LACORS/HPA Co-ordinated Food Liaison Group Studies:
Microbiological Examination of Vacuum Packed and Modified Atmosphere
Packaged Cooked Ready-To-Eat Meats at End of Shelf-life from Retail
Premises
SK Sagoo1*, CL Little1, G Allen2, K Williamson2, K Grant3 and the Food, Water and
Environmental Surveillance Network†.
1, Environmental and Enteric Diseases Department, CDSC, Health Protection Agency Centre for Infections,
61 Colindale Avenue, London NW9 5EQ
2, Food and Environmental Microbiology Services North West, Preston. Microbiology Services, Royal
Preston Hospital, Sharoe Green Lane North, Preston PR2 9HG
3, Food Safety Microbiology Laboratory, SRMD, Health Protection Agency Centre for Infections, 61
Colindale Avenue, London NW9 5EQ
*, Author for correspondence
†, FWES Network comprises Laboratories listed in Annex I
On behalf of the Local Authorities Co-ordinated Body of Regulatory Services and
the Health Protection Agency
Summary
During September to mid November 2003, a study of retail modified atmosphere
packed (MAP) and vacuum packed (VP) cooked ready-to-eat meats at the end of
shelf life was undertaken to determine their microbiological quality. Using the
PHLS guidelines with interpretation of the microbial flora of aerobic colony
counts, examination of 2981 samples revealed that two-thirds (66%) were of
satisfactory or acceptable quality, 33% were of unsatisfactory quality mainly due
to high Aerobic Colony Counts and Enterobacteriaceae, and 1% were of
unacceptable
microbiology
quality
due
to
the
presence
of
Listeria
monocytogenes at 100 cfu/g or more (27 samples; range of 10 2 –106 cfu/g), and
Campylobacter jejuni (one sample) indicating a risk to health. A further 5.5% of
samples at end of shelf life had L. monocytogenes present (<20 cfu/g; 4.8%) or
at levels below 100 cfu/g (0.7%). Twelve different L. monocytogenes typing
characters (serotyping/AFLP/phagetyping) were obtained from isolates recovered
from samples of unacceptable quality, with the 1/2/IX/NT type recovered from
almost half (48%) of these. Salmonella spp. was not detected in any samples
examined. Results from this study suggest that the shelf life assigned to some
VP/MAP meats may not be appropriate. The rise in listeriosis in England and
Wales during 2002-2003 and implications arising from this study is discussed.
1
Introduction
Pre-packed sliced meats make up a third of the UK sliced meat market and ham
is the most popular sliced meat accounting for over half of UK sales 1. Most prepacked sliced meats are purchased from multiple retailers1 and market growth of
retail sliced meats in the UK between 1999 and 2003 increased by 111%, and
was worth £570 million in 20032. Modified Atmosphere Packed (MAP) and
vacuum packed (VP) sliced meats have become increasingly popular due to
consumer demands for fresher, longer shelf-life convenience foods that are safe,
nutritional and organoleptically pleasing. Vacuum packaging is essentially the
evacuation of air from a package that is then hermetically sealed. With MAP, air
is again removed and replaced by a strictly controlled gaseous mixture
comprising of carbon dioxide, oxygen and/or nitrogen. A UK industry code of
practice exists that provides information on available VP and MAP methods 3, 4 .
Both packaging techniques have the potential to increase the shelf life of many
chilled foods without adversely affecting the quality.
Whilst changing the
atmosphere may retard the growth of spoilage organisms, it may allow growth of
psychrotrophic pathogenic bacteria such as Clostridium botulinum and Listeria
monocytogenes. The UK industry code of practice advises that the shelf life of
VP/MAP cooked, uncured meats should not exceed 10 days at 3-8ºC unless its
microbiological safety under extended storage conditions can be demonstrated.
Cured meats such as ham typically have specific controlling factors and therefore
can have a longer shelf life of more than 10 days 3. Temperature control
regulations require that chilled VP/MAP foods, including cooked meats, must be
stored and displayed at or below 8ºC in retail premises5.
However,
manufacturers often use a storage temperature of less than 3ºC during predistribution and generally recommend 5ºC or less for domestic storage by the
consumer6. Refrigeration storage temperatures may therefore vary from predistribution, retail and the consumer home.
2
Contaminated food is considered to be the main source of L. monocytogenes
infections in humans, including ready-to-eat meats, which have been responsible
for causing major outbreaks of L. monocytogenes in France, Norway, Australia,
and the US
7-11.
Although listeriosis is a rare disease in the UK in contrast to
infection caused by other major bacterial foodborne diseases 12 it remains a
cause for concern due to the increased risk posed to vulnerable groups and
severity of disease12,13. L. monocytogenes grows at refrigeration temperatures
and has the ability to colonise and become endemic in the food processing
environment, including process equipment, with potential contamination of endproducts. With a growing demand for ready-to-eat products with extended shelf
life this poses a serious challenge to the food industry and is of great concern.
The draft EC Regulation on microbiological criteria for foodstuffs proposes that L.
monocytogenes should be below 102 cfu/g during the shelf life of ready-to-eat
foods14.
VP/MAP cooked meats were the focus of regional studies involving Local
Authority food liaison groups in the North West and East of England during
200215-17. Almost 2% of VP/MAP meats at end of shelf life were found to be of
unacceptable microbiological quality due to levels of L. monocytogenes in excess
of 100 cfu/g, A valid shelf life and appropriate temperature control provided is
therefore paramount for the microbiological safety of these products.
As a
consequence of the regional investigations a national study was undertaken in
2003 as part of the Local Authority Co-ordinators of Regulatory Services
(LACORS), and the Health Protection Agency (HPA) Coordinated Food Liaison
Group Microbiological Sampling Programme. The aims of the study were to
determine the microbiological quality of VP/MAP cooked ready-to-eat meats on
sale in the UK at the end of their shelf life. This included identifying the
predominant microflora of high Aerobic Colony Counts (ACCs) from samples to
provide a more helpful interpretation of the microbiological quality of cooked meats.
3
Materials and Methods
Sample Collection
VP/MAP cooked ready-to-eat meats collected from retail premises were
examined at end of shelf life by 37 laboratories (HPA, HPA Collaborating and
non-HPA) in the UK between the 1st September and 10 th November 2003
according to a standardised protocol. VP/MAP meats included in the study were
those that were sliced, wafer thin or portions of meat. Fermented or dried meat
products and pate were specifically excluded from the study. Samples (~100g)
were collected and transported to laboratories by staff from 348 local
Environmental Health Departments, involving 52 Local Authority Food Liaison
Groups, in accordance with the Food Safety Act 1990, Code of Practice No 7 18
(revised in 2004) and guidance on microbiological food sampling19.
Information on the VP/MAP meat samples and retail premises was obtained by
observation and enquiry and recorded on a standard proforma. This included
information on the premises and practices with regard to type, and temperature,
of the display area, packaging practices, presence of a hazard analysis system
and the level of food hygiene training received by the manager. Food hygiene
inspections of premises are carried out by environmental health officers to
assess hygiene and compliance with public health protection aspects of food law
20.
Some food premises and businesses pose a greater risk to the consumer
than others, which is reflected by the frequency of inspection. Premises rated
Inspection Rating Category A posed the greatest risk and were visited at least
once every six months while premises rated Inspection Rating Category F posed
the least risk and were visited at least once every five years. Environmental
health officers also consider the number of customers likely to be put at risk if
there is a failure in food hygiene and safety procedures in a particular premise,
and award a consumer at risk score accordingly. Scores range from 0 (very few
customers at risk) to 15 (a substantial number of customers at risk). Confidence
in management and food safety management systems are also assessed and
4
scored accordingly. Confidence in management scores range from 0 (highly
confident) to 30 (no confidence).
Sample Examination
On receipt at the laboratory samples were stored in a monitored laboratory
refrigerator at 6±2ºC until the end of shelf life (i.e. use by date), whereupon
samples were examined. Aerobic Colony Counts (ACC), Enterobacteriaceae,
Escherichia coli, Clostridium perfringens, Staphylococcus aureus, total Listeria
spp. including L. monocytogenes were enumerated or presence sought in
accordance with HPA Standard Microbiological Methods21-27. Presence of
Campylobacter spp. were sought by enrichment in Bolton Selective Enrichment
Broth with incubation at 37°C for 4 hours, followed by further incubation at 41.5°C
and subculture to Campylobacter selective agar (CCDA) after 442 h. Inoculated
plates were incubated at 41.5°C for 48 h, and colonies identified as described in
HPA Standard Microbiological Method F2128. Presence of Salmonella spp. were
sought in accordance with
BS EN 1S0 6579:200229. Isolates of
L.
monocytogenes at levels at 102 cfu/g or more were sent to the Food Safety
Microbiology Laboratory (FSML), HPA Centre for Infections for further
characterisation by sero- and phage typing, and amplified fragment length
polymorphism (AFLP). Isolates of Campylobacter spp. were sent to the
Laboratory of Enteric Pathogens (LEP), HPA Centre for Infections for typing.
To improve the interpretation of the microbiological quality of cooked meats the
predominant microflora of high ACCs obtained from samples were identified. For
ham and tongue samples with ACCs at 107 cfu/g or more and for other meats
(e.g. beef, pork, poultry, etc.) with ACCs at 106 cfu/g or more the predominant
microflora was determined by carrying out the Gram stain, catalase and oxidase
tests. The percentage component of high ACC results were reported in to three
groups as follows:

Lactic acid bacteria (Gram positive and catalase negative; i.e. lactobacilli
and streptococci)
5

Gram negative and oxidase positive bacteria (e.g. Pseudomonas spp.,
Aeromonas)

Gram negative and oxidase negative bacteria (e.g. Enterobacteriaceae,
Acinetobacter)
Microbiological results were compared to the PHLS Guidelines for the
microbiological quality of some ready-to-eat foods sampled at the point of sale
(Table 1). The PHLS guidelines do not include interpretation of the component
microflora of the Aerobic Colony Counts. For the purpose of this study if an
unsatisfactory Aerobic Colony Count consisted predominantly of lactic acid
bacteria it was classified as unsatisfactory only if levels exceeded 10 8 cfu/g. If
Gram-negative bacteria predominated the Aerobic Colony Count was deemed
unsatisfactory if the level exceeded 107 cfu/g.
Table 1. PHLS guidelines for the microbiological quality of some ready toeat foods sampled at the point of sale30: Key to classification of sliced meat
Criterion
Aerobic Colony Count
(All meats other than
ham and tongue)
Aerobic Colony Count
(Ham, tongue)
Enterobacteriaceae
Escherichia coli
Staphylococcus aureus
Clostridium perfringens
Listeria spp. (total)
Listeria monocytogenes
Campylobacter spp.
Salmonella spp.
*N/A, Not Applicable
Microbiological quality (cfu per gram unless stated)
Satisfactory
Acceptable
Unsatisfactory
Unacceptable/
potentially
hazardous
<105
105-<106
>106
N/A*
<106
<102
<20
<20
<20
<20
<20
Not detected in 25g
Not detected in 25g
106-<107
102 - <104
20 - <102
20 - <102
20 - <102
20 - <102
20 - <102
>107
104
102
102 - <104
102 - <104
102
N/A
N/A
N/A
N/A
104
104
N/A
102
Detected in 25g
Detected in 25g
6
Statistical Analysis
Descriptive and statistical analysis of the data was undertaken using Microsoft
excel version 9 and Epi Info version 6.04d. Relative proportions were compared
using chi-squared (χ2) and fishers exact test.
Results
Bacteria isolated from VP/MAP ready-to-eat meats
Of the 2981 samples examined, 1362 were ham and tongue and of these, 56%
(757) had ACCs of 107 cfu/g or more. Of the 1619 other meat samples, 65%
(1047) had ACC levels in excess of 106 cfu/g. Enterobacteriaceae were present
at 104 cfu/g or more in 15% (458) of samples (Table 2). E. coli was present at 102
cfu/g or more in 0.3% (10) of all meat samples. Total Listeria spp. (including L.
monocytogenes) was detected in 6.4% (191) of samples, and also present in 1%
(29) of samples in the range of 20 to less than 100 cfu/g, and in a further 1.4%
(43) of samples at 100 cfu/g or more. L. monocytogenes was detected in 4.8%
(143) samples, and also present in 0.7% (20) of samples in the range of 20 to
less than 100 cfu/g and in a further 1% (27) of samples at 100 cfu/g or more
(ranging from 1.0x102 to 2.4x106 cfu/g). The Listeria isolates recovered from
samples with levels in excess of 102 cfu/g were L. innocua (5), L. seeligeri (2), L
welshimeri (2) and L. monocytogenes (27; serotype 1/2 (22), 4b (2), non-typable
(1) (Tables 3 and 4)). Campylobacter spp. (C. jejuni HS44 PT70) was detected
in 0.03% (1) sample (turkey, MAP). Salmonella spp. was not detected from any
of the samples examined.
7
Table 2. Microbiological results of 2981 VP/MAP ready-to-eat meats at end
of shelf life
ND*
in 25g
Aerobic Colony Counts
Enterobacteriaceae
Escherichia coli
Staphylococcus aureus
Clostridium perfringens
Listeria spp. (total)
-L. monocytogenes
Campylobacter spp.
Salmonella spp.
2717
2953
2971
D§
in
25g
<10/
<20†
110
1994a
2952b
2951b
2948a
191 (&<20b)
143 (&<20b)
1
20<102
102 <103
103 <104
104 <105
105 <106
106 <107
107
NE¶
46
138
6
9
4
29
20
121
184
155
207
2
190
188
1
330
183
437
45
1
1579
29
25
13
12
10
4
3
13
13
19
21
29
11
5
27
10
2
1
*ND; Not detected; §D, Detected; ¶NE, Not examined (full set of microbiological parameters not performed on sample due to
insufficient sample collected)
†, cfu/g
a, lower limit of detection 10 cfu/g; b, lower limit of detection 20 cfu/g
Table 3. Listeria spp. present in VP/MAP cooked meats at 102 cfu/g or more
Listeria spp.
No. Samples*
L. monocytogenes
27
L. innocua
L. seeligeri
L. welshimeri
Total
5
2
2
36
Meat type (No. Samples)
Ham (10), turkey (6), chicken (5), beef (4),
corned beef (2),
Ham (2), beef (2), chicken (1)
Ham (2)
Ham (1), Pork (1)
*, Six isolates were not typed
L. monocytogenes isolate types present in VP/MAP cooked meats at 102
cfu/g or more
Twelve different L. monocytogenes typing characters (serotyping/AFLP/phage
typing) were obtained from samples with levels of 10 2 cfu/g or more, i.e. of
unacceptable microbiological quality (Table 4), with the 1/2/IX/NT type recovered
from almost half (48%; 12/25) of these. Approximately half (48%; 12) of the
isolates were obtained from meats produced by Manufacturer A, with the typing
character 1/2/IX/NT predominating in these samples (8; 67%). These adverse
results were reported to the appropriate food authority, manufacturer and the
Food Standards Agency and full investigations were undertaken.
8
Table 4. Typing characters of L. monocytogenes isolated from VP/MAP
cooked meat of unacceptable microbiological quality at end of shelf life
Typing character
No. Samples*
Meat type (No. Samples)¶
12
Beef (1†), Chicken (3‡), Ham (5),
Turkey (3)
Beef
Chicken
Turkey
Corned beef†
Beef
Beef (1), Ham (2)
Turkey
Corned beef
Ham
Chicken
Ham
(Serotype/AFLP§/phagetype)
1/2/ IX/NT
1/2/II/Y
1/2/VII/NT
1/2/XI/NT
4b/V/A
4b/II/NT
1/2/II/Z
1/2/IX/Y
1/2/IX/VV
1/2/II/NT
NT/XI/NT
1/2/NT/WW
Total
1
1
1
1
1
3
1
1
1
1
1
25
*, Two isolates were not typed
§, Amplified fragment length polymorphism
¶, MAP meats unless stated (†, Vacuum packed; ‡, 1 sample of chicken was vacuum packed)
Microbiological quality of VP/MAP cooked ready-to-eat meats
Based on the PHLS microbiological guidelines for some ready-to-eat foods
sampled at the point of sale (Table 1) and without interpretation of the component
microflora associated with high ACCs, a quarter (24%; 715/2981) of the VP/MAP
meat samples were satisfactory, 13% were acceptable, and 62% were of
unsatisfactory microbiological quality (Fig. 1). However, 1% (28) of samples were
of unacceptable microbiology quality due to the presence of L. monocytogenes at
102 cfu/g or more (27), and C. jejuni (1).
For some cooked sliced meats the ACC can reach 10 8 cfu/g or more during shelf
life due to the presence and growth of lactic acid bacteria without detrimental
effect to the product. However presence of Gram negative bacteria in high
numbers (>107 cfu/g) may cause spoilage31, usually due to slime production or
taste taint. High ACC results from samples were therefore examined to identify
the bacteria that predominated. The majority (88% 1587/1804) contained lactic
acid bacteria (Table 5), which comprised the entire component (100%) of the
9
ACC, 2% (40) of samples with high ACC levels contained Gram-negative oxidase
positive bacteria and 10% (177) of samples contained Gram-negative oxidase
negative bacteria (Table 5).
Table 5. Predominant microflora of high Aerobic Colony Counts from VP/MAP
cooked meats at end of shelf life
Predominant bacteria of ACC
Ham, tongue
(≥107 cfu/g;
n=757)
Other meats
(≥106 cfu/g;
n=1047)
All meats
Gram positive, catalase negative (Lactic
acid bacteria*)
Gram negative, oxidase positive
(e.g. Pseudomonas spp., Aeromonas)
Gram negative, oxidase negative
(e.g. Enterobacteriaceae, Acinetobacter)
715 (94%)
872 (83%)
1587 (88%)
12( 2%)
28 (3%)
30 (4%)
147 (14%)
(n=1804)
40 (2 %)
177 (10%)
*, lactobacilli, streptococci
Re-evaluation of the results following interpretation of high ACCs according to
their predominant flora (>108 cfu/g LAB; >107 cfu/g Gram negative bacteria)
classified 46% (1381/2981) of the VP/MAP meat samples as satisfactory, 20%
(600) as acceptable, 33% (972) as unsatisfactory and 1% (28) as unacceptable
microbiology quality (Fig. 2).
Fig 1 Microbiological quality of VP/MAP cooked meats at end
of shelf-life; without interpretation of high ACCs (n=2981)
Acceptable
13%
Unsatisfactory
62%
Satisfactory
24%
Unacceptable
/potentially
hazardous
1%
10
Fig 2 Microbiological quality of VP/MAP cooked meats at end
of shelf-life; with interpretation of high ACCs (n=2981)
Acceptable
46%
Satisfactory
20%
Unacceptable
/potentially
hazardous
1%
Unsatisfactory
33%
Product information in relation to microbiological quality
Data analysis was carried out on samples and product information using the
PHLS microbiological guidelines with interpretation of ACCs.
Type of VP/MAP cooked meat
Almost half (45%; 1351/2981) of the VP/MAP meat samples collected were ham,
followed by turkey (18%), chicken (17%), beef (12%) and pork (7%) (Fig 3).
Significantly more samples of chicken (45%; 224/495), beef (43%; 160/371) and
turkey (41%; 219/523) were of unsatisfactory or unacceptable quality compared
with ham (23% 317/1351) or pork (32% 67/206) (p=0.0001).
11
Fig 3 Types of VP/MAP ready-to-eat meat collected from
retail premises (n=2981)
Chicken
17%
Turkey
18%
Other (Duck, lamb,
haslet etc) 1%
Beef
12%
Pork
7%
Ham
45%
Over two-thirds of samples collected were sliced meat (67%; 1992/2981), 18%
(549) were wafer thin meats, 4% (122) were portions (e.g. chunks, shavings,
strips) and for 11% (318), this information was not recorded. The proportion of
sliced, portioned and other meat products of unsatisfactory or unacceptable
microbiological quality was higher (36%, 37% and 33%, respectively) when
compared to wafer thin meat (26%).
This finding was only significant when
comparing sliced meat to wafer thin meat (p=0.0001).
Most samples (80%; 2391/2981) were MAP, 18% (525) were VP, and for 2% (65)
of samples, this information was not recorded. Significantly more samples that
were VP (43%; 228/525) were of unsatisfactory or unacceptable microbiological
quality compared to those that were MAP (31%; 751/2391) (p=0.0001).
The majority of cooked meat samples (95% 2844/2981) were not packaged on
the premises, 4% (113) were and for 1% (24) of samples, this information was
not recorded.
Although represented in comparatively low numbers, more
samples packaged on the premises were of unsatisfactory or unacceptable
12
microbiological quality (48%; 54/113) compared to meat samples packaged
elsewhere (32%; 934/2844).
Four (119/2981) percent of samples were packed more than once in their history
as a ready-to-eat product, 22% (676) were not, but for 74% (2186) of samples
this information was not known. Proportionally the number of unsatisfactory or
unacceptable VP/MAP meat samples packed more than once was higher (38%)
compared to those that were not (36%), however this finding was not statistically
significant.
The majority (96%; 2871/2981) of meat samples were not organic, 1% (27) were
and for 3% (83) of samples, this information was not recorded. The proportion of
samples of unsatisfactory or unacceptable microbiological quality that was not
produced organically was higher (33%) when compared to organic meats (15%),
however this was not statistically significant.
Approximately two-thirds (67%; 1990/2981) of samples were recorded as of UK
origin, 12% (360) were non-UK produced (i.e. of other EU or Third Country
origin) and for 21% (631) of samples, this information was not recorded. There
was no significant difference in the proportion of meat samples of unsatisfactory
or unacceptable microbiological quality when comparing samples that were
imported (30%) with those that were not (35%).
Cooked meats packaged on the premises
Of the 113 meat samples packaged on the premises, most were VP (96%; 108),
and the remainder were MAP (4%; 5). Forty eight percent (52/108) and 40%
(2/5) of VP and MAP meat, respectively, packaged on the premises were of
unsatisfactory or unacceptable microbiological quality.
However it should be
noted that the sample number of MAP meats packed on the premises is small
and that no statistical conclusions should be drawn from these results.
13
Almost two-thirds (63%) of samples were packaged with machinery used for only
cooked ready-to-eat food, and a quarter (26%) were packaged with machinery
used for both raw meat and cooked/ready-to-eat food (Table 6). The different
uses of the packaging machinery had no significant effect on the microbiological
quality of the VP/MAP meats with regard to samples of unsatisfactory or
unacceptable microbiological quality (Table 6).
Most (86%) samples were packed using packaging materials kept in a visually
clean area and away from any source of contamination as judged by the
sampling officer (Table 6). No significant difference in the proportion of samples
that were of an unsatisfactory or unacceptable microbiological quality was found
between those packed in a visually clean area compared to those that were not
(Table 6).
The majority (81%: 92/113) of samples were packed with machinery that was
cleaned in between uses, 10% were not and for 9% of samples, this information
was not recorded. Of the samples collected from premises where the machinery
was cleaned in between uses, almost half (46% 42/92) of the machinery were
cleaned using disinfectant, 30% using detergent, 15% using a sanitizer and for
9%, this information was not recorded. There was no significant difference in the
microbiological quality of VP/MAP meats in relation to the cleaning practices
used on packaging machinery (Table 6).
Forty five percent of samples were packaged using machinery that had the
original manufacturers machinery instructions available (Table 6). However, the
presence or not of the original manufacturers machinery instructions had no
significant effect on the microbiological quality of the VP/MAP meats with regard
to samples of unsatisfactory or unacceptable microbiological quality (Table 6).
14
Table 6. Microbiological quality of VP/MAP meats in relation to packaging
practices on the premises
Packing Details
No. Samples
No. samples of unsatisfactory or
unacceptable quality (%)
(n=113)
(%)
Packaging machinery used for:
Raw Meat
Cooked RTE* food
Both raw meat & cooked RTE food
Not Recorded
8
71
29
5
(7)
(63)
(26)
(4)
2/8 (25%)
35/71 (49%)
14/29 (48%)
3/5 (60%)
Packing material kept in a visually
clean area:
Yes
No
Not Recorded
97
6
10
(86)
(5)
(9)
47/97 ((48%)
1/6 (17%)
6/10 (60%)
Packing machinery cleaned in
between uses:
Yes
No
Not Recorded
92
11
10
(82)
(9)
(9)
44/92 (48%)
5/11 (45%)
5/10 (50%)
Original manufacturers instructions
available for packaging machinery:
Yes
No
Not Recorded
51
52
10
(45)
(46)
(9)
24/51 (47%)
25/52 (48%)
5/10 (50%)
Meat packaging included in retailer’s
hazard analysis system:
Yes
No
Not Recorded
92
12
9
(82)
(10)
(8)
43/92 (47%)
6/12 (50%)
5 /9 (55%)
Meat product with shelf-life of ≥10
days:
Yes
No
Not Recorded
88
20
5
(78)
(18)
(4)
40/88(45%)
11/20(55%)
3/5 (60%)
Comprehensive risk assessment
undertaken for product with shelf-life
≥10 days (n=88)
Yes
No
Not known
Not Recorded
56
23
4
5
(64%)
(25%)
(5%)
(6%)
23/56 (41%)
12/23 (52%)
2/4(50%)
3/5 (60%)
*RTE, Ready-to-eat
For most (82%) samples packaged on the premises, meat packaging was
included in the retailer’s hazard analysis system (Table 6). The inclusion or not
15
of meat packaging in the hazard analysis system had no significant effect on the
microbiological quality of the VP/MAP meats with regard to samples of
unsatisfactory or unacceptable microbiological quality (Table 6).
Over three-quarters (78%) of the products packed on the premises had a shelf
life of more than 10 days, and of these 64% had undertaken a comprehensive
risk assessment (Table 6). A higher proportion of the samples sampled with a
shelf life of 10 or more days and where a risk assessment had not been
undertaken for product shelf life were of unsatisfactory or unacceptable quality
(52%) compared to those sampled which had such a risk assessment undertaken
(41%), although this was not significant (Table 6).
Premises Information
Storage and display temperature
The majority (97%) of samples were stored in a visually clean display area as
judged by the sampling officer, and most samples (87%) were displayed in
upright units with shelves (Table 7). There was no significant difference in the
proportion of unsatisfactory or unacceptable samples and the visual cleanliness
or the type of display unit the VP/MAP meat was displayed in (Table 7).
At the time of sampling, the air temperature between VP/MAP meat on display
was equal or below 5°C for over two-thirds (68%) of samples, and above 5°C and
equal or below 8°C for a further quarter (23%) of samples (Table 7). The storage
temperature of packaged meat on display had no significant effect on the
microbiological quality of VP/MAP meat with regard to samples of unsatisfactory
or unacceptable microbiological quality (Table 7).
Most (93%) samples had
storage temperature information present on the packaging, of which 61% advised
to keep the product refrigerated and 32% specified a refrigeration temperature
(Table 7).
Where a particular storage temperature was provided on the
16
packaging, 75% specified to store between 0-5°C, 15% between 2-5°C, 5%
specified at less than 7°C and another 5% specified at less than 8°C.
Table 7 Microbiological quality of VP/MAP meats in relation to their display
and storage
Storage and display details
Display area visually clean:
Yes
No
Not recorded
No. Samples
(n=2981)
(%)
No. samples with unsatisfactory
or unacceptable quality (%)
2883
39
59
(97)
(1)
(2)
969/2883 (34%)
9/39 (23%)
22/57 (37%)
2604
137
72
107
(87)
(4)
(2)
(3)
848/2604 (32%)
54/137 (39%)
29/72 (40%)
44/107 (41%)
61
(2)
Storage temperature on
packaging:
Keep refrigerated
No temperature indicated
Temperature specified
Not recorded
1806
145
953
77
(61)
(5)
(32)
(2)
535/1806 (29%)
53/145 (36%)
373/953 (39%)
39/77 (50%)
Air temperature between
packaged meat on display:
Below 5ºC
Above 5ºC and equal/below 8ºC
Above 8ºC
Not recorded
2030
685
160
106
(68)
(23)
(5)
(4)
668/2030 (33%)
242/685 (35%)
51/160 (32%)
39/106 (37%)
Temperature of display unit
monitored by retailer:
Yes
No
Not recorded
2752
103
126
(93)
(3)
(4)
919/2752 (33%)
39/103 (38%)
42/126 (33%)
Temperature of display unit
monitored by: (n=2752):
Link to local/remote computer
Thermometer in unit
Temperature probe
931
1211
610
(34)
(44)
(22)
325/931 (35%)
438/1211(36%)
237/610 (39%)
Type of display unit:
Upright with shelves
Upright with hooks
Chest
Other (e.g. flat units, wire racks,
boxes)
Not recorded
25/61
(40%)
The majority (93%) of retailers monitored the temperature of the display unit, of
which a thermometer in the unit was used by almost half (44%), 34% used a link
17
to a local/remote computer, and 22% used a temperature probe (Table 7). A
higher proportion of the samples from display units where temperature was not
monitored were of unsatisfactory or unacceptable quality (38%) compared to
those from units where temperature was monitored (33%), although this was not
significant. In display units where temperature was monitored, more samples
sampled from units where a temperature probe was used were more likely to be
of unsatisfactory or unacceptable quality (39%) compared to those sampled from
units where temperature was monitored by a link to a computer (35%) or by a
thermometer in the unit (36%) (Table 7).
Type of premises
Sixty one percent (1822/2981) of samples were collected from supermarkets, and
30% (909) from convenience/corner shops. The remaining 9% of samples were
collected from licensed butchers (3%; 87), greengrocers (1%; 23), delicatessens
(1%; 20) non-licensed butchers (<1%; 3), market stalls (<1%; 7) and other
premises (4%; 107), such as bakeries, wholesalers and farm shops (Table 8).
Fifty-two percent (950/1822) of samples from supermarkets were ‘own label’
products. In comparison, virtually all samples from greengrocers, butcher shops,
and delicatessens were ‘branded’ products.
The proportion of VP/MAP meat samples from convenience/corner shops (35%),
delicatessens (40%), market stalls (42%), greengrocers (52%), licensed butchers
(53%)
and
other
premises
(42%)
of
unsatisfactory
or
unacceptable
microbiological quality was higher when compared to those collected from
supermarkets (31%). This finding was only significant when comparing samples
from convenience shops (p=0.0302), licensed butchers (p=0.0001), and
greengrocers (p=0.0405) to those from supermarkets.
18
Food hygiene inspection
Half (50%) of the samples were collected from premises categorised as
Inspection Rating Category C (inspected at least every 18 months) (Table 8).
More samples of unsatisfactory or unacceptable microbiological quality were
collected from premises with inspection rating category D (37% 211/569) than
premises with ratings of C (31%), B (35%) and A (26%) (Table 8). This finding
was only significant when comparing samples collected from premises rated as
category D to those rated as C (p=0.01).
Most of the samples were obtained from premises categorised in consumer at
risk score 5 (few numbers of customers, 60%) and 10 (intermediate numbers of
customers, 23%) (Table 8). In proportion more samples collected from premises
with consumer at risk scores of 0 to 5 (very few to few numbers of customers,
34%) were of unsatisfactory or unacceptable microbiological quality compared to
those from premises with consumer at risk scores of 10 to 15 (intermediate to
substantial number of customers, 30%) (Table 8).
Most samples were collected from premises that had a confidence in
management score 5 (moderate confidence in management/control systems,
39%) and 10 (some confidence in management/control systems, 37%) (Table 8).
There was no significant difference in the proportion of unsatisfactory or
unacceptable samples from premises with different confidence in management
scores (Table 8).
Hazard analysis system
Eighty percent of samples were collected from premises that had a hazard
analysis system in place (63% documented, 11% undocumented; 6%
documentation status not recorded) (Table 8). Samples collected from premises
without a hazard analysis system in place were more likely to be of unsatisfactory
or unacceptable microbiological quality (36%) compared to those collected from
premises where hazard analysis was in place (33%) (Table 8).
19
Table 8 Microbiological quality of VP/MAP meats in relation to premises
details
Premises Details
No. Samples
(n=2981)
(%)
No. samples of unsatisfactory
or unacceptable quality (%)
Premises Type
Supermarket
Convenience/corner shop
Licensed butchers
Delicatessen
Greengrocers
Non-licenced butchers
Other (e.g. baker, market stalls, wholesalers,
petrol forecourt)
Not recorded
1822
909
87
20
23
3
114
(61)
(30)
(3)
(1)
(1)
(<0.1)
(4)
567/1822 (31%)
321/909 (35%)
46/87 (53%)
8/20
(40%)
12/23
(52%)
1/3
(34%)
45/114 (39%)
3
(<0.1)
-
46
220
1481
569
304
31
330
(2)
(7)
(50)
(19)
(10)
(1)
(11)
12/46
78/220
466/1481
211/569
96/304
12/31
125/330
(26%)
(35%)
(31%)
(37%)
(31%)
(40%)
(38%)
22
1792
706
46
415
(1)
(60)
(23)
(2)
(14)
11/22
610/1792
219/706
6/46
154/415
(50%)
(34%)
(31%)
(13%)
(37%)
138
1158
1095
135
32
423
(5)
(39)
(37)
(4)
(1)
(14)
50/138
368/1158
369/1095
42/135
4/32
157/423
(36%)
(32%)
(34%)
(31%)
(12%)
(37%)
1877
337
164
324
279
(63)
(11)
(6)
(11)
(9)
636/1877
118/37
41/164
117/324
88/279
(33%)
(35%)
(25%)
(36%)
(31%)
2320/2981
1441/2320
509/2320
92/2320
150/2320
128/2320
395/2981
266/2981
(78)
(62)
(22)
(4)
(6)
(6)
(13)
(9)
788/2320
509/1441
155/509
34/92
49/150
35/128
130/395
88/266
(34%)
(35%)
(30%)
(37%)
(33%)
(27%)
(33%)
(33%)
Inspection Rating Category
Category
A
B
C
D
E
F
Not Recorded
Minimum Frequency of
Inspection
At least every 6 months
At least every year
At least every 18 months
At least every 2 years
At least every 3 years
At least every 5 years
Consumer at Risk Score
0 (Very few)
5 (Few)
10 (Intermediate)
15 (Substantial)
Not recorded
Confidence in Management
0 (High)
5 (Moderate)
10 (Some)
20 (Little)
30 (None)
Not recorded
Hazard Analysis system
In place and documented
In place and undocumented
In place; documentation status not recorded
Not in place
Not recorded
Management Food Hygiene training
Received training and attended
-Basic 6 hour course
-Intermediate course
-Advanced course
-Other recognised course
-Not specified
No training
Not Recorded
20
Food hygiene training
Over three-quarters of samples (78%) were collected from premises whose
managers had received food hygiene training (Table 8). No significant difference
was found between premises with managers that had received food hygiene
training or not and samples that were of unsatisfactory or unacceptable
microbiological quality (Table 8).
Discussion
Although listeriosis is a relatively rare disease, the severity of the disease and the
frequent involvement of manufactured foods, especially during outbreaks, mean
that the social and economic impact of listeriosis is among the highest of the
foodborne diseases14. An important factor in foodborne listeriosis is that the
pathogen can grow to significant numbers at refrigeration temperatures when
given sufficient time. L. monocytogenes is able to grow in sliced meats, even if
stored under appropriate refrigeration conditions32-34.
Factors affecting the
growth of L. monocytogenes in foods include product formulation, storage time
and temperature, and interactions with other microorganisms present in the
product. In VP and MAP meats, lactic acid bacteria (LAB) can reach the
stationary of the growth cycle phase without product spoilage. This can slow, or
even prevent, the subsequent growth of L. monocytogenes. However, the extent
of that growth suppression is not known with certainty 35.
The shelf life of a product is the time after production during which it remains
acceptable, i.e. both safe and of good quality, for consumption36. The end point
of shelf life for perishable chilled foods may be defined by levels of
microorganisms present based on recommended guidance 30,31. A number of
different groups of spoilage organisms could be present in chilled meat products,
including LAB, Enterobacteriaceae and Pseudomonads37. The total bacterial
count (Aerobic Colony Count (ACC)) therefore can provide an assessment of the
overall microbiological levels within a food product. However determination of
count levels needed to be augmented by tests to determine the types of flora
21
present, as a high ACC in itself may not indicate poor quality. Using this
information about component microflora, this study has shown that 66% of
MAP/VP meat samples at end of shelf-life were of satisfactory/acceptable quality,
a third (33%) were of unsatisfactory quality and 1% were of unacceptable
microbiological quality, or were a potential risk to public health according to
published microbiological guidelines30.
Unsatisfactory microbiological results
were mainly due to high levels of ACC, namely LAB at 10 8 cfu/g or more and/or
Enterobacteriaceae in excess of 104 cfu/g. High ACCs and Enterobacteriaceae
levels can indicate that the cooking process was inadequate, that post
processing contamination had occurred, that the length of time and temperature
control in storage or facilities was inadequate to prevent bacterial growth, or that
a combination of these factors was involved. A previous UK study in 1995
reported a lower proportion (10%) of pre-packed sliced cooked meats at end of
shelf-life that had LAB present at or over 10 8 cfu/g, and found that microbial
growth of spoilage organisms, such as LAB and Enterobacteriaceae, had
occurred during storage after slicing and packaging1. It is therefore important to
minimise post processing contamination as well as enforcing strict temperature
control throughout storage and whilst on retail sale to minimise any proliferation
of the organisms in food.
The pathogens L. monocytogenes, Staph. aureus, and C. perfringens were
detected in 190 (6.4%), 9 (0.3%) and 4 (0.1%) samples, respectively in this
study.
In addition, Campylobacter spp. was detected from one sample.
An
earlier UK study of pre-packed sliced meats tested at the end of shelf life found
that 5.3% of samples contained L. monocytogenes, 1% Staph. aureus, 0.2% C.
perfringens, and Campylobacter spp. was detected from one sample1. Three
regional studies in England during 2002 reported a similar prevalence of L.
monocytogenes in MAP/VP sliced meats at end of shelf-life (5.0% - 5.3%)15-17.
The prevalence of L. monocytogenes at unacceptable levels observed in
MAP/VP meats in the current study (1%) was comparable to that previously
found in England (0.6%-1.7%)1,15-17 Denmark (1.4%)38 but higher than that in
22
Ireland (0%)39. The presence of these organisms, and in particular the presence
of L. monocytogenes at unacceptable levels, demonstrates the need for good
hygiene practices during processing to prevent contamination and emphasises
the importance of strict temperature controls during the shelf-life of VP/MAP
ready-to-eat sliced meats.
In 2002 to 2003 there was a marked increase in the number of Listeriosis cases
reported in England and Wales and included three outbreaks (one linked to
butter, two linked to sandwiches) 40. Furthermore, the same rise in Listeriosis has
also been observed in other European countries (Denmark, Germany,
Netherlands)
41.
Microbiological sub-typing has been helpful in unravelling what
appears to be a complex epidemiological picture. The predominant typing
character (48%; 1/2/IX/NT) of L. monocytogenes recovered from VP/MAP meat
samples of unacceptable microbiological quality in this study has also been
observed in a very small number (4) of human cases of L. monocytogenes during
2003 (K Grant, HPA Centre for Infections pers comm).
A greater proportion of VP meats at end of shelf life were of unsatisfactory or
unacceptable microbiological quality (43%) compared to MAP meats (31%).
Those meats packed on the retail premises had a higher proportion of
unsatisfactory and/or unacceptable samples (48%) compared to those that were
not (32%). Additionally, a higher proportion of meats packed on the premises
with a shelf life of 10 days or more and where a risk assessment had not been
undertaken for product shelf life were shown to be of unsatisfactory and/or
unacceptable microbiological quality. In relation to the potential for growth of
psychrotrophic C. botulinum during storage, the UK industry code of practice
advises that the shelf life of a chilled MAP/VP food (i.e. one stored at 3-8°C)
should not exceed 10 days unless its safety under expected storage conditions
can be demonstrated3,4,41. Due attention should also be given to the effect on
storage for other food pathogens, such as L. monocytogenes, which would also
be relevant to the subsequent shelf-life3. The influence of packaging type and
23
place of packaging on L. monocytogenes contamination and microbiological
quality of MAP/VP meats warrants further investigation.
Slicing is a process that is carried out post-cooking and poses a microbiological
risk because of the potential for recontamination via the slicing blade. In recent
years, wafer thin sliced meats have been introduced onto the market. This
product is sliced thinner than traditional sliced meats. In this study, slice width
was found to have an effect on microbiological quality, with more sliced meats
being of unsatisfactory and/or unacceptable quality (36%) compared to wafer thin
meats (26%). This may be due to a difference in the way the meat is sliced and
equipment cleaned. Cooked meat slicing machines if incorrectly cleaned can be
a source of contamination and cross-contamination 42,43.
Samples collected from display units where temperature was not monitored were
more likely to be of unsatisfactory or unacceptable quality (38%) compared to
those from units where temperature was monitored (33%). In conjunction with
implementing HACCP principles as the basis for the retailers’ product safety
management systems, correct maintenance of storage temperature is vital for
ensuring the microbiological safety and stability of chilled food products. The
performance of the proposed distribution chain should therefore be validated and
monitored and taken into account when specifying shelf life of the product6.
The long shelf life of VP/MAP meats may allow the population of L.
monocytogenes to reach unacceptable levels, i.e. over 100 cfu/g. It is clear that
efforts must be made either to ensure that the product does not become
contaminated before final packaging, or to reduce shelf life so that
recontamination does not result in the growth of the organism to high numbers.
Where the product is sold through other outlets, the performance of the proposed
distribution chain should be taken into account when specifying shelf life of the
product6, in particular the point that refrigeration storage temperatures will vary
24
from pre-distribution, retail and the consumer home. An alternative strategy
would be to re-formulate products to retard greatly, or inhibit altogether, the
growth of this organism.
Acknowledgements
The authors would like to thank all the staff in the Environmental Health
Departments throughout the UK who collected samples for this study, and all the
staff in both HPA and non-HPA laboratories who performed microbiological
examination. Thanks are extended to FSML and LEP (HPA Centre for Infections)
for typing isolates, to David Lock at LACORS for co-ordinating the participation of
Environmental Health Practitioners and advice from the LACORS Food
Examination Focus Group, to the Regional Food, Water and Environmental Coordinators Forum and Heather Aird for advice on the sampling protocols, and to
Lillian Hucklesby for entering the data.
25
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29
Annex 1: Participating Laboratories and Local Authority Food Liaison Groups
Table I: Participating HPA and HPA Collaborating Laboratories and number of
samples
HPA Region
Laboratory Name
East
Chelmsford
Number of Samples
143
Norwich
167
London
London FWEM1
139
South East
Ashford
102
Brighton
192
West Midlands
North West
North East, Yorkshire & the Humber
South West
East Midlands
Reading
16
WEMS2
103
Birmingham
89
Coventry
129
Hereford
24
Shrewsbury& Telford
78
Stoke
102
Chester
55
Preston
190
Carlisle
34
Hull
119
Leeds
92
Middlesbrough
123
Newcastle
101
Sheffield
146
Bristol
161
Exeter
67
Gloucester
47
Plymouth
22
Truro
89
Leicester
130
Lincoln
Total
175
2835
1, London Food, Water & Environmental Microbiology Laboratory
2, Wessex Environmental Microbiological Service
Table II: Participating Other Laboratories and number of samples
Nation
Laboratory
Northern Ireland
Scotland
Belfast City Hospital
Aberdeen City Council Public Analyst
Edinburgh A & S Services
Glasgow Scientific Services
Bangor
Cardiff
Rhyl
Wales
Total
Number of Samples
53
4
2
30
55
37
19
200
30
Table III: Participating Food Safety Liaison Groups and number of samples
Local Authority Food Liaison Group
Berkshire
Number of Samples
11
Buckinghamshire
6
Cambridgeshire
40
Cheshire
Cleveland
39
67
Cornwall
89
Cumbria
41
Derbyshire
75
Devon
62
Dorset
Durham
40
24
East Sussex
81
Essex
80
Gloucestershire
57
LFCG1 Greater London NE Sector
22
LFCG Greater London NW Sector
LFCG Greater London SE Sector
28
28
LFCG Greater London SW Sector
24
Greater Manchester
72
Hampshire & Isle Of Wight
56
Hereford & Worcester
54
Hertfordshire & Bedfordshire
Humberside
33
108
Kent
102
Lancashire
108
Leicestershire
130
Lincolnshire
77
Merseyside
10
North Yorkshire
Northamptonshire
91
71
Northern Ireland Food Group2
53
Northumberland
21
Norfolk
120
Nottinghamshire
100
Scottish Food Enforcement Liaison Committee3
Shropshire
36
34
Somerset
27
South West Yorkshire
61
Staffordshire
112
Suffolk
67
Surrey
Tees Valley
57
3
Tyne & Wear
63
Wales North Group
80
Wales South East Group
39
Wales South West Group
2
Warwickshire
West Midlands
56
101
West of England
86
West Sussex
55
West Yorkshire
62
Wiltshire
Total
74
3035
1, London Food Co-ordinating Group
2, Northern Ireland Food Group comprises of the Eastern, Northern, Southern and Western Groups
3, SFELG comprises of Central Scotland, Fife & Tayside, Lothian & Scottish Borders, North Scotland, and West of
Scotland
31