded that the
mechanisms by which ochratoxin A causes nephro-
toxicity and renal carcinogenicity are unknown,
although genotoxic and non-genotoxic modes of
action have been proposed (JECFA 2001). The
 Ochratoxin A in conventional and organic cereal derivatives
JECFA retained the previous established provisional
tolerable weekly intake of 0.1 mg kg
1 body weight
(bw), recommending a further review of the myco-
toxin in 2004, and it concluded that given the distri-
bution of ochratoxin contamination in cereals,
imposing a limit of 5 or 20 mg kg
1 would make no
significant difference to the average consumer’s intake
(JECFA 1996, 2001).
The Italian Ministry of Health (1999) adopted the
European Union limit of 3 mg kg
1 ochratoxin A for
cereal derivatives and established a further Italian
limit of 0.5 mg kg
1 for baby foods.
In view of the JECFA’s advice that ochratoxin A
intake should be monitored in different countries, the
Downloaded by [University of California, San Francisco] at 23:06 22 February 2015
present paper determined the concentration of ochra-
toxin A in cereal-based foods (commercial flours and
bakery products). Products resulting from different
agricultural practices were included to evaluate the
toxicological risk for specific groups of consumers
from these foods.
Materials and methods
A total of 211 batches (422 samples) of commercial
cereal-based foods were analysed, of which 77 were
from conventional agriculture (use of pesticides and
fertilizers), 96 from organic agriculture (without
synthetic pesticides and fertilizers) and 38 from
integrated pest management agriculture (using a few
selected conventional pesticides, bioregulators, phero-
mones, insect attractants, etc.). Ochratoxin A was
also determined in 30 samples of wheat flour and in
six samples of hard wheat flours immediately after
milling.
Commercial cereal derivatives (flours and bakery
products) were randomly selected in different super-
markets, while baby foods were from different phar-
macies and supermarkets; all samples were from
Northern Italy. Flours and derivatives were from
different brands and collected from March 2001 to
December 2002; for baby foods, all the different
batches commercialized in the period and in the
geographical area considered were collected.
Samples were analysed immediately after the pur-
chase (or collection at mill); samples were quartered
and two-quarters of each sample were carefully
587
blended. Each batch and each sample was analysed
at least twice.
Chemicals
Ochratoxin A from A. ochraceus (benzene free) was
from Sigma Aldrich (Milan, Italy); a stock concen-
trated solution was prepared in toluene–acetic acid
(99:1 v/v) at a final concentration of 1 mg ml
1 and
stored at
20 C.
The ochratoxin A working solution was prepared by
diluting the stock solution with the same solvent to
approximately 10 mg ml
1. The actual concentration
of the mycotoxin was calculated using an ultraviolet
light spectrophotometer set at 333 nm (" ¼ 5550)
(AOAC 1995, Jørgensen and Vahl 1999).
After suitable dilutions in water–methanol–acetic acid
(50:49:1 v/v/v), the working solution was used to
prepare the external calibration curve (0.50, 1, 2, 4,
8 and 12 ng ml).
To spike samples, the working solution was diluted
10 times using toluene–acetic acid (99:1 v/v).
High-performance liquid chromatography (HPLC)
The HPLC instrument was equipped with a 980-PU
Jasco pump (Tokyo, Japan), a Rheodyne 7125
injection system (Cotati, CA, USA) with a 100 ml
loop, and a 920-FP Jasco fluorescence detector
(Tokyo, Japan). The system was connected to a
SIC Chromatocorder 12 (Waters, Milford, MA,
USA).
An Inertsil ODS-3 analytical column (5 mm,
4.0  250 mm) preceded by an ODS-3 guard column
(5 mm, 4.0  10 mm; all GL Sciences, Inc., Tokyo,
Japan) was used. A 100-ml volume of sample was
injected. The mobile phase (water–acetonitrile–acetic
acid 50:49:1 v/v/v) was maintained at a flow rate
of 1 ml min
1 and the Column Heater 7971 (Jones
Chromatography, Hengoed, UK) was set at 40 C.
The fluorescence detector was operated at
ex ¼ 333 nm and em ¼ 443 nm (Scudamore and
MacDonald 1998). LC-grade solvents were from
Lab-Scan (Dublin, Ireland).
 588 R. Biffi et al.
Sample preparation
The samples of cereal-based foods were extracted and
cleaned up according to Scudamore and MacDonald
(1998) with some modifications. A 10-g portion of
sample was extracted with 40-ml acetonitrile–water
(60:40 v/v) using high-speed blending for 2 min. The
mixture was centrifuged (J2-21 Centrifuge, Beckman
Instruments, Inc., Palo Alto, CA, USA) at 6000 rpm
for 25 min at 4 C and a 9-ml aliquot was diluted with
99 ml phosphate buffer solution (PBS). The whole
extract (108 ml) was added to an immunoaffinity
column, OchraTest (Vicam, Digen, Oxford, UK), at
a flow rate of 3 ml min
1. The column was washed
by passing 20 ml LC-grade water at approximately
Downloaded by [University of California, San Francisco] at 23:06 22 February 2015
6 ml min
1 and all remaining liquid was removed
from the column at the end of elution. Ochratoxin A
was collected by eluting with 1.5 ml methanol–acetic
acid (98:2 v/v). The eluates were dried under nitrogen
and suspended in 300 ml water–methanol–acetic acid
(50:49:1). A 100-ml portion was subjected to HPLC.
To estimate the percentage recovery, flours samples
(10 g) were spiked with 3 ng ochratoxin A (30 ml of a
standard solution containing 0.1 mg ml
1) and stored
overnight at 4 C. A spiked sample was prepared for
every group of six analyses.
Statistical analysis
The significance of the difference between the means
was calculated by analysis of variance and then by a
Student’s t-test.
Figure 1. HPLC chromatogram of a sample of hard whole wheat flour after extraction of ochratoxin A and purification
through an immunoaffinity chromatography column. The sample illustrated contains 0.309 g kg
1 ochratoxin A.
Results
An example of HPLC analysis is shown in figure 1.
The ochratoxin A retention time was close to 10 min.
The detection and reliable quantitation limits of this
technique were 0.025 and 0.050 ng, corresponding
to 0.06 and 0.13 mg kg
1, respectively. The recovery
ranged between 78 and 103%.
Table 1 shows the mean, standard deviation, median
and range of ochratoxin A contents in all cereal
products analysed. The last column shows the num-
ber of samples exceeding the legal limits: 0.5 mg kg
1
for baby foods (Italian directive) and 3 mg kg
1 for
other cereal derivatives (European directive).
All samples of commercial cereal derivatives were
below the legal limit, while four samples of baby food
(two semolinas from conventional agriculture and
two rice creams from organic agriculture) were above
the Italian limit of 0.5 mg kg
1. There was no signifi-
cant difference between similar samples from conven-
tional and organic agriculture in commercial flours
and derivatives, while some differences were observed
in baby foods. Semolina from conventional agricul-
ture had a higher content of mycotoxin than the
corresponding products from organic agriculture
and integrated pest management agriculture
( p < 0.01 and <0.005, respectively). By contrast, rice
formulas from organic agriculture were the more
contaminated ( p < 0.01 versus conventional agricul-
ture, and p ¼ 0.02 versus integrated pest management
agriculture). All baby foods from integrated pest
management agriculture contained ochratoxin A
below the limit of detection (0.025 mg kg
1).
 Ochratoxin A in conventional and organic cereal derivatives 589

Table 1. Ochratoxin A content (
g kg
1) in cereal flours and derivatives found in the Italian market, 2001
02.
Samples above
Agricultural Number of Mean* Median Range legal limits
Cereal Product practices batches (mg kg
1) SD (mg kg
1) (mg kg
1) (n)

Wheat Flour CV 14 0.134 0.146 0.069 ND–0.157 0

OR 11 0.053 0.069 ND ND–0.219 0
Whole flour OR 8 0.210 0.232 0.136 ND–0.700 0
Crackers OR 1 ND – – – 0
Hard wheat Flour CV 8 0.223 0.146 0.235 0.041–0.536 0
OR 4 0.246 0.239 0.170 ND–0.636 0
Whole flour OR 2 0.189 – 0.189 0.068–0.309 0
Baby food CV 10 0.234 0.231 0.173 ND–0.650 2
IPM 10 ND – ND ND 0
OR 10 0.027 0.050 ND ND–0.177 0
Corn Flour CV 9 0.170 0.056 0.160 0.100–0.267 0
Downloaded by [University of California, San Francisco] at 23:06 22 February 2015

OR 4 0.037 0.036 0.021 ND–0.097 0

Whole flour CV 2 0.115 – 0.115 0.015–0.215 0
OR 1 0.198 – – – 0
Baby food CV 10 ND – ND ND 0
(þ tapioca) IPM 10 ND – ND ND 0
OR 10 ND – ND ND 0
Spelt Whole flour OR 3 0.399 0.298 0.246 0.136–0.816 0
Crackers OR 2 0.023 – 0.023 ND–0.045 0
Extruded OR 1 0.03 – – – 0
Oats Whole flour OR 2 0.221 – 0.221 ND–0.441 0
Barley Whole flour OR 2 ND – ND – 0
Pearl CV 1 ND – – – 0
Rye Whole flour OR 4 0.347 0.459 0.117 0.045–1.15 0
Rice Whole flour OR 3 0.071 0.056 0.056 0.012–0.147 0
Crackers OR 3 ND – ND ND 0
Baby food CV 13 ND – ND ND 0
IPM 9 ND – ND ND 0
OR 11 0.228 0.725 ND ND–0.736 2
Multicereal Crackers OR 3 1.439 0.591 1.277 0.81–2.23 0
Baby food CV 10 0.159 0.098 0.180 ND–0.315 0
IPM 9 ND – ND ND 0
OR 11 ND – ND ND 0
CV, conventional agriculture; OR, organic agriculture.
IPM, integrated pest management agriculture; ND, not detectable.
*To calculate averages and standard deviations, values below the limit of detection were considered as 0.06 mg kg
1 and those between the limit of
detection and limit of quantification as such.

To evaluate the role of storage in the development
of fungi producing ochratoxin A, several samples
of wheat and hard wheat flours were analysed
immediately after milling. The content of mycotoxin
immediately after milling was compared with that
in commercial products (figure 2). The values in
wheat flours measured at the mill and at retailers
were similar: 0.074  0.025 mg kg
1 (mean  SE) in
flour from the mill versus 0.134  0.039 and
0.053  0.21 for conventional and organic commercial
flours, respectively. A different ochratoxin A content
was found for flour from hard wheat: from
0.057  0.021 mg kg
1 (mean  SE) in newly milled
flour to 0.223  0.052 and 0.246  0.12 for conven-
tional and organic commercial flours, respectively.
Discussion and conclusions
The presence of ochratoxin A is usually associated
with cereals and derivatives, although recent data
have shown that other sources can contribute signifi-
cantly to the total intake of the mycotoxin. In recent
 590
0,4
Ochratoxin A concentration (µg/kg)
0,3
0,2
0,1
Downloaded by [University of California, San Francisco] at 23:06 22 February 2015
0
mill CV
wheat flour
Figure 2. Ochratoxin A concentrations (mean þ SE) in
flour samples directly from the mill and from commercial
retailers. Mill samples were from conventional agricul-
ture; commercial products were from conventional (CV)
and organic agriculture (OR).
years, the market for organic products has greatly
increased, and some concern has been raised that
this agricultural practice could be more likely to
encourage development of mycotoxin-producing
fungi. Several papers have been published on this
topic (e.g., for ochratoxin A: Beretta et al. 2002,
Czerwiecki et al. 2002a, b).
The present study analysed a large number of
commercial products found in the Italian market in
2001
02, paying particular attention to products
from organic agriculture. All organic foods analysed
were chosen from those that had received European
Union certification according to the European
Union Legislation No. 2092/91 and subsequent
modifications.
All commercial flours and derivatives contained
ochratoxin A in quantities very much below the legal
limit (3 mg kg
1): the highest value, 0.816 mg kg
1, was
detected in a sample of spelt whole flour from organic
agriculture. In many samples, the ochratoxin A con-
tent was below the limit of detection and only rarely
did values exceed 0.5 mg kg
1.
In baby foods, four samples were found above the
Italian permitted level of 0.5 mg kg
1.
R. Biffi et al.
A few significant differences were found between
samples from conventional and organic agriculture
when specific categories of products were evaluated
(namely, baby-food semolinas and rice creams), no
important difference was found between the two types
of agricultural practice when all kinds of cereal
derivatives were considered.
An important finding is that all baby foods from
integrated pest management agriculture presented
an undetectable quantity of ochratoxin A, probably
because of the strict quality control performed by the
producing industry (one trade mark) on raw materials
and on the final products.
OR mill CV OR
Estimated daily intake of ochratoxin A from
consumption of commercial cereal derivatives
hard wheat flour
In Mediterranean countries, cereals and their deriva-
tives are traditionally important components of the
diet both during weaning and adult life. In Europe,
the average cereal consumption for an adult has
been estimated as 226.3 g day
1 (GEMS/Food 1998).
Accepting this and assuming a bw of 60 kg and a
worst contamination of 0.816 mg kg
1, the average
daily intake of ochratoxin A would be 3.08 ng kg
1
bw or 21.6 ng kg
1 bw week
1.
On the basis of the report of the Joint FAO/WHO
Expert Committee on Food Additives (JECFA 1996,
2001), which declared a provisional tolerable weekly
intake of 100 ng kg
1 bw for ochratoxin A, it can be
concluded that there is no significant toxicological
risk for the Italian consumer.
Similarly, there is no significant risk for a child
who occasionally consumes a baby food containing
ochratoxin A at a level slightly above the Italian limit
(0.74 mg kg
1), since the intake would be approxi-
mately 2.28 ng kg
1 bw day
1.
Thus, the average consumption for Italian consumers
seems to be on the safe side, but as an increasing
number of food sources are contaminated by ochra-
toxin A, strict quality control, with rejection of rogue
batches, will need to be performed.
Acknowledgements
Research was supported by MiPAF (Ministero
delle Politiche Agricole e Forestali). The authors
 Ochratoxin A in conventional and organic cereal derivatives
thank Professor Peter Woodford for editorial
assistance.
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