Food Control 62 (2016) 104109

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Occurrence of Listeria monocytogenes and Salmonella spp. in meat

processed products from industrial plants in Southern Italy
Valeria DOstuni a,1, Mariana Tristezza b,1, Maria Grazia De Giorgi a, Patrizia Rampino c,
Francesco Grieco b,, Carla Perrotta c
a
Studio di Microbiologia ed Ecologia S.r.l., Via S. Nicola 87, 73100, Lecce, Italy
b
Istituto di Scienze delle Produzioni Alimentari, Consiglio Nazionale delle Ricerche, Unit Operativa di Supporto di Lecce, Via Prov. Lecce-Monteroni, 73100,
Lecce, Italy
c
Dip. di Scienze e Tecnologie Biologiche ed Ambientali, Universit del Salento, Via Prov. Lecce-Monteroni, 73100, Lecce, Italy

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

Article history: The main goal of the present investigation was to assess the microbiological safety of two typical meat-
Received 7 July 2015 derived products, i.e. raw pork sausages and entrails lamb rolls, produced in Salento (Apulia, Southern
Received in revised form 5 October 2015
Italy). Analyses were carried out for 7 years (from 2008 to 2014) and a total number of 6720 samples
Accepted 20 October 2015
was collected by specialized personnel. The presence of Listeria monocytogenes and Salmonella spp. was
Available online 23 October 2015
detected by a PCR-based assay, combined with culturing in enrichment broth. The prevalence of L. mono-
Keywords: cytogenes was assessed in 2.4% entrails lamb rolls and in 4.2% raw pork sausages samples, whereas the
Meat products occurrence of Salmonella spp. was revealed in 2.7% lamb rolls and in 3.5% pork sausages. A statistically
Raw pork sausages signicant seasonal variation was found in the occurrence of L. monocytogenes; in fact a higher number
Entrails lamb rolls of samples contaminated by this pathogen was recorded in spring and autumn. On the contrary, no sig-
Listeria monocytogenes nicant seasonal changes occurred in the prevalence of Salmonella spp. The data reported indicate that,
Salmonella spp
due to the presence of these pathogens, the Italian food processors need to improve the microbiological
monitoring of the processing chains, in order to guarantee health safety.
2015 Elsevier Ltd. All rights reserved.

1. Introduction bacteria such as Listeria monocytogenes and Salmonella spp., which

Foods of animal origin, and especially meat, are important com-
ponent of human diet constituting an essential supply of valuable
nutrients, however sometimes they also represent the source of
serious food-borne infections. Epidemics related to meat products
consumption produce both harsh health impact in the long term
and important economic loss to the food industry (Anonymous,
2013; Olsen et al., 2005). Therefore, in order to ensure product
safety, it is ultimate to detect and estimate the contamination
sources of meat-derived foods in the raw materials and along pro-
cessing plants (Rhoades, Duffy, & Koutsoumanis, 2009). Poor hy-
gienic levels of meat raw materials may be a source of pathogenic
Corresponding author.
E-mail addresses: valeriadostuni@hotmail.it (V. DOstuni), mariana.tristezza@
unifg.it (M. Tristezza), microbiostudio14@gmail.com (M.G. De Giorgi), patrizia.
rampino@unisalento.it (P. Rampino), francesco.grieco@ispa.cnr.it (F. Grieco),
carla.perrotta@unisalento.it (C. Perrotta).
1
Both authors equally contributed to this work.
have often been related with outbreaks of human salmonellosis
(82,694 conrmed cases, 0.14% fatality rate) and listeriosis (1763
conrmed cases, 15.68% fatality rate) in 2012 in Europe (EFSA,
2014).
Salmonella is a Gram negative rod-shaped bacterium, it is one
of the major food-borne pathogen and it is present in the gastroin-
testinal tract of animals. It can be found in foods of animal origin
like raw meat, and its derivatives, causing infections and intoxica-
tions (Anonymous, 2012; EFSA, 2014). The number of salmonellosis
cases is increasing and the inspection of food for the presence of
Salmonella is becoming a routine all over the world.
Another microorganism whose presence is a concern for food
industry is L. monocytogenes, a Gram positive pathogen contam-
inating unprocessed food like raw meat, sh and milk, since it
is widely present either in the environment or along production
plants (Larsen et al., 2014). This bacterium can be also found in
some processed foods such as cheese, ice cream, and processed
meat because of post-processing contamination.
Because of their ability to survive unfavorable conditions, these

http://dx.doi.org/10.1016/j.foodcont.2015.10.025
0956-7135/ 2015 Elsevier Ltd. All rights reserved.
 V. DOstuni et al. / Food Control 62 (2016) 104109 105

Table 1
Microbial quality of raw meat products for three processing plants in Salento (Southern Italy) during a seven-years period (20082014).

Plant Product Total Detection Negative samples (%) Positive samples (%)

A Rolls 3627 L. monocytogenes 3589 (99.0) 38 (1.0)

Salmonella spp. 3612 (99.6) 15 (0.4)
Sausages 559 L. monocytogenes 548 (98.0) 11 (2.0)
Salmonella spp. 546 (97.7) 13 (2.3)
B Rolls 1491 L. monocytogenes 1408 (94.4) 83 (5.6)
Salmonella spp. 1382 (92.7) 109 (7.3)
Sausages 932 L. monocytogenes 878 (94.2) 54 (5.8)
Salmonella spp. 891 (95.6) 41 (4.4)
C Rolls 303 L. monocytogenes 299 (98.7) 4 (1.3)
Salmonella spp. 292 (96.3) 11 (3.6)
Sausages 168 L. monocytogenes 164 (97.6) 4 (2.4)
Salmonella spp. 164 (97.6) 4 (2.4)

pathogens represent a high concern for the meat industries (Sofos
& Geornaras, 2010). It is important to note that the variety
and amount of the above pathogen incidence in the process-
ing plants are strongly related to the origin of raw materials
and to the insucient hygiene of staff involved in production
(Sofos, 2014). The isolation of L. monocytogenes and Salmonella
spp. from meat processing environments indicates the proba-
ble persistence of these pathogenic strains, thus conrming the
need for sanitation procedures improvement (Vongkamjan, Roof,
Stasiewicz, & Wiedmann, 2013; Yildirim, Gonulalan, Pamuk, &
Ertas, 2011). Due to this reason, it is highly required to iden-
tify these pathogens combining traditional microbiological meth-
ods with modern molecular approaches, such as Polymerase Chain
Reaction (Dalmasso et al., 2014; Jofr et al., 2005; Kawasaki
et al., 2005) or Pulse Field Gel Electrophoresis (Senczek, Stephan,
& Untermann, 2000). In particular, multiplex real-time PCR as-
say, performed after an enrichment step, has demonstrated to
be a fast and trustworthy method for ecient screening of
single or multiple pathogen occurrence in various meat prod-
ucts (Suo, He, Tu, & Shi, 2010; Wang, Jothikumar, & Griths,
2004).
Two typical products popular in the Salento area (Apulia, South-
ern Italy) are fresh-made pork sausages and entrails lamb rolls that
constitute a good substrate for the growth of both pathogens. With
the exception of two previous reports about the contamination
level of different foods of animal origin in Italy (Busani, Cigliano,
Taioli, et al., 2005; Di Pinto, Novello, Montemurro, Bonerba, & Tan-
tilli, 2010), at the present, to our knowledge, there are no pub-
lished data on whether and with which frequency L. monocytogenes
and Salmonella spp. are present in meat-derived products in South-
ern Italy. Therefore, the objective of the present study was to sup-
ply the rst evaluation of the presence of both pathogens in meat
processing plants located in Salento.
2. Materials and methods
2.1. Sampling plan
Three meat processing plants located in Salento (Southern Italy)
were selected. The selection was based on: i) capability to process
large quantity of meat, ii) dissimilar processing lines (beef, pork,
lamb) and iii) the variety of nal products. A total number of 6720
samples were collected over a 7-year-period (20082014), through
504 independent sampling times. Samples were collected from two
typical nal meat products: fresh-made pork sausages and entrails
lamb rolls. Sausages are made of pork intestine (gut) stuffed with
minced pork meat, spices, salt, sugar (dextrose or saccharose). En-
trails lamb rolls are made of pieces of suckling lamb liver, lung and
heart wrapped into its omentum and tied with gut. All samples
were transferred to the laboratory under aseptic and refrigerated
conditions in portable insulated cold-boxes. Samples were kept at
4 C and analyzed within 24 h.
2.2. Detection of L. monocytogenes and Salmonella spp. in meat
samples
Samples were enriched before bacterial genomic DNA isolation,
by separately adding 25 g of meat samples to 225 mL of buffered
peptone water (Salmonella spp. enrichment) or Half Fraser broth
(L. monocytogenes enrichment) in sterile plastic Seward lter bags
(Norfolk, UK). The samples were then homogenized in a stomacher
(Seward Stomacher 400 Lab System, Norfolk, UK) for 1 min. The
homogenate was poured into sterile containers and incubated for
1620 h at 37 C (Salmonella spp.) or 1426 h at 30 C (L. monocy-
togenes). Aliquots of culture-enriched samples (1 mL for Salmonella,
1.5 mL for Listeria) were removed and transferred to 1.5 mL ster-
ile tubes for DNA extraction. Bacterial genomic DNA was isolated
from the enriched samples using either the iQ-CheckTM Salmonella
spp. II or iQ-CheckTM L. monocytogenes II (Bio-Rad; USA) according
to suppliers instruction. Extracted DNA was suspended in 500 L
and 5 L of each sample were taken to perform real-time PCR.
Monitoring of the reaction was carried out by CFX manager IDE
software by Bio-Rad. Validation of positive samples was performed
using the RAPID Salmonella spp. and RAPID L. monocytogenes (Bio-
Rad, USA) according to suppliers instruction. Both the above meth-
ods according to the ISO 16140 standard, are an alternative method
to the reference standards ISO 11290-1 (for Listeria spp detection)
and to the ISO 6579 (for Salmonella spp detection) in all food prod-
ucts.
2.3. Statistical analysis
The chi-squared test was employed to evaluate the relative cor-
relations between quantity of positive and negative samples. Com-
parison among months, years or seasons, based on the proportion
of negative/positive samples, was performed with the Fisher exact
test (alpha 0.05). The probability statistically signicant value was
identied as p < 0.05. The statistical analysis was carried out using
PAST software (Hammer, Harper, & Ryan, 2001).
3. Results and discussion
3.1. Occurrence of L. monocytogenes
The presence of L. monocytogenes was determined in 5421 sam-
ples of lamb rolls over a seven-year-period, during which the
samples were collected from three different production plants
(Table 1). In total, the bacteria were present in 2.3% (125/5421) of
the analyzed samples. Contamination distribution, along the seven-
year-period, of the three monitored plants is reported in Table 2,
106 V. DOstuni et al. / Food Control 62 (2016) 104109

indicating that the number of positive samples of plant A de-

L+ = L. monocytogenes positive sample; S+ = Salmonella spp. positive sample; T, total sample number; values with different letters within a column respectively belonging to lamb rolls or sausages samples, differ at p < 0.05.
creased from 11.2% (5/42; year 2008) to 0.8% (5/625; year 2014).

625
220
29

23
80
90
A similar trend is highlighted for plant B, in which the amount of

T
infected samples decreased from 7.9% (11/139; year 2008) to 1.8%

10 (4.5)b
0 (0.0)ab
a
2 (0.3)

0 (0.0)
0 (0.0)
S+ (%)
(4/220; year 2014). A different trend was observed for plant C, in

1 (1.1)
which the presence of L. monocytogenes was ascertained only in
the years 20102012 and ranged from 3.3% (2/60; year 2010) to

(0.8)

(0.0)
(0.0)

(0.0)
L+ (%)

(1.8)

(1.1)
2.0% (1/50; year 2012).
2014

The same analysis was carried out on raw pork sausages sam-
5
4
0
0
1
0
500 ples; a total number of 1659 samples was analyzed for the pres-
239
44
77
169
22
ence of L. monocytogenes, revealing that this food-borne pathogen
T

contaminated 4.2% (69/1659) of them. In Table 2 the contamination

21 (8.8)b
2 (4.5)ab
a
3 (0.6)

4 (2.4)
0 (0.0)

0 (0.0)
S+ (%)

levels of the three production plants are reported for each year.
The contamination level of raw pork sausages from plants A and B
ranged respectively from 6.5% (6/92; year 2008) to 0% (0/80; year
(0.0)ab
(3.8)b
a

(3.5)
(0.0)

(0.0)
L+ (%)

(1.2)

2014) and from 9.1% (15/164; year 2012) to 1.1% (1/90; year 2014);
2013

in general the level of contamination of plant B was much higher

6
9

6
0
0

than plant A. On the contrary, in plant C, similarly to the previ-

795

50
302

100
164
25

ously reported evidence about L. monocytogenes contamination of

T

lamb rolls, the presence of the bacterium was detected only in the
17 (5.6)b
1 (2.0)ab
a

4 (2.4)
0 (0.0)

0 (0.0)

0 (0.0)

year 2010 when 4 out of 26 samples (15.4%) were found to be in-

S+ (%)

fected.
Taken together our data reveal the presence of this pathogen
15 (5.0)b

15 (9.1)b
1 (2.0)ab

0 (0.0)ab
a

in all the analyzed production plants, conrming the data of pre-

1 (1.0)a
2 (0.3)
L+ (%)
2012

vious similar surveys (Nrrung, Andersen, & Schlundt, 1999; Os-

aili et al., 2014; Peccio, Autio, Korkeala, Rosmini, & Trevisani, 2003;
1176
220
43
74
110
20

Rhoades et al., 2009). However, our results indicate that the fre-
T

quency of L. monocytogenes occurrence is higher than that detected

in different meat-derived products in Sweden (1.2%, Lambertz
17 (7.7)b
0 (0.0)ab
a
2 (0.2)

0 (0.0)

0 (0.0)
S+ (%)

2 (1.8)

et al., 2012), Belgium (1.1%, Uyttendaele et al., 2009) and Estonia

(0.1% Kramarenko et al., 2013), but lower than that reported in
other studies, such as the survey carried out in United Kingdom
(2.3)b
a

(7.7)b
Occurrence of L. monocytogenes and Salmonella spp. in 25 g of raw lamb rolls and raw sausages in years 20082014.

(8.2)
(0.0)

(0.0)
(1.3)
L+ (%)

(2010), showing that the 8.34% (88/1056) of the analyzed lamb-

2011

0
17
1
1
9
0

meat-derived products were infected by L. monocytogenes. More-

over Modzelewska-Kapitula and Maj-Sobotka (2014) have noticed
300
138
60
70
139
26

the occurrence of the pathogen in 26.1% raw pork sausages ex-

T

amined in Poland, Gamboa-Marin et al. (2012) referred the pres-

(13.3)b

(15.4)b
(8.7)b
a

(0.0)a
(0.7)a
(0.0)

ence of L. monocytogenes in 7.69%, raw pork sausages in Colombia;

S+ (%)

a very similar percentage was found in Bulgaria (Karakolev, 2009).

0
12
8
0
1
4

Other analogous investigations on pork sausages have reported a

4 (15.4)b
11 (8.0)b
2 (3.3)ab

pathogen occurrence of 42.0% in Brasil (Miyasaki et al., 2009) and

a

5 (3.6)a
1 (1.4)a
9 (3.0)
L+ (%)
2010

16.9% in Spain (Cabedo, Picart, Barrot, Teixido, & Canelles, 2008).

These studies conrm that there is variability in the occurrence
of L. monocytogenes in raw meat products and sausages, which is
189
233
42
66
110
25
T

likely connected to the preparation and storage procedures (Wesley

(4.2)
(9.0)
(0.0)

(0.0)
(9.1)
(9.1)

et al., 2008), the environmental conditions (Nesbakken, Kapperud,

S+ (%)

& Caugant, 1996) and the sanitary condition of the production

8
21

6
0

10
0

chains (Autio et al., 2000).

(5.8)
(6.7)

(3.0)
(4.5)
(0.0)

(0.0)
L+ (%)
2009

3.2. Occurrence of Salmonella spp.

16

2
5
11

0
42
139
35
92
150
27

The prevalence of Salmonella spp. was ascertained in the above-

T

mentioned 5421 samples of lamb rolls. The survey revealed that

(12.7)
(0.0)
(0.0)

(0.0)
(7.9)

(7.6)

2.5% of the analyzed samples (135/5421) was contaminated by this

S+ (%)

pathogen (Table 1). The occurrence of Salmonella spp. in the three

0
11
0

0
7
19

monitored plants during the 20082014 period is shown in Table 2.

(11.2)

Plant A is characterized by the absence of positive samples in the

(6.5)
(0.0)

(0.0)
(7.9)

(7.3)
L+ (%)
2008

years 2008, 2010 and 2012. A consistent number of contaminated

11
0

11
0
5

samples (4.2%) was detected in 2009, representing the highest con-

Plant

tamination level. In fact, in the remaining years the contamination

percentage is always lower than 1% (from 0.6 to 0.2%). A differ-
A

A
B

B
C

ent annual contamination prole is revealed by samples of plant

Lamb rolls

Sausages

B, in which, the amount of contaminated samples was quite high

Table 2

during all the analyzed years ranging from 9.0% (2009) to 4.5%
(2014). As far as plant C is concerned, the presence of Salmonella
 V. DOstuni et al. / Food Control 62 (2016) 104109
Fig. 1. Monthly distribution of the number, over a three-year period (20112013), of: (A) samples of entrails lamb rolls and (B) samples of raw pork sausages contaminated
by L. monocytogenes; (C) samples of entrails lamb rolls and (D) samples of raw pork sausages contaminated by Salmonella spp. Different letters indicate signicant differences
beyond level alpha = 0.05; the absence of letters indicate no statistical signicance.
spp. was 0% in the years 2008, 2009, 2011 and 2014 whereas
for the years 2010, 2012 and 2013 was 13.3%, 2.0% and 4.5%
respectively.
The prevalence of Salmonella spp. was evaluated also on raw
pork sausages samples during the same seven-year-period. A to-
tal number of 1659 samples were analyzed for the presence of
Salmonella spp., indicating that the 3.5% (58/1659) was contam-
inated (Table 1). As shown in Table 2, the contamination lev-
els of raw pork sausages from plant A showed the occurrence of
Salmonella spp. in the years 2008 and 2009 (7.6% and 9.1% respec-
tively), while there was a 0% contamination in the years 2010
2014. The prevalence of this pathogen in samples from plant B
showed a different annual distribution (Table 2). In fact, Salmonella
spp. was detected at high level 12.7 and 9.1% in 2008 and 2009 re-
spectively and then the pathogen occurrence decreased from 2.4%
(2012) to 0.7% (2010). Samples recorded from plant C were highly
contaminated (15.4%) only in the year 2010.
The value of 2.5% Salmonella spp. contaminated samples in-
dicates a lower Salmonella spp. occurrence in our samples when
compared to other published investigations. In fact, in a survey
conducted in Belgium, it was reported the presence of Salmonella
in 4.3% porcine minced meat samples (Delhalle et al., 2009) and
in 24.4% fresh pork sausages from Brazil (Mrmann, Dos Santos,
& Cardoso, 2009). When considering raw pork sausages, the oc-
currence of this pathogen here documented (mean value of the
seven-year-period = 3.7%) is in accordance with the 3.4% value
recently reported by Manios et al. (2015) for Salmonella preva-
lence in pork-based products in Greece, but it is lower than the
12.6% value found in the same country during 2010 (EFSA ECDC,
2012).
107
3.3. Different occurrence of L. monocytogenes and Salmonella spp.
in a three-year-period
In order to highlight differences in samples contamination
throughout the year, the distribution of positive samples (%) was
analyzed in respect to months and seasons. During the years 2011,
2012 and 2013, the monthly occurrence of L. monocytogenes or
Salmonella spp. in samples coming from plant B, the one with the
highest occurrence of both pathogens, was analyzed. The number
of samples positive for the presence of either L. monocytogenes or
Salmonella spp. per month is extremely variable (Fig. 1AD). In re-
lation to the prevalence of L. monocytogenes in lamb rolls, no posi-
tive samples were found in February, April and October, while the
pathogen was present in every month being at its higher level
in January, March, September and November (Fig. 1A). The high-
est numbers of Listeria contaminated raw pork sausage samples
were recorded in January, March, and October. The contamination
was always absent in February, June, July, August and November
(Fig. 1B). In the case of L. monocytogenes, a statistically signicant
seasonal change in the number of samples non containing the bac-
teria was observed. In fact, the highest number of non contam-
inated samples occurred in winter and summer. It is not fully as-
certained if Listeria occurrence undergoes seasonal variations, since
several surveys have indicated that a seasonal variation is present
in summer (Rivoal et al., 2010) and in winter (Guerini et al., 2007),
whereas other investigations did not detect any seasonal uctua-
tion (Esteban, Oporto, Aduriz, Juste, & Hurtado, 2009; Mohammed
et al., 2010).
Concerning Salmonella prevalence in lamb rolls, this pathogen
was detected in all months (Fig. 1C); the highest percentage was
108 V. DOstuni et al. / Food Control 62 (2016) 104109
found in January, February, July and November. The presence of
this pathogen in raw pork sausage samples was recorded at its
maximum level in January, February and April; no positive sam-
ples were identied from May to September and in December; a
slight contamination was detected in March, October and Novem-
ber (Fig. 1D). No statistically signicant seasonal changes were de-
tected with regard to the prevalence of Salmonella spp. As found
for L. monocytogenes, contrasting ndings indicate the presence
(Barkocy-Gallagher, Arthur, Rivera-Betancourt, et al., 2003) or ab-
sence (Ravel et al., 2010) of seasonal patterns of pathogen occur-
rence. However, the increasing or decreasing trend of pathogen in-
cidence in the different plants over the 7-year -period of analysis
can be explained by the intervention of managements as well as
the improvement of sanitation procedures achieved by the produc-
ers. In fact, the elevate occurrence of Salmonella spp. in the plant
C, recorded in the year 2010, on both meat rolls and sausages can
be correlated with the adoption, in that year, of new raw material
suppliers. Whereas, the reduction (beginning from 2010) of the oc-
currence of both pathogens in plant A can be associated to an en-
hancement of the sanitary measures in response to the results of
the 2009 survey.
4. Conclusions
The data reported in this study represent, to our knowledge, the
rst survey describing the prevalence of Listeria and Salmonella in
raw meat preparations in Italy. From the results obtained we en-
visage the need to improve the microbiological quality of raw ma-
terials and the adoption of more restrictive criteria to improve the
hygiene (Salmonella spp.) and the food safety (L. monocytogenes) of
the nal products (Delhalle et al., 2009; Leong, Alvarez-Ordez,
& Jordan, 2014). Furthermore our results indicate that the level of
Listeria contamination, although lower than that reported in other
countries, do not meet the food-safety requirements of Italian reg-
ulation, according to which these pathogens must be absent in
meat-derived preparations.
Although the prevalence of L. monocytogenes and Salmonella
spp., assessed in this investigation, is in most of the cases, lower
than the prevalence rates found in RTE foods across the E.U. (EFSA,
2012), the number of the samples in which both pathogens were
detected indicates that hygienic conditions in the examined meat-
processing plants are still unsatisfactory, thus urging the food pro-
cessors to be on their guard against food-borne contamination in
the meat-processing chain in order to avoid public health threats.
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