SURVEY

Ital. J. Food Sci., vol. 27 - 2015 271

- Keywords: Aspergillus, carry-over, ELISA -

A ONE-YEAR SURVEY ON AFLATOXIN M1 
IN RAW MILK

M. SCHIRONE1, P. VISCIANO1*, A.M.A. OLIVASTRI2, R. TOFALO1, 
G. PERPETUINI1 and G. SUZZI1

1Facoltà di BioScienze e Tecnologie Agro-Alimentari e Ambientali, Università di Teramo, 
Via C.R. Lerici 1, 64023 Mosciano Sant’Angelo, Teramo, Italy

2Azienda Sanitaria Unica Regionale Marche - Ascoli Piceno, Italy
* Corresponding author: Tel. +39 0861 266911, Fax +39 0861 266940,

email: pvisciano@unite.it

ABSTRACT

In the year 2012, 288 raw milk samples were collected from six different dairy cow farms and 
analyzed for the presence of aflatoxin M

1
 (AFM

1
) using the ELISA technique. The AFM

1
 levels 

ranged from 5 to 25 ng/kg and the highest concentrations were found in autumn, with a signif-
icant difference (p<0.05) between February and November. The EU legal limit of 50 ng/kg has 
never been exceeded. Even if the results of the present study show a low risk for AFM

1
, its occur-

rence in dairy products has to be regularly monitored due to their importance as foodstuffs for 
people and children above all.

mailto:pvisciano@unite.it


272 Ital. J. Food Sci., vol. 27 - 2015

INTRODUCTION

Nowadays food industry has the responsibil-
ity to develop and implement a Hazard Analy-
sis and Critical Control Point (HACCP) system 
aiming at identifying and preventing important 
hazards to food safety. The presence of aflatox-
ins (AFs) in dairy products is one of the most 
important critical control points to be checked 
in raw milk supplies. Aflatoxins are secondary 
metabolites mainly produced by three species of 
Aspergillus including Aspergillus flavus, Asper-
gillus parasiticus and Aspergillus nomius (CRAP-
PY, 2002). Even if eighteen AFs have been iden-
tified, only four out of them have been found in 
food and feed, i.e. AFB

1
, AFB

2
, AFG

1
 and AFG

2 
(HESHMATI and MILANI, 2010). The toxic effects 
of these compounds can be both acute, thus 
causing hepatitis, oedema or hemorrhagic ne-
crosis, and chronic, thus resulting in liver, lung 
and kidney carcinomas as well as immunosup-
pression (WILLIAMS et al., 2004). In particular, 
AFB

1
 shows different toxic activities, including 

teratogenicity, mutagenicity and carcinogenicity 
(MCLEAN and DUTTON, 1995). Therefore, the In-
ternational Agency for Research on Cancer (IARC) 
has included AFB

1
 in group 1 as a human car-

cinogen (IARC, 1993). Animals eating contami-
nated feed rapidly adsorb and transfer AFB

1 
to 

the liver, where it is metabolized into the 4-hy-
droxylated derivate AFM

1 
and excreted through 

faeces and urine (POLONELLI et al., 2011). Con-
sequently, AFM

1
 may be secreted in mammali-

an milk by means of a carry-over process, with-
in 12-24 h after the ingestion of AFB

1
 (KAV et 

al., 2011). AFM
1
 exhibits a high level of genotox-

ic activity due to its possible accumulation and 
linkage to DNA (SHUNDO and SABINO, 2006). It 
can cause DNA damage, gene mutation, chro-
mosomal anomalies and cell transformation in 
in-vitro mammalian cells, insects, lower eukar-
yotes and bacteria (PRANDINI et al., 2009). For 
that reason, AFM

1
 has been included in group 

1 (IARC, 2002) and removed from group 2B (i.e. 
as a possible human carcinogen). 

Sources of AFs contamination in animal food-
stuffs may vary geographically, with prevalence 
in areas with favorable environmental and cli-
matic conditions. Aspergillus flavus and A. par-
asiticus colonize plants when still in the field, 
mainly when damaged; the highest AFs produc-
tion occurs at temperatures between 20° and 
30°C. In particular, A. parasiticus prefers a soil 
environment and can be found more commonly 
on peanuts, while A. flavus is better adapted to 
an aerial environment and colonizes cotton and 
corn (PRANDINI et al., 2009). These molds can 
also colonize products in post-harvest if not ad-
equately stored. However, the relationship be-
tween the amount of AFB

1
 ingested by animals 

and the quantity of AFM
1
 in milk is quite vari-

able, as many factors – such as the individual 
variability among animals, the presence of ud-

der infections, and the lactation period (at the 
beginning the carry-over is 3.3-3.5 times great-
er compared to the advanced lactation) – can af-
fect carry-over (VAN EGMOND, 1989). The maxi-
mum limit for AFM

1
 concentration in food varies 

in the legislation of different countries (GODIČ 
TORKAR and VENGUŠT, 2008). The European 
Community has prescribed a limit of 50 ng/
kg in raw milk, heat-treated milk and milk for 
the manufacture of milk-based products (EC, 
2006) while, according to US regulations, the 
action level of AFM

1
 in milk should not be high-

er than 500 ng/kg (GHANEM and ORFI, 2009). 
AFM

1
 is relatively stable in raw and processed 

milk products and is not affected by pasteur-
ization or cheesemaking processes performed 
in dairy industry (KAV et al., 2011). It has been 
reported that AFM

1 
concentration in dairy prod-

ucts can be 3 to 4 times higher than in milk, 
as it is associated with milk proteins (BATTA-
CONE et al., 2003). 

The present study aims at detecting the AFM
1 

levels in bovine raw milk designed to a dairy fac-
tory located in the Marche region, central Italy. 
The preventive action used by such factory to 
control this hazard will also be discussed. The 
samples were analyzed by means of an enzyme-
linked immunosorbent assay (ELISA) that is the 
most representative method for the fast screen-
ing analysis of AFs.

MATERIALS AND METHODS

A total of 288 samples of raw milk collected 
from six different suppliers (named 1 to 6) locat-
ed in the Marche region, central Italy, were ex-
amined over the year 2012. Raw milk samples 
from each farm were provided to that dairy fac-
tory four times in a month and were transported 
in tanks at 0-4°C. All samples were analyzed in 
duplicate. Such raw milk samples (10 mL) were 
at first centrifuged at 3,500 g for 10 min at 4°C, 
then the upper cream layer was completely re-
moved. A sample unit of 100 µL was used for 
the quantitative analysis of AFM

1
 using the com-

mercial kit RIDASCREEN (R-Biopharm, Germa-
ny). Such kit includes microtiter plates coated 
with capture antibodies, AFM

1
 standard solu-

tions used for the construction of the calibration 
curve, peroxidase-conjugated AFM

1
, substrate 

(urea peroxidase), chromogen (tetramethylben-
zidine) and stop reagents 1 N sulfuric acid. The 
test procedure was performed according to HES-
HMATI and MILANI (2010). The evaluation of AFM

1
 

was obtained dividing the absorbance values of 
the standards and the samples by the absorb-
ance value of the first standard (zero standard), 
then multiplying the result by 100 (percentage 
of maximum absorbance). The adsorption was 
inversely proportional to the AFM

1
 concentration 

in samples. The limit of quantitation according 
to the kit was 5 ng/kg. 



Ital. J. Food Sci., vol. 27 - 2015 273

A statistical analysis was carried out by 
GraphPad InStat Version 3.0, GraphPad Soft-
ware (San Diego, California, USA). All the ob-
tained data were assessed for normality by 
means of Kolmogorov-Smirnov test. Since the 
values were not normally distributed, non-para-
metric tests were applied. The differences among 
the values obtained from the six different suppli-
ers and among the milk samples collected over 
12 months were evaluated by Kruskal-Wallis 
Test (non-parametric ANOVA). When the p value 
was lower than 0.05, the Dunn’s Multiple Com-
parisons Test was used.

RESULTS AND CONCLUSIONS

The mean AFM
1 
concentrations in four collec-

tions (analyzed in duplicate) of raw milk over a 
month (for a total of 12 months) from each dairy 
farm are reported in Table 1. The levels ranged 
from the limit of quantitation (5 ng/kg) to a max-
imum of 25 ng/kg, with the highest values ob-
served in the months of September, October and 
November. However, no sample exceeded the 
maximum levels (50 ng/kg) set for AFM

1
 in milk 

by EU legislation (EC, 2006). No significant dif-
ference (p>0.05) was also observed among the 
AFM

1 
concentrations in samples from the dif-

ferent suppliers, while a significant difference 
(p<0.05) was noticed only between the values 
obtained in February and November. 

According to the HACCP plan implemented 
in the dairy factory of the present study, AFM

1
 

content is regularly monitored four times in a 
month but, when it results to be higher than 10 
ng/kg, the supplier is contacted (as a preven-
tive action) and analyses of raw milk from the 
matching dairy farm are repeated at the next 
supply. In this study (Table 2), 68.4% of the 
samples contained AFM

1
 in the range of 5-10 

ng/kg, while 27.1% was in the range of 11-19 
ng/kg, exceeding the above mentioned preven-
tive limit (10 ng/kg). Moreover, the dairy facto-
ry has set an internal system of corrective ac-
tions when AFM

1 
content exceeds 20 ng/kg, 

defined as action limit. In the present study, 
the action limit was exceeded only in 4.5% of 
the samples collected from some dairy farms 
in different months (i.e. January, September, 
October, November and December), with val-
ues ranging from 20 ng/kg to a maximum of 
25 ng/kg. In that case the supply of milk from 
the dairy farm is suspended until concentra-
tions return to regular values. Whereas, if such 
value exceeds 50 ng/kg (the maximum level by 
law), the positive sample is analyzed by means 
of the HPLC as confirmatory assay, and milk 
has then to be intended as “Category 2 materi-
al” according to the EU regulations on animal 
by-products (EC, 2009). However, as a preven-
tive measure, the HPLC procedure is routinely 
performed every four months. T

a
b
le

 1
 -

 C
o
n

ce
n

tr
a
ti

o
n

s 
o
f 
A

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M

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 (
n

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n

d
 r

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 (
in

 p
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re

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th

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es

) 
fo

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ea

ch
 s

ix
 s

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p
p
li
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s 
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 t
h

e 
ye

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r 

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1
2
.

S
up

pl
ie

r
Ja

nu
ar

y
Fe

br
ua

ry
a

M
ar

ch
A

pr
il

M
ay

Ju
ne

Ju
ly

A
ug

us
t

S
ep

te
m

be
r

O
ct

ob
er

N
ov

em
be

rb
D

ec
em

be
r

1
N

D
N

D
12

.5
±2

.9
*

(5
.0

-1
5.

0)
10

.0
±3

.3
(5

.0
-1

5.
0)

N
D

7.5
±2

.9
(5

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5.
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N
D

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10

±3
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(5
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5.

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±2
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5.

0)
9.

0±
3.

2
(5

.0
-1

5.
0)

11
.8

±4
.8

(5
.0

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2.

0)
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±3

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(5

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8.
0)

2
8.

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3
(5

.0
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0.
0)

N
D

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8±

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0

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9
(5

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5.
0)

9.
0±

3.
2

(5
.0

-1
5.

0)
N

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10

.0
±3

.3
(5

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5.
0)

13
.4

±2
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(5
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7.0

)
15

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(1

5.
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15

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(5

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5.
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9.
3±

2.
9

(5
.0

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5.

0)
10

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.3
(5

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-1

5.
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3
13

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±5

.5
(5

.0
-2

4.
0)

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D

N
D

7.5
±2

.9
(5

.0
-1

5.
0)

9.
0±

3.
2

(5
.0

-1
5.

0)
N

D
N

D
N

D
17

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±0

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(1

5.
0-

18
.0

)
10

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±4

.3
(5

.0
-1

9.
0)

11
.0

±4
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(5
.0

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9.

0)
7.5

±2
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(5
.0

-1
5.

0)

4
6.

8±
2.

0
(5

.0
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2.
0)

7.0
±2

.6
(5

.0
-1

5.
0)

N
D

N
D

9.
0±

3.
2

(5
.0

-1
5.

0)
6.

8±
2.

0
(5

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2.
0)

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D

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2.
6

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5.

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5
N

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9.

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2.

9
(5

.0
-1

5.
0)

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D

7.6
±3

.4
(5

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-1

8.
0)

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±2

.9
(5

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-1

5.
0)

9.
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3.
3

(5
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6.

0)
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(1

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17

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(5

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5.

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6
N

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at
a 

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se

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an

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rd

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rr

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; N

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= 

A
FM

1<
 5

 n
g/

kg
; a

,b
 (p

<0
.0

5)



274 Ital. J. Food Sci., vol. 27 - 2015

In Figure 1 the mean content of AFM
1
 in milk 

per month was reported, without considering 
the different suppliers. 

In the present study, the overall contamina-
tion levels of AFM

1
 in milk samples were lower 

than those reported by other authors (HAN et al., 
2013; HUSSAIN and ANWAR, 2008; RAHIMI and 
AMERI, 2012; TAJIK et al., 2007). These differ-
ences could be due to several factors, including 
different analytical techniques, samples size, 
season of the year, livestock management, and 
dairy processing systems. Moreover, the AFM

1
 

levels in milk seemed to be significantly influ-
enced by the geographical region. The outcomes 
of some studies carried out in Italy showed an 
AFM

1
 concentration range of 2-90 ng/kg (NACHT-

MANN et al., 2007) and < 23 ng/kg (GALVANO et 
al., 2001). In 2003, the risk of mycotoxins was 
brought to public attention following the indi-
cation of the presence of unusual amounts of 
AFM

1
 in milk, in northern Italy in particular. At 

the beginning controls aimed at checking that 
the levels in milk did not exceed the limit estab-

lished by law, but special monitoring plans were 
coordinated for milk and feed towards the end 
of 2003 due to an alarming amount of positiv-
ity in the self-check plan carried out on milk. 
Maybe the positive levels found in feed at the 
end of 2003 were the consequence of partic-
ularly unusual climatic conditions (high tem-
peratures and drought lasting more than four 
months) that characterized the summer in the 
year 2003 (DECASTELLI et al., 2007). Such ap-
proach – i.e. paying particular attention to the 
correlation in milk-feed monitoring procedures 
– could be considered particularly valid in order 
to find contaminated batches starting from con-
trols on milk. In fact, many countries in Europe 
have shown relatively low levels of AFM

1
 contam-

ination in milk samples as a result of stringent 
rules on AFB

1
 in dairy cattle feed (TRUCKSESS, 

2006). In the present study AFM
1 
concentrations 

were not very high and that result could be due 
to the feeding practices in dairy cow farms. The 
lower limits adopted by this dairy factory could 
be particularly effective, above all when the Ital-
ian Ministry of Health established an increase in 
milk analyses in order to detect AFM

1
 following a 

series of notifications on AFB
1
 in maize of Euro-

pean origin by the Rapid Alert System for Food 
and Feed (RASFF) since the last maize harvest 
in autumn 2012 (ANONYMOUS, 2012). In order 
to control AFM

1
 levels in milk it is necessary to 

reduce AFB
1
 contamination of feed for dairy cat-

tle by preventing fungal growth and AFB
1
 for-

mation in agricultural commodities. That pur-
pose can be achieved through some agricultural 
practices, such as the choice of hybrids, seeding 
time and density, suitable ploughing and fertir-
rigation, and stricter chemical or biological con-
trols. Cereals harvested with the lowest possible 
moisture and conservation moisture close to or 
less than 14% are necessary to reduce contam-
ination risks. Furthermore, kernel mechanical 

Table 2 - Distribution of AFM
1
 in raw milk samples.

Months  Range of AFM
1
 concentrations (ng/kg)

 5-10 11-19 20-25
 Number  of samples (%) Number of samples (%) Number of samples (%)

January 20 (83.4) 2 (8.3) 2  (8.3)
February 23 (95.8) 1 (4.2) -
March 17 (70.8) 7 (29.2) -
April 19   (79.2) 5 (20.8) -
May 16 (66.7) 8 (33.3) -
June 22 (91.7) 2 (8.3) -
July 21 (87.5) 3 (12.5) -
August 15 (62.5) 9 (37.5) -
September 9 (37.5) 14 (58.3) 1 (4.2)
October 9 (37.5) 12 (50.0) 3 (12.5)
November 12 (50.0) 8 (33.3) 4 (16.7)
December 13 (54.2) 10 (41.6) 1 (4.2)

- = no sample.

Fig. 1 - Mean content of AFM
1
 in milk per month.



Ital. J. Food Sci., vol. 27 - 2015 275

damage, grain cleaning practices and conserva-
tion temperature are also factors which need to 
be carefully controlled (PRANDINI et al., 2009).

A marked seasonal variation in AFM
1
 levels 

in milk has been previously reported (KAMKAR, 
2005; RAHIMI and AMERI, 2012; RUANGWISES 
and RUANGWISES, 2010). It has been reported 
that AFs levels in feed are higher in rainy than in 
dry seasons. Moreover, the use of high amounts 
of contaminated concentrates is more frequent 
in cold months (KAMKAR et al., 2011). Although 
no significant differences were observed in AFM

1
 

levels among the different months, except be-
tween February and November, the results of 
the present study shows that the mean concen-
trations in raw milk samples collected in au-
tumn were higher than in other seasons. Such 
variation may be a result of toxin accumulation 
when storage occurs in hot and humid condi-
tions. Many authors (BLANCO et al., 1988; LO-
PEZ et al., 2003; KAMKAR, 2005) reported on a 
higher number of yeasts, moulds and conse-
quently on a higher concentration of mycotox-
ins in ensiled feed, mostly used in autumn or 
winter. Also DASHTI et al. (2003) observed that 
the contamination levels in the samples from 
local companies were higher in winter than in 
summer. That could be explained by the pro-
longed storage required for feed, which would 
provide favorable conditions for fungi to grow; or 
by the use of contaminated feed for the animals 
in winter, in addition to other factors such as 
temperature and relative humidity, agricultur-
al products used as animal feed as well as sea-
sonal effects from the country of origin of feed. 
Two other studies showed similar results – i.e., 
AFM

1
 contamination is higher in winter than in 

summer. The first study was conducted in five 
regions of Iran on ninety-eight samples of raw 
milk analyzed in order to observe the possible 
presence of AFM

1
. All samples resulted positive 

for AFM
1
 with an overall mean level of 53 ng/L. 

The levels of AFM
1
 were also higher in winter and 

spring than in summer and autumn (TAJKARIMI 
et al., 2007). The second study was carried out 
in Sarab City, Iran, and showed that 76.6% of 
111 raw milk samples was positive, with AFM

1
 

levels ranging between 15 and 280 ng/L. The 
lowest AFM

1
 levels (24 ng/L) were found in Au-

gust and the highest (118 ng/L) in December 
(KAMKAR, 2005).

In conclusion, the occurrence of AFM
1
 in milk 

intended for human consumption is a critical 
control point to be steadily monitored in dairy 
products. Controls of the supply chain from feed-
stuffs for lactating cows to milk production rep-
resents the key to guarantee the safety of the end 
product, due to the large variation in the content 
of AFB

1
 in animal feed and consequently of AFM

1 
in milk. Even if the risk of a high AFM

1
 content 

appears limited, it is certainly of great interest to 
implement a valid system of regular monitoring 
in order to have always safe raw materials. Es-

tablishing more restrictive limits, as those cho-
sen by the dairy factory, taken as a case-study 
in the present paper, could be a good approach 
to achieve a better food quality for consumers.

ACKNOWLEDGEMENTS

The authors thank Francesca Rosati, University of Teramo, 
for her support in editing the English text.

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Paper Received February 14, 2014  Accepted August 6, 2014