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Food Microbiology 27 (2010) 243e249

Contents lists available at ScienceDirect

Food Microbiology
journal homepage: www.elsevier.com/locate/fm

The microbiological safety of ready-to-eat specialty meats from markets


and specialty food shops: A UK wide study with a focus on Salmonella
and Listeria monocytogenes
F.J. Gormley a, *, C.L. Little a, K.A. Grant a, E. de Pinna a, J. McLauchlin b
a
Department of Gastrointestinal, Emerging and Zoonotic Infections, Health Protection Agency Centre for Infections, 61 Colindale Avenue, London NW9 5EQ, UK
b
Health Protection Agency Regional Microbiology Network, London WC1V 7PP, UK

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

Article history: From 2359 specialty meats (continental sausages, cured/fermented, dried meats) sampled from markets
Received 21 August 2009 and specialty food shops, 98.9% of samples were of satisfactory or acceptable microbiological quality.
Received in revised form However, 16 (0.7%) were unsatisfactory as a result of Escherichia coli, Staphylococcus aureus or Listeria spp.
12 October 2009
contamination (102 CFU/g), and nine (0.4%) were unacceptable due to presence of Salmonella spp. or
Accepted 13 October 2009
Available online 21 October 2009
Listeria monocytogenes (>102 CFU/g). Meats with unacceptable levels of L. monocytogenes were within
shelf life (range: 8e143 days remaining). Nine different subtypes of L. monocytogenes were detected with
sero/AFLP type 1/2c VII predominating (37%), although this subtype was not overrepresented in any
Keywords:
Continental sausage particular meat type (P > 0.05). Ninety-six percent of continental sausages and cured/fermented products
Fermented meats were stored at <8  C at premises, including seven of the nine unacceptable samples. These nine meats
Dried meats were all pre-packed prior to supply to retail premises (OR ¼ 0.1 P ¼ 0.003) indicating that contamination
Listeria monocytogenes with bacterial pathogens occurred earlier in the production chain. Most samples (72.7%, 8/11) with
Salmonella unsatisfactory levels of E. coli were sliced on request, suggesting cross-contamination at point of sale. This
study highlights the importance of ensuring that products do not become contaminated before final
packaging, that storage conditions are controlled, and that durability dates are an accurate indication of
the shelf life of the product so as to minimise the potential for L. monocytogenes to be present at levels
hazardous to health at the point of sale.
Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction water activity (aW) (as low as 0.85) of dried meats also restricts
microbial growth. The resulting characteristics of these products
Markets, delicatessens and other specialty food shops may offer allow for a long shelf life, for example 12 months for a typical dried
a wide variety of specialist foods such as ready-to-eat (RTE) meat.
specialty meats for sale direct to the consumer. These meats on Salmonella, Listeria monocytogenes and verocytotoxin-producing
retail sale in the UK are sourced worldwide and include dried, cured Escherichia coli O157 (E. coli O157) have been shown to survive
or fermented meats such as chorizo, salami, biltong and prosciutto. some fermentation, maturation and drying processes of dried and
Since these meat products do not require further treatment (such fermented meats (Lucke, 2009). Sliced meats are also a potential
as cooking) before consumption, the absence of pathogenic source of L. monocytogenes as cross-contamination during handling
microorganisms in these products is paramount. The production of or slicing on the premises can occur if proper controls are not in
specialty meats usually involves traditional techniques and their place (Swaminathan and Gerner-Smidt, 2007). Slicing machines
safety intrinsically rests with the microbiology of these processes. may act as harbourage sites for L. monocytogenes (Humphrey, 1990)
This is generally ensured by the microenvironments the meats and this organism can rapidly adhere to other food preparation
provide as a result of their intrinsic preservation. Fermented meats, surfaces, e.g. stainless steel surfaces, which will also act as a reser-
for example, have a typical pH of 4.6e5.3, which will inhibit growth voir for contamination (Beresford et al., 2001; Frye et al., 2002;
of many microorganisms (Greig et al., 2005). The low maximum Gombas et al., 2003). The ability of L. monocytogenes to grow at
refrigerated temperatures is also of concern for chilled meats with
an extended shelf life. Published studies have reported L. mono-
* Corresponding author. Tel.: þ4420 8327 7925. cytogenes prevalences of 13.3% in Italian style salamis collected
E-mail address: fraser.gormley@hpa.org.uk (F.J. Gormley). from Brazilian markets (De Fatima Borges et al., 1999), 19.0% in

0740-0020/$ e see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.fm.2009.10.009
244 F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249

unpacked dry sausages from markets in Yugoslavia (Buncic, 1991), Table 1


and 2.6% in whole or sliced (loose sold) fermented meats on retail Details of the specialty meat categories and the most common types within each
that were sampled.
sale in Ireland (Food Safety Authority of Ireland, 2004). Further-
more, investigations of dried sausage processing plants in France Meat type Specific type No. of samples
showed that L. monocytogenes could be isolated at all stages of the (% of meat type)

processing (Thevenot et al., 2005). Continental sausage Othera 839 (51.1)


(n ¼ 1642) Chorizo 375 (22.8)
Previous UK studies in the mid 1990s reported the presence of
Milano salami 258 (15.7)
Salmonella (0.1e0.2%) and L. monocytogenes at 10e100 CFU/g (3.3%) Danish Salami 93 (15.7)
in retail fermented and dried meats (Little et al., 1998; Ministry of Pepperoni 38 (2.3)
Agriculture, Fisheries and Food, 1997). Specialty meats sampled Hungarian salami 31 (1.9)
from travelling markets and specialist shops have been shown to be Bologna 8 (0.5)

contaminated with Salmonella (e.g. S. London from cured, smoked Cured or fermented Otherb 224 (39.0)
ham, Salmonella typhimurium PT 18 and S. typhimurium PT U320 meat (n ¼ 575) Prosciutto/Parma 184 (32.0)
Pastrami 78 (13.6)
from chorizo products) and were removed from sale (Food Stan-
Serrano 60 (10.4)
dards Agency (FSA), 2004a,b). Recent European outbreak investi- Bresaola 29 (5.0)
gations have identified meats such as salami to be important
Dried Meat (n ¼ 141) Biltong 93 (66.0)
vehicles for infection by Salmonella, L. monocytogenes and E. coli
Otherc 37 (26.2)
O157 (Emberland et al., 2006; Swaminathan and Gerner-Smidt, Jerky 11 (7.8)
2007; Luzzi et al., 2007). E. coli O157 has also been implicated in
Not recorded (n ¼ 1) Smoked chicken product 1 (100)
outbreaks involving Genoa salami in Canada (Williams et al., 2000)
and both commercially distributed dry cured salami and home- Total 2359
made jerky in the United States (Keene et al., 1997). Enterotoxin a
Other continental sausages primarily included salami varieties such as Napoli,
production of Staphylococcus aureus is also a public health concern German, Italian and garlic.
b
Other cured or fermented meat included pancetta, sopocka and other cured ham
owed to its ability to grow in environments of high salt concen-
varieties.
tration (Gillespie, 2007). In cured meats, such as cured hams, which c
Other dried meats included droewars. In each of the three main categories, the
have a high pH, the aw should be below 0.90 to prevent the diversity of other types was so high that the majority of samples were single types.
production of staphylococcal enterotoxin (Christian, 2000). Appli-
cation of good manufacturing practice, good hygiene practice, and
Hazard Analysis Critical Control Point (HACCP) systems are 2.2. Sample examination
important to prevent the occurrence of pathogens and microbial
toxins in RTE specialty meats. Samples were examined by 28 official control laboratories.
Prior to this study, there was no published microbiological Salmonella spp., L. monocytogenes and other Listeria spp., S. aureus
information on these meats from UK markets and specialty food and E. coli (faecal indicator organism) were enumerated or presence
shops. We therefore undertook a microbiological study of specialty sought in accordance with HPA Standard Microbiological Methods
meats to assess their microbiological safety primarily in relation to (Health Protection Agency, 2005a,b, 2008, 2009). All isolates of
prevalence of Salmonella and frequency and levels of L. mono- Salmonella and L. monocytogenes were sent to the Laboratory of
cytogenes. The study also was designed to evaluate the effect of risk Gastrointestinal Pathogens (LGP), Health Protection Agency Centre
factors (e.g. packed on or off the premises, display and storage for Infections, for further characterisation. This included serotyping
temperatures, hygiene conditions) on the microbiological safety of and phage typing for Salmonella isolates (Bale et al., 2007; Popoff
these meats at market and specialty food shops. and Le Minor, 2001) and serotyping and amplified fragment length
polymorphism (AFLP) for L. monocytogenes isolates (Doumith et al.,
2004; Guerra et al., 2002).
2. Materials and methods Microbiological results were interpreted in accordance with
microbiological criteria previously described (Gilbert et al., 2000;
2.1. Sample collection Commission Regulation (EC) No 2073/2005) (Table 2). These
criteria use the presence or level of bacterial contamination as an
A total of 2359 ready-to-eat (RTE) specialty meat samples were indicator of food safety, and classify RTE foods as being of satis-
collected from 968 markets and specialty food shops between 1st factory, acceptable, unsatisfactory or of unacceptable (potentially
April 2008 and 31st March 2009. Samples were collected and hazardous) microbiological quality.
transported in accordance with the Food Standards Agency (FSA)
Food Law Code of Practice (Food Standards Agency (FSA), 2008a) 2.3. Statistical analysis
and LACORS guidance on microbiological food sampling (Local
Authorities Co-ordinators of Regulatory Services (LACORS), 2006). Data analysis was performed using Microsoft Excel. Relative
Samples ( 100 g) were collected by sampling officers from 257 proportions were compared using the chi-squared test and Fisher's
Environmental Health Departments, involving 50 Local Authority exact test (http://home.clara.net/sisa/twoby2.htm) and a proba-
food liaison groups across the UK. bility value of less than 0.05 was defined statistically significant.
Specialty meats were defined as those which required no Comparisons of means were achieved using two-tailed student's
further cooking by the consumer (i.e. ready-to-eat) and were cat- t-tests using Microsoft Excel.
egorised as continental sausage, cured or fermented meats and
dried meats (Table 1). Information on premises and samples 3. Results
including storage temperature, packaging, slicing method, dura-
bility date, and country of origin was recorded on a standard 3.1. Microbiological quality of specialty meats
questionnaire. Information on meats sampled in Scotland was
collected using the UK Food Surveillance System (FSS UK) (Cree and Within each of the different meat categories 95.7e97.2% of
Reid, 2009). samples were of satisfactory microbiological quality (Table 3).
F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249 245

Table 2
Microbiological criteria/guidelines for ready-to-eat specialty meats placed on the market: key to classification.

Criterion Guidelines: microbiological quality (CFU/g)a Regulation (EC) No. 2073/2005

Satisfactory Acceptable Unsatisfactory Unacceptable Unsatisfactory: food safety criteria (CFU/g)


Escherichia coli <20 20e<100 100 N/Ab N/A
Staphylococcus aureus <20 20e<100 100e<104 104 N/A
Listeria spp. (Total) <20 20e<100 100 N/A N/A
Listeria monocytogenes N/A N/A N/A N/A >100c
Salmonella spp. Not detected in 25 g N/A N/A Detected in 25 gd
a
Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale. Communicable Disease Public Health 2000; 3:163e167.
b
N/A, Not applicable.
c
A L. monocytogenes count of 100 CFU/g or more exceeds food safety criteria for ready-to-eat foods placed on the market during their shelf life and is thus deemed to be
legally unsatisfactory (Regulation (EC) No. 2073/2005).
d
Salmonella spp. detected in ready-to-eat specialty meats are of unacceptable quality using published public health Guidelines and are also covered by Regulation (EC)
No. 178/2002 (General Food Law Regulation).

Samples of unsatisfactory or unacceptable quality were observed in sampling while the Napoli salami sample was open and sliced on
continental sausages (0.9%) and cured/fermented meats (1.7%). request using a meat slicing machine at the premises. This slicing
None of the 141 samples of dried meats were found to be of machine was recorded to be cleaned only at the end of trading
unsatisfactory or unacceptable quality. and this salami sample was also contaminated with L. monocytogenes
Of the 2359 specialty meat samples examined, 0.8% (18) at 1.1 103 CFU/g. All nine products were within their shelf life at the
were of unsatisfactory microbiological quality due to E. coli time of sampling as judged by their durability date and their
(102 CFU/g, 0.5%), Listeria spp. (102 CFU/g, 0.04%), or S. aureus remaining shelf-lives ranged from 8 days (ears and tongue roll)
(102e<104 CFU/g, 0.2%). A further nine samples were found to be to 203 days (chorizo). All affected batches were recalled (Food
of unacceptable microbiological quality due to high levels of Standards Agency (FSA), 2008b,c,d,e).
L. monocytogenes (>102 CFU/g, 6 samples, 0.3%) or presence of
Salmonella (3 samples, 0.1%). These meats were therefore not 3.3. Diversity of L. monocytogenes isolates
compliant with the food safety requirements of Regulation (EC) No.
178/2002 (General Food Law Regulation). The six samples of Of the L. monocytogenes isolates referred for serotyping and
specialty meats with L. monocytogenes levels at >102 CFU/g also AFLP typing, 74.1% (40/54) were from continental sausage and the
exceeded the food safety criteria for RTE foods placed on the market remaining 25.9% (14/54) were from cured/fermented meats. Over-
during their shelf life and were thus also judged to be legally all, nine different L. monocytogenes subtypes were obtained with
unsatisfactory (Regulation (EC) No. 2073/2005 (as amended)) 1/2c VII recovered from most of these (37.0%, 20/54), followed by
(European Commission, 2005). 1/2a IX (20.3%, 11/54) (Fig. 1). There was no significant association
with a specific meat type (P > 0.05). L. monocytogenes isolates
3.2. Specialty meats contaminated with Salmonella spp. originated from meats produced from 13 different countries.
and L. monocytogenes (>102 CFU/g) However, the majority of L. monocytogenes isolates were charac-
terised from meat samples which originated in Italy (25.9%, 14).
Samples contaminated with Salmonella (S. Unnamed (I 1,4,12: i: -),
S. typhimurium DT 193a and S. Derby) were two chorizo products 3.4. Shelf life of specialty meats
and one turkey salami product. The six samples contaminated with
L. monocytogenes at unacceptable levels (2.2  102e1.5  106 CFU/g) Of the 2359 specialty meats sampled, 61.7% (1455) displayed
were a cured bacon extra product, a Napoli salami, three Lithuanian a durability date (best before date or use by date). Dried meats had
ear and tongue rolls and a Hungarian sausage (Table 4). Of these nine a significantly longer remaining shelf until they reached the dura-
meat samples, eight were stored below 8  C (a requirement for RTE bility date displayed on their packaging (94 days, range: 9e335 days)
foods which may support growth of pathogenic microorganisms compared to continental sausage (68 days, range: 0e389 days)
(Food Hygiene (England) Regulations, 2006), while the chorizo (P ¼ 0.0004, 2 tailed t-test) and cured/fermented meats (65 days,
sample contaminated with S. Derby was stored at 10.1  C at the range: 0e380 days) (P ¼ 0.0006, 2 tailed t-test). Three and two
premises. Eight of the meats were pre-packed at the time of samples of continental sausage (0.2%, 1062) and cured/fermented

Table 3
Microbiological quality of specialty meats collected from markets and specialty food shops.

Total Microbiological quality

Satisfactory Acceptable Unsatisfactory Unacceptable/potentially


(% of samples) (% of samples) (% of samples) hazardous (% of samples)
All samples 2359 2272 (96.3) 62 (2.6) 16 (0.7) 9 (0.4)
Continental sausage 1642 1584 (96.5) 43 (2.6) 10 (0.6) 5 (0.3)
Cured or fermented meat 575 550 (95.7) 15 (2.6) 6 (1.0) 4 (0.7)
Dried meat 141 137 (97.2) 4 (2.8) 0 (0.0) 0 (0.0)
Not recorded 1 1 (100.0) e e e
L. monocytogenes 2359 2352 (99.7) 1 (0.04) e 6 (0.3)
Listeria spp. 2359 2357 (99.9) 1 (0.04) 1 (0.04) e
S. aureus 2359 2318 (98.3) 37 (1.6) 4 (0.2) e
Salmonella 2359 2356 (99.9) e e 3 (0.1)
E. coli 2359 2338 (99.1) 8 (0.3) 13 (0.5) e
246 F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249

Table 4
Salmonella spp. and L. monocytogenes (>102 CFU/g) isolated from specialty meats.

Specialty meat Country Salmonella sero- L. monocytogenes Storage Date Best before Use by Remaining shelf
of origin and phage types (CFU/g) temperature ( C) sampled date date life (days)
Chorizo Spain S. Unnamed (I 1,4,12:i :-)a NDb 5.0 14/05/2008 3/12/2008 203
Chorizo Spain S. Derby ND 10.1 03/06/2008 e 4/08/2008 62
Turkey meat Salami Germany S. typhimurium DT 193a ND 3.0 03/12/2008 12/01/2009 40
Bacon Extra Portugal ND 3.5  104 5.0 03/07/2008 23/11/2008 143
Napoli Salami Italy ND 1.1  103 5.0 08/07/2008 10/08/2008 33
Ears & tongue roll Lithuania ND 3.6  103 3.5 08/10/2008 16/10/2008 8
Ears & tongue roll Lithuania ND 1.5  106 3.5 08/10/2008 16/10/2008 8
Ears & tongue roll Lithuania ND 4.4  102 3.5 02/10/2008 16/10/2008 14
Hungarian sausage Hungary ND 2.2  102 5.7 06/11/2008 e 19/12/2008 43
a
Salmonella Unnamed (I 1,4,12: i: -); although the isolate was monophasic, it showed a reaction with the S. typhimurium phages and had the pattern for definitive type
(DT) 195.
b
Not detected.

meats (0.6%, 305), respectively were sampled on the date of expiry Dried meats are shelf-stable due to their inherent low water
and were all of satisfactory microbiological quality. activity (aw) and are therefore exempt from chill holding require-
The relationship between the time remaining until the dura- ments. Because of this, the 141 dried meat samples were omitted
bility date would be reached and bacterial contamination was from the following analysis as a result of their relative temperature
investigated (Table 5). For samples where E. coli, S. aureus and independent shelf life. From the remaining 2218 continental
Listeria spp. (not L. monocytogenes) were present at satisfactory or sausage and cured or fermented meats, storage temperature data
acceptable levels, the mean time remaining was not significantly was available for 2109 (95%) of the samples: 1791 (84.9%) were
longer than for samples of unsatisfactory microbiological quality stored 8  C (mean: 4.5  C, range: 0e8  C) and 318 (15.1%) were
(P > 0.05), although the satisfactory and acceptable samples were stored >8  C (mean: 11.8  C, range: 8.1e25  C). Comparisons
all tested early in their shelf life. Of note, the six samples with were made between the proportions of meat samples stored at
L. monocytogenes exceeding the food safety criteria limit were each temperature grouping (i.e. 8  C and >8  C) and their
all within their durability date (Table 3, range of 8e143 days microbiological status. Microbiological quality was not significantly
remaining). affected by the storage temperature (P > 0.05).
Of the 2359 samples, 1332 (56.5%) were sliced on request, 306
(13.0%) were sliced off the premises and 531 (22.5%) were un-sliced
3.5. Specialty meat packaging, storage and hygiene

Thirty seven percent (867) of the 2359 meats sampled were pre-
Table 5
packed, 714 (30.3%) were covered, 700 (29.7%) were open and for Remaining time until durability date reached for specialty meat samples contami-
the remaining 78 (3.3%), the display and storage details were not nated with specific bacteria.
recorded. Although there was no significant statistical association
Bacteria Microbiological No. of meat Remaining time
between packaging and the microbiological quality of the samples, (CFU/g) quality samplesa until durability
even when comparing those which were covered or open with date reached (days)
those pre-packaged (P > 0.05), it is noteworthy that samples of Mean Maximum
unacceptable quality were all pre-packed.
L. monocytogenes
ND Satisfactory 1372 69 389
<20 Satisfactory 77 65 268
10e<102 Acceptable 0 0 0
102e<103 Unacceptable 2 29 43
103e<104 Unacceptable 2 21 33
104e<105 Unacceptable 1 143 143
106e<107 Unacceptable 1 8 8

Listeria spp.
ND Satisfactory 1333 68 389
<20 Satisfactory 121 73 364
103e<104 Unsatisfactory 1 33 33

S. aureus
<20 Satisfactory 1437 69 389
20e<102 Acceptable 16 61 222
102e<103 Unsatisfactory 1 26 26
103e<104 Unsatisfactory 1 5 5

Salmonella
Detected Unacceptable 3 102 203
Not Satisfactory 1452 69 389
detected

E. coli
<20 Satisfactory 1444 69 389
20e<102 Acceptable 3 69 139
102e<103 Unsatisfactory 6 67 170
103e<104 Unsatisfactory 1 3 3
104e<105 Unsatisfactory 1 43 43
Fig. 1. Diversity of L. monocytogenes sero/AFLP subtypes detected in continental
a
sausage and cured/fermented meats. Data included are for samples where a durability date was specified.
F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249 247

Table 6 sliced. Similarly, the specialty meat samples with unsafe levels of
Microbiological quality of specialty meats in relation to location of slicing of meats. L. monocytogenes (>100 CFU/g) were also significantly associated
Microbiological Meat sliced Meat sliced Odds 95% CI Significanceb with pre-packed meats sliced off the premises. Increased handling
quality on premises off premises ratioa and/or cutting of RTE meats prior to packaging may increase the risk
n ¼ 1332 n ¼ 306 of L. monocytogenes contamination (Angelidis and Koutsoumanis,
(56.5%) (13.0%) 2006). However, improved sanitary practice in RTE meat processing
Satisfactory 1278 (96.0) 297 (97.1) 0.7 0.4, 1.5 0.23 plants has been shown to reduce the risk of L. monocytogenes
Acceptable 42 (3.2) 4 (1.3) 2.5 0.9, 6.9 0.05 contamination in the meats (Gibbons et al., 2006) and in the
Unsatisfactory 11 (0.8) 1 (0.3) 2.5 0.3, 19.7 0.31
EU, processing areas and equipment used in the manufacture of
Unacceptable/ 1 (0.08) 4 (1.3) 0.1 0.0, 0.5 0.005
potentially
RTE foods must be monitored for L. monocytogenes (European
hazardous Commission, 2005). These findings indicate that improved food
a safety and reduction of Salmonella and L. monocytogenes at the farm,
Odds ratio (OR) defined as the ratio of the odds of a sample being of a particular
microbiological quality at above or below a storage temperature of 8  C. slaughterhouse or meat processing plant is required, through Good
b
Statistical significance at P < 0.05. Agricultural Practice, Good Manufacturing Practice, Good Hygiene
Practice and overall coherence with all stages of HACCP.
Additional sampling of the two chorizo products contaminated
(e.g. strips). This information was not available for 190 samples with Salmonella spp. revealed further batches to be contaminated.
(8.0%). Microbiological quality was not significantly different in The chorizo product contaminated with S. Unnamed (I 1,4,12: i:-)
meats sliced on the premises compared to those sliced off the showed further contamination with the same serotype in
premises for all quality categories (P > 0.05) with the exception of a different batch while samples tested from the batch contami-
meats of unacceptable quality which were more likely to be sliced nated with S. Derby uncovered the presence of a different serotype,
off the premises (OR 0.1, P ¼ 0.003) (Table 6). However, most Salmonella Unnamed (I 1,4,5,12:i:-). Similarly, further product
samples (72.7%, 8/11) with unsatisfactory levels of E. coli, were not sampling of the ears and tongue roll batch contaminated with high
pre-packed and were sliced on request, suggesting cross-contam- levels of L. monocytogenes (Food Standards Agency (FSA), 2008c) at
ination at point of sale. the UK importer level found further unsafe levels (>102 CFU/g,
Hand washing facilities were available and accessible for use in ranging up to 2.8  106 CFU/g) in nearly all samples tested (94.4%,
736 (76.0%) of the 968 retail premises, absent in 87 (9.0%), and for 17/18). These findings highlight the value of targeted microbio-
the remaining 145 (15.0%) this information was not recorded. A logical food studies in identifying products which are potentially
greater proportion of market premises did not have these facilities hazardous to public health and ensure that such contaminated
(21.1%, 22/104) compared to specialty food shops (7.4%, 63/856) products are removed from the market (Food Standards Agency
(P < 0.0001). Meat samples from market premises with no hand (FSA), 2008b,c,d,e).
washing facilities available were more likely to contain unsatis- The time remaining until the durability date was reached for
factory levels of E. coli (0.4%, 1/266) than those that had these meats contaminated with unsafe levels of L. monocytogenes ranged
facilities (0%, 0/266). In contrast, meat samples collected from from 8 to 143 days. While these specialty meats were all stored
specialty food shops that had available hand washing facilities were below 8  C, L. monocytogenes levels were already at concentrations
more likely to contain unsatisfactory levels of E. coli (0.9%, 20/2052) that pose a public health risk to the consumer, particularly if
than those without these facilities (0.1%, 2/2052). consumed by high risk groups such as pregnant women, the elderly
or immunocompromised individuals. However, L. monocytogenes
levels below 102 CFU/g may be equally detrimental if there is a long
4. Discussion enough remaining shelf life and the food is able to sustain the
growth of the pathogen. This problem could be exacerbated by the
This study highlighted that although 99% of 2359 RTE specialty inconsistency in which consumers may refrigerate meat products,
meats sold through specialist retailers in the UK were of satisfac- with storage temperatures often being too high to adequately
tory or acceptable microbiological quality, 1% were either of control L. monocytogenes growth (Kennedy et al., 2005). Further-
unsatisfactory or unacceptable quality. The findings reported here more, samples showing satisfactory or acceptable levels of other
are not significantly different (P > 0.05) from those found in Listeria spp., E. coli and S. aureus were all sampled early in shelf life
a survey of retail fermented meats sampled in the Republic of indicating that given a longer storage period, levels may have
Ireland in 2004 (Food Safety Authority of Ireland, 2004), where 98% elevated.
of meats were of satisfactory or acceptable microbiological quality, The L. monocytogenes serogroups responsible for most human
and 2% were of unsatisfactory quality. infection in the UK are 4b and 1/2a, with the subtype 4b AFLP I
RTE foods contaminated with Salmonella spp. are unsafe. They being most common in England and Wales (Gillespie and McLau-
are considered to be injurious to health and/or unfit for human chlin, 2007; McLauchlin, 1997). The predominant serogroup of
consumption and contravene food safety requirements. The L. monocytogenes recovered in this study from specialty meats was
Salmonella detected in 0.1% of specialty meats included S. Derby, serotype 1/2c, with AFLP subtype VII being the most common;
S. typhimurium DT 193a and S. Unnamed (I 1, 4, 12:i:-). S. Derby however, the subtype 1/2c VII was not overrepresented in any
(isolated from chorizo produced in Spain) has long been associated particular specialty meat. This is the fourth most common type
with pork and is one of the most common Salmonella serotypes in observed in food isolates in the UK (after types 1/2a IX, 4b I and
swine (Valdezate et al., 2005), including those from Spanish swine 1/2a VII) accounting for 10% of isolates typed from 2004eMarch
farms (14% from 100 positive herds) (Garcia-Feliz et al., 2007). The 2009, and is primarily associated with meats including ham, pork
Salmonella contamination of pre-packed chorizo in this study shows and beef (HPA, unpublished data).
that contamination occurred prior to packaging either on the swine The use of E. coli as a faecal indicator organism is based on the
farms, at slaughter or during meat processing. Contamination of concept that its detection in food samples indirectly provides
a pre-packed sliced turkey salami sample with S. typhimurium DT evidence that the sample has been contaminated with faecal
193a also indicates that contamination occurred at some earlier material and that there is an increased risk that pathogenic
stage in production or indeed at the previous premises where it was organisms may be present. Unsatisfactory quality was identified in
248 F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249

1.0% of specialty meat samples as a result of this organism being Doumith, M., Buchrieser, C., Glaser, P., Jacquet, C., Martin, P., 2004. Differentiation of
the major Listeria monocytogenes serovars by multiplex PCR. J. Clin. Microbiol.
present at levels over 102 CFU/g. Over 70% of these meats were open
42, 3819e3822.
(not pre-packed) and were sliced on request suggesting that cross- Emberland, K.E., Nygard, K., Heier, B.T., Aavitsland, P., Lassen, J., Stavnes, T.L.,
contamination had occurred at the retail premises, that the length Gondrosen, B., 2006. Outbreak of Salmonella Kedougou in Norway associated
of time and temperature control in storage or display facilities was with salami, AprileJune 2006. Euro. Surveill. 11, E060706.
Food Safety Authority of Ireland (FSAI), 2004. Microbiological safety and quality of
inadequate to prevent bacterial growth, or that a combination of fermented meat, 2004.
these factors was involved. Hand washing facilities were not Food Standards Agency (FSA), 2004a. Food Alert: Salmonella Contamination of
accessible or not used in 21.1% of market premises compared to 7.4% Picante Chorizo Extra. Food Standards Agency. Available from: http://www.
food.gov.uk/enforcement/alerts/2004/nov/pcsalmonella (accessed 24.06.09).
for specialty food shops visited to sample specialty meats. However, Food Standards Agency (FSA), 2004b. Food Alert: Salmonella Contamination of
meat samples collected from specialty food shops that had avail- Sabari Embutidos Chorizo. Food Standards Agency. Available from: http://www.
able hand washing facilities were more likely to contain unsatis- food.gov.uk/enforcement/alerts/2004/feb/sabarichorizo (accessed 24.06.09).
Food Standards Agency (FSA), 2008a. Food Law Code of Practice (England). FSA,
factory levels of E. coli suggesting that either personal hygiene is not London. Available from: http://www.food.gov.uk/news/newsarchive/2006/mar/
being maintained, or there is potentially a breakdown in the food copengland (accessed 24.06.09).
safety management system. Food Standards Agency (FSA), 2008b. Food Alert: Listeria monocytogenes Contamina-
tion of Ears and Tongue Roll. Food Standards Agency. Available from: http://www.
The maintenance of a food safety management system based on food.gov.uk/enforcement/alerts/2008/nov/samsonoupdate (accessed 24.06.09).
HACCP principles (as required by Regulation (EC) No 852/2004) in Food Standards Agency (FSA), 2008c. Food Alert: Lituanica UK Ltd Recalls All Date
food production and retail is essential. The presence of pathogens Codes of ‘Samsono’ Brand Ears and Tongue Roll Due to Contamination With
Listeria monocytogenes. Food Standards Agency. Available from: http://www.
in pre-packed RTE specialty meats suggested that contamination
food.gov.uk/enforcement/alerts/2008/oct/lituanicauk (accessed 24.06.09).
occurred either during processing or as a result of post processing Food Standards Agency (FSA), 2008d. Food Alert: Salmonella in Chorizo Products.
cross-contamination. Efforts must be made to ensure that specialty Food Standards Agency. Available from: http://www.food.gov.uk/enforcement/
alerts/2008/jun/chorizo (accessed 24.06.09).
meats do not become contaminated before final packaging. Dura-
Food Standards Agency (FSA), 2008e. Food Alert: Aytac Halal Foods Ltd Recalls
bility dates must accurately reflect the shelf life of the product so a Batch of Its Own-brand Pre-packed Sliced Turkey Salami Due to Presence of
that contamination with L. monocytogenes does not result in the Salmonella. Food Standards Agency. Available from: http://www.food.gov.uk/
growth of this pathogen to unsafe levels (>102 CFU/g). The enforcement/alerts/2008/dec/slicedturkeysalami (accessed 24.06.09).
Frye, D.M., Zweig, R., Sturgeon, J., Tormey, M., LeCavalier, M., Lee, I., Lawani, L.,
performance of the proposed distribution chain, including refrig- Mascola, L., 2002. An outbreak of febrile gastroenteritis associated with deli-
eration storage temperatures, should also be taken into account catessen meat contaminated with Listeria monocytogenes. Clin. Infect. Dis. 35,
when calculating the shelf life of the product. 943e949.
Garcia-Feliz, C., Collazos, J.A., Carvajal, A., Vidal, A.B., Aladuena, A., Ramiro, R., de la, F.M.,
Echeita, M.A., Rubio, P., 2007. Salmonella enterica infections in Spanish swine
fattening units. Zoonoses Public Health 54, 294e300.
Acknowledgments Gibbons, I.S., Adesiyun, A., Seepersadsingh, N., Rahaman, S., 2006. Investigation for
possible source(s) of contamination of ready-to-eat meat products with Listeria
spp. and other pathogens in a meat processing plant in Trinidad. Food Micro-
The authors would like to thank all the staff in the Environ- biol. 23, 359e366.
mental Health Departments throughout England, Wales, Scotland Gilbert, R.J., de Louvois, J., Donovan, T., Little, C., Nye, K., Ribeiro, C.D., Richards, J.,
Roberts, D., Bolton, F.J., 2000. Guidelines for the microbiological quality of some
and Northern Ireland who collected samples for this study; and all
ready-to-eat foods sampled at the point of sale. PHLS advisory committee for food
the staff in HPA, HPA collaborating laboratories, and other Official and dairy products. Commun. Dis. Public Health 3, 163e167.
Control Laboratories who performed the microbiological exami- Gillespie, I.A., 2007. Microbial agents of food poisoning and foodborne infection. In:
nations. Thanks are extended to LGP, HPA Centre for Infections for McLauchlin, Jim, Little, Christine (Eds.), Hobbs' Food Poisoning and Food
Hygiene, seventh ed. Hodder Arnold, pp. 59e93.
typing Salmonella and Listeria monocytogenes isolates, to Gemma Gillespie, I.A., McLauchlin, J., 2007. Advisory Committee on the Microbiological
Cantelo at LACORS for co-ordinating the participation of Environ- Safety of Food, Paper ACM/879.
mental Health Officers and advice from the LACORS Food Exami- Gombas, D.E., Chen, Y., Clavero, R.S., Scott, V.N., 2003. Survey of Listeria mono-
cytogenes in ready-to-eat foods5. J. Food Prot. 66, 559e569.
nation and Food Hygiene Focus Groups, to the HPA Regional Food, Greig, J., Nesbakken, T., Stephan, R., Kasuga, F., 2005. Meat and meat products 258.
Water and Environmental Co-coordinators Forum for advice on the In: ICMSF (Ed.), Microorganisms in Foods 6. Kluwer Academic/Plenum
sampling protocols, to Lynn Cree (Health Protection Scotland) for Publishers, New York, pp. 1e106.
Guerra, M.M., Bernardo, F., McLauchlin, J., 2002. Amplified fragment length poly-
providing data from Scotland; and finally to Nalini Rawal for morphism (AFLP) analysis of Listeria monocytogenes. Syst. Appl. Microbiol. 25,
co-ordinating data collation and validation. 456e461.
Health Protection Agency (HPA), 2005a. Enumeration of Staphylococcus aureus.
National Standard Method: F12 Issue 1.4. Available from: http://www.hpa-
standardmethods.org.uk/documents/food/pdf/f12.pdf (accessed 12.06.09).
References Health Protection Agency (HPA), 2005b. Enumeration of Escherichia coli. National
Standard Method: F20 Issue 1.4. Available from: http://www.hpa-standard
Angelidis, A.S., Koutsoumanis, K., 2006. Prevalence and concentration of Listeria methods.org.uk/documents/food/pdf/F20.pdf (accessed 12.06.09).
monocytogenes in sliced ready-to-eat meat products in the Hellenic retail Health Protection Agency (HPA), 2008. Detection of Salmonella species. Natl. Stand.
market. J. Food Prot. 69, 938e942. Method F 13 Issue 3.1. Available from: http://www.hpa-standardmethods.org.
Bale, J., de Pinna, E., Threlfall, E.J., Ward, L., 2007. Kauffmann-white Scheme e 2007: uk/documents/food/pdf/F13.pdf (accessed 12.06.09).
Salmonella Identification e Serotypes and Antigenic Formulae. Health Protection Health Protection Agency (HPA), 2009. Detection and enumeration of, Listeria
Agency. monocytogenes and other Listeria species. Stand. Method F19 Issue 3.1. Available
Beresford, M.R., Andrew, P.W., Shama, G., 2001. Listeria monocytogenes adheres to from: http://www.hpa-standardmethods.org.uk/documents/food/pdf/f19.pdf
many materials found in food-processing environments. J. Appl. Microbiol. 90, (accessed 12.06.09).
1000e1005. Humphrey, T.J., 1990. Listeria contamination of retail meat slicers. PHLS Microbiol.
Buncic, S., 1991. The incidence of Listeria monocytogenes in slaughtered animals, in Dig. 7.
meat, and in meat products in Yugoslavia. Int. J. Food Microbiol. 12, 173e180. Keene, W., Sazie, E., Kok, J., Rice, D., Hancock, D., Balan, V., Zhao, T., Doyle, M., 1997.
Christian, J., 2000. Drying and reduction of water activity. In: Lund, B., Baird- An outbreak of Escherichia coli O157:H7 infections traced to jerky made from
Parker, T., Gould, G. (Eds.), The Microbiological Safety and Quality of Food. deer meat. J. Am. Med. Assoc. 277, 1229e1231.
Springer, pp. 146e174. Kennedy, J., Jackson, V., Blair, I.S., McDowell, D.A., Cowan, C., Bolton, D.J., 2005. Food
Commission Regulation (EC) No 2073/2005 of,15 November 2005. On microbiological safety knowledge of consumers and the microbiological and temperature status
criteria for foodstuffs. Official Journal of the European Union, 22-12-2005. of their refrigerators 2. J. Food Prot. 68, 1421e1430.
Cree, L.M., Reid, M.H., 2009. Development of the UK food samples surveillance Little, C.L., Monsey, H.A., Nichols, G.L., de Louvois, J., 1998. The microbiological
system. Public Health 123, 89e94. quality of ready-to-eat dried and fermented meat and meat products. Int. J.
De Fatima Borges, M., de Siqueira, R., Bittencourt, A.M., Vanetti, M.C.D., Environ. Health Res. 8, 277e284.
Gomide, L.A.M., 1999. Occurrence of Listeria monocytogenes in salami. Rev. Local Authorities Co-ordinators of Regulatory Services (LACORS), 2006. LACORS
Microbiol. 30, 362e364. Guidance Food Sampling for Microbiological Examination.
F.J. Gormley et al. / Food Microbiology 27 (2010) 243e249 249

Lucke, F.-K., 2009. Fermented meats. In: . Lund, B., Baird-Parker, T., .Gould, G. Swaminathan, B., Gerner-Smidt, P., 2007. The epidemiology of human listeriosis.
(Eds.), The Microbiological Safety and Quality of Food. Springer, pp. Microbes. Infect. 9, 1236e1243.
420e444. The Food Hygiene (England) Regulations, 2006. SI 2006/14. The Stationary
Luzzi, I., Galetta, P., Massari, M., Rizzo, C., Dionisi, A.M., Filetici, E., Cawthorne, A., Office: London. Available at: http://www.opsi.gov.uk/si/si2006/20060014.htm
Tozzi, A., Argentieri, M., Bilei, S., Busani, L., Gnesivo, C., Pendenza, A., Piccoli, A., (accessed 12.10.09).
Napoli, P., Loffredo, L., Trinito, M.O., Santarelli, E., Ciofi degli Atti, M.L., 2007. An Thevenot, D., Delignette-Muller, M.L., Christieans, S., Vernozy-Rozand, C., 2005.
easter outbreak of Salmonella typhimurium DT 104A associated with traditional Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and
pork salami in Italy. Euro. Surveill. 12, E11eE12. their products. Int. J. Food Microbiol. 102, 85e94.
McLauchlin, J., 1997. The pathogenicity of Listeria monocytogenes: a public health Valdezate, S., Vidal, A., Herrera-Leon, S., Pozo, J., Rubio, P., Usera, M.A., Carvajal, A.,
perspective. Rev. Med. Microbiol. 8, 1e14. Echeita, M.A., 2005. Salmonella Derby clonal spread from pork. Emerg. Infect.
Ministry of Agriculture, Fisheries and Food (MAFF), 1997. A National Study on Dis. 11, 694e698.
Ready-to-eat Meats and Meat Products. Williams, R.C., Isaacs, S., Decou, M.L., Richardson, E.A., Buffett, M.C., Slinger, R.W.,
Popoff, M., Le Minor, L., 2001. Antigenic Formulas of the Salmonella Serovars, eighth Brodsky, M.H., Ciebin, B.W., Ellis, A., Hockin, J., 2000. Illness outbreak associated
ed. WHO Collaborating Centre for Reference and Research on Salmonella, with Escherichia coli O157:H7 in Genoa salami. E. coli O157:H7 working group.
Institut Pasteur, Paris. CMAJ 162, 1409e1413.