LACORS/PHLS Co-ordinated Food Liaison Group Studies:
Microbiological Examination of Ready To Eat Cold Sliced
Meats and Pâté from Catering and Retail Premises.
R Elson, F Burgess, CL Little*, RT Mitchell and the Food, Water and
Environmental Surveillance Network†.
Environmental Surveillance Unit, Health Protection Agency Communicable Disease
Surveillance Centre, 61 Colindale Avenue, London, NW9 5EQ.
On behalf of the Local Authorities Co-ordinators of Regulatory Services and the
Public Health Laboratory Service.
Summary
During May and June 2002, a study of ready-to-eat cold sliced meats and pâtés from
catering and retail premises was undertaken to determine their microbiological quality.
Examination of 4,078 samples of ready-to-eat cold sliced meats and pâtés revealed that
most (75%) were of satisfactory/acceptable microbiological quality and 25% were of
unsatisfactory quality due to high Aerobic Colony Counts and high levels of
Enterobacteriaceae, Escherichia coli or Listeria spp.
Two samples (<1%) were of
unacceptable microbiological quality due to the presence of Campylobacter jejuni and
Listeria monocytogenes in excess of 100 cfu/g. Acceptable microbiological quality of
ready-to-eat sliced cold meats and pâtés was associated with premises that had
management food hygiene training and hazard analysis in place. Poor microbiological
quality was associated with storage or display of meats and pâtés above 8°C, pre-sliced
meats, infrequent cleaning of meat slicing equipment, poor physical separation of raw
meat and ready to eat meat products and movement of staff between areas used for raw
meats and ready-to-eat foods.
*Author for correspondence
†, FWES Network comprises Laboratories listed in Annex I
1
Introduction
Cooked sliced meats and pâtés are regarded as high-risk foods1.Their manufacture and
sale is well regulated in the UK, production in approved premises being controlled by the
Meat Products (Hygiene) Regulations 1994 (as amended)2
and production in retail
premises for sales direct to consumers being controlled by the Food Safety (General Food
Hygiene) Regulations 19953 and the Food Safety (Temperature Control) Regulations
19954. In response to the 1996 Central Scotland Escherichia coli O157 outbreak5 and the
subsequent inquiries6,7, premises preparing handling, selling and supplying unwrapped
raw meat together with ready to eat foods as part of a retail operation in the UK now
require a licence, the granting of which is dependent upon enhanced food hygiene
requirements3.
Meat, including pre-cooked meat, forms an important part of the UK diet and
consumption patterns have shown marked changes over the last two decades. Between
1979 and 1999 in the UK, consumption of cooked poultry more than quadrupled and
cooked bacon and ham consumption increased by around 10 grams per person per week
in the same time period8. The role of cooked sliced meats and pâtés as a vehicle or source
of infection of a number of pathogens is well documented9,10. It has been highlighted that
in order to work towards a 20% reduction in foodborne disease by April 2006 in line with
the Food Standards Agency’s target11, more emphasis needs to be placed on reducing
infection with Campylobacter spp.. Although the commonest cause of acute bacterial
gastroenteritis, the epidemiology of campylobacter infection remains poorly understood.
While the widespread contamination of raw poultry and poultry products with
Campylobacter spp. is well documented10,12, the role of other foods as the source of
infectious disease is less clear. In May 2000 a population-based sentinel surveillance
scheme for campylobacter infection was launched by the Public Health Laboratory
Service (PHLS) in England and Wales with the aim of generating hypotheses for
campylobacter infection systematically by the integration of standardised epidemiological
and microbiological typing data. During the first year of the scheme the study found that
indigenous cases infected with C. jejuni were more likely to report the consumption of
pre-cooked cold meats13.
Cold cooked meats have also been implicated in a US
2
epidemiological study of campylobacter infection. The US researchers found that cases
were more likely to report the consumption of chicken luncheon meat and ham than
controls14.
Cold ready to eat meats, pâtés and similar meat products have also been associated with
outbreaks of Listeria monocytogenes15,16. L. monocytogenes, whilst responsible for less
morbidity in England and Wales than Campylobacter, remains a cause for concern due to
the increased risk posed to vulnerable groups17. L. monocytogenes is ubiquitous in the
environment, and its ability to colonise food-processing environments is well
recognised18. This pathogen is also able to grow at refrigeration temperatures19. A small
proportion of ready-to-eat cold meats and pâté in the UK have been shown to be
contaminated with L. monocytogenes and occasionally at levels higher than 102 cfu/g20,21.
This study was the first of two studies that formed the 2002/2003 Local Authority
Coordinators of Regulatory Services (LACORS)/PHLS Coordinated Food Liaison Group
Microbiological Sampling Programme. The study aimed to establish the microbiological
quality of ready-to-eat cold sliced meats and pâté from catering and retail premises, and
to investigate possible links hypothesised by the PHLS Campylobacter Sentinel
Surveillance Scheme between foodborne campylobacter infection and the consumption of
cold sliced meats and pâté.
Materials and Methods
Sample Collection
Cold sliced ready to eat meats and pâtés were collected from supermarkets, delicatessens,
butchers, market stalls, hotels, public houses, hospitals, residential care homes
restaurants, cafés and school and staff restaurants and examined in PHLS and non-PHLS
laboratories in the UK between the 1st May and 30th June 2002 using a standardised
protocol and reporting system. Samples (100g) consisted of meats and pâté cooked and
sliced on or off the premises from where the sample was taken. Fermented, dried and
stuffed meats, fish or fish products (except pâtés), frozen samples and unopened packages
3
originating from premises other than those where the sample was taken were specifically
excluded from this study. Samples were collected by staff from local Environmental
Health Departments and were transported to the laboratory in accordance with the Food
Safety Act 1990 Code of Practice No.722 and advice provided in the LACORS guidance
on microbiological food sampling23.
Information on the catering or 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 cooking, slicing and storage of meats and pâté, documentation of
a hazard analysis system and the level of food hygiene training received by the manager.
Food hygiene inspections are carried out in a way that focuses enforcement authority
resources on premises presenting most risk to consumers. To do this, food hygiene
inspections are carried out in accordance with Food Safety Act 1990 Code of Practice No
924 which specifies that, amongst other factors, the number of consumers at risk and
confidence in management control systems (including the application of HACCP based
systems) should be assessed to produce a risk rating of the premises. The risk rating
determines the frequency of inspection and ranges from Category A (highest risk,
inspected every 6 months) to F (lowest risk, inspected every 5 years). Consumer at risk
scores range from 0 (Very few) to 15 (Substantial) and confidence in management ranges
from 0 (High Confidence) to 30 (No Confidence).
Isolation of bacteria
Aerobic Colony Counts (ACC), Enterobacteriaceae, E. coli, L. monocytogenes and other
Listeria spp., and Salmonella spp., were enumerated or detected in accordance with
PHLS Standard Microbiological Methods25-30Campylobacter spp. were detected 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 PHLS Standard Microbiological Method F2131. Isolates of
Campylobacter spp. were sent to the Laboratory of Enteric Pathogens (LEP), Central
Public Health Laboratory (CPHL) for confirmation and typing. L. monocytogenes at
4
levels at 102 cfu/g or more were sent to the Food Safety Microbiology Laboratory
(FSML), CPHL for further characterisation. Microbiological results were compared to
the PHLS Guidelines for the microbiological quality of some ready-to-eat foods sampled
at the point of sale32 (Table 1). Satisfactory results indicate good microbiological quality,
acceptable results are an index reflecting a borderline limit of microbiological quality,
whereas unsatisfactory results indicates that further sampling may be necessary and that
environmental health officers may wish to undertake a further inspection of the premises
concerned to determine whether hygiene practices for food production or handling are
adequate or not. An unacceptable microbiological result indicates that urgent attention is
needed to locate the source of the problem.
Statistical analysis
Descriptive and statistical analysis of the data was undertaken using Microsoft Excel
version 7 and Epi Info version 6.04d. Relative proportions were compared using the Chisquared test (χ2) and χ2 test for trend. A probability value of less than 5% was deemed to
be significant.
Table 1. Key to classification in the PHLS Microbiological Guidelines for cooked
meat and pâté sampled at the point of sale 32
Criterion
Microbiological quality (cfu per gram unless stated)
Satisfactory
Acceptable
Unsatisfactory
Aerobic Colony Count Cat. 3†
<105
105 - <106
‡
6
Aerobic Colony Count Cat. 4
<10
106 - <107
2
Enterobacteriaceae
<10
102 - <104
Escherichia coli (total)
<20
20 - <102
Listeria spp. (total)
<20
20 - <102
Listeria monocytogenes
<20
20 - <102
Campylobacter spp.
Not detected in 25g
Salmonella spp.
Not detected in 25g
†; cooked ham, tongue, ‡; other cooked meats and pâté, *, N/A; Not applicable
106
107
104
102
102
N/A
Unacceptable/
potentially
hazardous
N/A*
N/A
N/A
N/A
N/A
102
Detected in 25g
Detected in 25g
Results
A total of 2,894 cold meats and 1,184 pâtés collected from 2288 catering and retail
premises were examined in 38 laboratories (31 PHLS and 7 non-PHLS) in England,
Wales, Scotland and Northern Ireland.
368 Local Authorities, involving 52 Local
5
Authority Food Liaison Groups, submitted samples (Annex 1). A further 35 samples did
not fit the criteria described in the study protocol and were not included in the analysis.
Microbiological quality of cold ready to eat sliced meats
Over half (54%) of the cooked sliced meat samples were satisfactory, 20% were
acceptable, and 26% were of unsatisfactory microbiological quality (Figure 1). However,
two (<1%) samples were of unacceptable microbiological quality due to the presence of
Campylobacter jejuni HS18 Phage Type 44 (beef sample) and L. monocytogenes serotype
4b at 3.4 x 104 cfu/g (ham sample). Unsatisfactory results were due to high ACCs (≥107
cfu/g for cooked ham and tongue samples; ≥106 cfu/g for other sliced meat samples), or
high levels of Enterobacteriaceae (≥104 cfu/g), E. coli (≥102 cfu/g), or Listeria spp. (L.
innocua ≥102 cfu/g) (Table 2).
Table 2. Microbiological results of 4,078 ready to eat cold meat and pâtés
ND*
in
25g
Cold Meats (n=2894)
Aerobic Colony Count
Enterobacteriaceae
E. coli (total)
Listeria spp. (total)
-L. monocytogenes
Salmonella spp.
Campylobacter spp.
Pâté (n=1184)
Aerobic Colony Count
Enterobacteriaceae
E. coli (total)
Listeria spp. (total)
-L. monocytogenes
Salmonella spp.
Campylobacter spp.
2,694
2,887
2,823
1134
D§
in
25g
<10/
<20/
<100†
10/20
-<102
102 <103
103 <104
104 <105
105 <106
106 <107
107
NE¶
92b
1747a
2805b
60
407
43
3
277
304
26
1
584
213
8
530
127
3
1
1
526
68
357
14
464
10
1
4
4
8
20
20
7
70
75b
892a
1131b
53
99
12
191
94
36
1
272
52
3
177
29
160
17
114
140
2
1
2
6
6
2
16
175c
60c
1
43c
22c
1182
1168
*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
c, detected in 25g and present at <20 cfu/g
Meat types sampled included ham (49%), beef (19%), turkey (14%), pork (8%), chicken
(4%), and lamb (1%) (Table 3). Other meat types (bacon, gammon, brawn, haslet,
6
luncheon meat tongue, corned beef, duck, venison, pastrami, polony and mixed meats)
made up the remaining 5% of samples. The proportion of turkey meat samples of
unsatisfactory or unacceptable microbiological quality (40%) was higher when compared
to all other meat types (beef; 34%, pork; 34%, chicken; 30%, ham; 16%, and other types;
29%). This finding was significant when comparing turkey with ham (p<0.001), chicken
(p=0.04), or other meat types (p=0.03) (Table 3).
Figure 1. Microbiological Quality of Cold Sliced Meats and Pâté Samples based on
the PHLS Microbiological Guidelines32
Cold Sliced Meats
Pate
1%
23%
26%
Satisfactory
Acceptable
Unsatisfactory
53%
Unacceptable
15%
20%
62%
Microbiological quality of pâté samples
Approximately two-thirds (62%) of pâté samples were satisfactory, 15% were acceptable,
and 23% were of unsatisfactory microbiological quality. No pâté samples were of
unacceptable microbiological quality (Table 4, Figure 1). Unsatisfactory results were due
to high ACCs (≥107 cfu/g), or high levels of Enterobacteriaceae (≥104 cfu/g), E. coli
(≥102
cfu/g),
or
Listeria
spp.
(L.
seeligeri;
7
240
cfu/g).
(Table
2).
Table 3. Microbiological Quality of cold sliced meats based on the PHLS
Microbiological Guidelines32
Microbiological Quality
Meat Type
Satisfactory (%) Acceptable (%) Unsatisfactory
Ham
901
(63)
297
(21)
224
Beef
232
(42)
126
(23)
187
Turkey
170
(41)
75
(18)
166
Pork
112
(46)
49
(20)
82
Chicken
64
(53)
21
(17)
36
Lamb
12
(63)
2
(11)
5
Other (bacon, gammon etc.)
78
(60)
15
(11)
38
1569
(54)
585
(20)
738
Total
(%) Unacceptable (%)
(16)
1
(<1)
(34)
1
(<1)
(40)
0
(34)
0
(30)
0
(26)
0
(29)
0
(26)
2
(<1)
Two-thirds (66%) of pâté samples were meat based, 26% were poultry based, 4% were
fish or seafood based, 3% were vegetarian, and 1% were other pâté types (mixed meat
and poultry, duck and pork, game, liver and potted meat). For <1% of samples, the pâté
type was not recorded. The proportion of vegetarian and fish and seafood-based pâtés of
unsatisfactory quality was higher (42% and 31%, respectively) when compared to meat
(23%), poultry (21%), other pâté types (7%), and unknown pâté types (17%). This
finding was only significant when comparing vegetarian pâtés to meat, poultry, and other
pâté types (p<0.02) (Table 4).
L. monocytogenes was present in 2% of samples, and at levels below 20 cfu/g. L.
monocytogenes was detected in more fish and seafood pâté samples (10%; 4/42)
compared to meat (1%; 10/782), poultry (2%; 2/308) and vegetarian (3%; 2/31) pâtés.
This finding was significant when comparing fish and seafood pâté samples with meat
and poultry based pâtés (p<0.005).
8
Total
1423
546
411
243
121
19
131
2894
Table 4. Microbiological quality of pâté samples based on the PHLS Microbiological
Guidelines31
Pâté Type
Microbiological Quality
Total
Satisfactory (%) Acceptable (%) Unsatisfactory (%) Unacceptable (%)
Meat based
495
(63)
111
(14)
176
(23)
0
- 782
Poultry based
191
(62)
52
(17)
65
(21)
0
- 308
Fish/Seafood based
17
(40)
12
(29)
13
(31)
0
- 42
Vegetarian
15
(48)
3
(10)
13
(42)
0
- 31
Other (game, mixed meat)
13
(87)
1
(7)
1
(7)
0
- 15
Not recorded
5
(83)
0
1
(17)
0
6
Total
736
(62)
179
(15)
269
(23)
0
- 1184
Product history in relation to microbiological quality
Place of cooking cold meats
Approximately one third (32%) of cold meat samples were cooked on the premises from
which they were sampled, 65% were cooked elsewhere and for 3% of samples, this
information was not recorded. The proportion of cold meat samples of unsatisfactory or
unacceptable microbiological quality was significantly higher where the meat was cooked
elsewhere (27%) compared to meat samples cooked on the premises (21%) (p<0.001).
Of the 918 meat samples cooked on the premises, 12% had been cooked within 1 day of
sampling, 24% between 1-2 days, 22% between 2-3 days, 13% between 3-4 days, and
23% more than 4 days before sampling. For 4% of samples the time since cooking was
not known and for 2%, this information was not recorded. Significantly fewer samples
which had been cooked within one day were of unsatisfactory or unacceptable
microbiological quality (8%) compared to those which had been cooked and kept for
longer than this time (>1 day (21%), >2 days (21%), >3 days (30%), >4 days (24%))
(p<0.01).
Almost two-thirds (64%) of meat samples cooked elsewhere were supplied by
wholesalers, 9% were from butchers, and 5% were from supermarkets. Other suppliers
(including company warehouses, bakeries and sandwich filling suppliers) accounted for
9
16% of samples and this information was not recorded for 6% of samples. Significantly
more unsatisfactory or unacceptable samples were supplied by wholesalers (32%) and
butchers (29%) than those supplied by supermarkets (15%) and other suppliers (14%)
(p<0.01).
Over three-quarters (79%) of the cold meat samples were transported to the food
premises vacuum wrapped, 3% were wrapped in cling film and <1% were transported in
open trays. Other methods of packaging (grease proof paper, cook bags, sealed plastic
bag or container, closed trays, aluminium foil, box, modified atmosphere packaging,
cans) were used for 6% of samples. For 11% of samples the transportation packaging
was not known.
The small numbers of cold meats packaged in cling film were more
likely to be of unsatisfactory or unacceptable microbiological quality (33%) compared to
those packaged in vacuum packing (28%) or other wrapping methods (24%).
Slicing cold meats
The majority (88%) of cold meat samples were sliced on the premises, 10% were presliced elsewhere, and for 2% of samples, this information was not recorded. The
proportion of samples of unsatisfactory or unacceptable microbiological quality was
significantly higher where the meat was pre-sliced elsewhere (35%) compared to meat
sliced on the premises (24%) (p<0.0001).
Where the meat was sliced on the premises, most (81%) were sliced using a meat slicing
machine and a further 18% by using a knife. For 1% of samples, this information was not
known or not recorded. The proportion of unsatisfactory or unacceptable meat samples
sliced using meat slicers was higher (25%) when compared to those sliced with a knife
(22%), however this was not significant.
Where the meat was sliced using a meat-slicing machine, sampling officers noted that 6%
of slicers had damaged carriage guards and 11% were soiled. Proportionally, the number
of unsatisfactory or unacceptable meat samples sliced on damaged (29%) or soiled (26%)
10
slicing machines was higher compared to those sliced on unsoiled, undamaged slicing
machines (25%), however, this finding was not significant.
Most (87%) meat slicing equipment was only used to slice ready-to-eat food, 7% was not,
and for 6% of samples this information was not recorded. There was no significant
difference in the proportion of unsatisfactory or unacceptable meat samples that had been
cut with equipment used for ready to eat food only (24%) when compared to meat cut
with equipment that was not dedicated for ready to eat food only (25%).
Over three-quarters (78%) of meat slicing equipment was cleaned periodically throughout
the day while 16% was cleaned at the end of trading. For 6% of samples, this information
was not recorded. Significantly more samples were of unsatisfactory or unacceptable
microbiological quality when sliced with equipment cleaned only at the end of trading
(30%) than those sliced using equipment cleaned regularly throughout the day (23%)
(p=0.005).
Manufacture of pâté
Almost a fifth (18%) of pâtés were made on the premises from which they were sampled,
80% were made elsewhere and for 2%, this information was not recorded. In contrast to
the cold meat samples, there was no significant difference between the proportion of
unsatisfactory pâté samples when comparing pâtés made on the premises (24%) with
those supplied from elsewhere (22%).
Of 180 meat and poultry based pâté samples made on the premises, 41% were made by
flash frying the livers followed by further heating and 27% were made by flash frying the
livers followed by further processing. Less samples which had been cooked by flash
frying the livers followed by further heating were of unsatisfactory microbiological
quality (20%) compared to those which had been cooked by flash frying followed by
further processing (23%), however this finding was not significant.
11
A garnish or glaze was added to 30% of pâté samples following cooking on the premises,
for 64% it was not, and for 6% of samples, this information was not recorded. A higher
proportion of pâtés that had a garnish or glaze added after cooking were of unsatisfactory
microbiological quality (27%) compared to those that did not have any further ingredients
added after cooking (23%) however this finding was not significant
Pâté shelf life
Of the 209 pâté samples cooked on the premises, approximately three quarters (42%) had
an allocated shelf life of less than one week, 15% had less than 2 weeks, 10% had less
than 3 weeks, 11% had less than 4 weeks, 12%had between 4 and 8 weeks, 1% had
between 8 and 12 weeks, and 1% had a shelf life equal to or exceeding 12 weeks. For 8%
of samples, this information was not known.
There was no difference in the
microbiological quality of pâtés cooked on the premise in relation to their allocated shelf
life.
For 80% of pâté samples, the period of time remaining until the pâté’s shelf life expired
was recorded. The shelf life of 8% of pâté samples expired within 1 day of sampling,
36% expired between 1 and 10 days of sampling and 16% expired over 10 days from
sampling. For 20% of samples this information was not known. A higher proportion of
the pâté samples sampled over ten days from their expiry date were of unsatisfactory
quality (23%) compared to those sampled closer to their expiry date (1-10 days; 20%, <1
day; 18%) although this was not significant.
Storage, display and service of cold meats and pâté
The majority (92%) of cold ready to eat meat and pâté samples were stored or displayed
at or below 8ºC, 5% of samples were stored above 8ºC, and for 3% of samples, this
information was not recorded. A significantly higher proportion of cold meat and pâté
samples (38%) that were stored above 8ºC were of unsatisfactory or unacceptable
microbiological quality compared to those stored below 8ºC (24%) (p<0.0001).
12
Over half (55%) of the meat and pâté samples were covered at the time of sampling, 40%
were not and for 5% of samples, this information was not recorded. The proportion of
meat and pâté samples that were of unsatisfactory or unacceptable microbiological
quality was significantly higher where the meats and pâtés were covered at the time of
sampling (26%) compared to those that were not (22%) (p=0.002).
Over a third (34%) of cold meat and pâté samples were served using gloved or protected
hands, 22% were served with bare hands, 17% were served using a dedicated utensil, 6%
were served using shared utensils, 5% were served using the product protective
packaging and 4% were served using another method (combination of gloved or bare
hand with a dedicated or shared utensil, plastic bag or polythene wrapping). For 12% of
samples, this information was not recorded. The proportion of unsatisfactory or
unacceptable cold meat and pâté samples was lower when served using a dedicated
utensil (21%) compared to service by protected hand (26%), bare hand (25%), shared
utensil (25%), packaging (26%) and other methods (24%). This finding was significant
when comparing the use of a dedicated utensil with service by protected hand (p=0.03).
Catering and retail premises in relation to microbiological quality
Type of premises
Cold meat and pâté samples were collected from 630 catering and 1658 retail premises.
Catering premises comprised of hotels, cafes, public houses, restaurants, (including staff,
hospital and school restaurants) prison kitchens, fish and chip shops, takeaways, mobile
snack vans and sandwich shops. Retail premises comprised of supermarkets,
delicatessens, butchers shops, bakers shops and market stalls. Three-quarters (75%) of the
meat and pâté samples were collected from retail premises and 25% from catering
premises. Proportionally more unsatisfactory or unacceptable meat and pâté samples
were from catering premises (26%) than from retail premises (24%), however this
difference was not significant.
13
Significantly more samples from market stalls (43%) and delicatessens (39%) were of
unsatisfactory or unacceptable microbiological quality compared with those from other
retail premises (butchers 27%, supermarkets 13%, and other premises types 25%)
(p<0.04). Significantly more samples from cafes (39%) and other catering premises
(35%) (fish and chip shops, takeaways, mobile snack vans, prison kitchens) were of
unsatisfactory or unacceptable microbiological quality when compared to hotels (18%),
public houses (21%), and restaurants (21%) (p<0.03).
Food safety practices in premises handling open raw meat and ready-to-eat food
The results presented in this section relate to all premises unless otherwise specified. A
detailed breakdown of results relating to catering and retail sectors is provided in Table 5.
Over three-quarters (76%) of premises handled open raw meat on the premises, 22% did
not and for the remaining 2% of premises, this information was not recorded.
Significantly more catering premises (82%) handled open raw meat as well as ready to
eat foods when compared to retail premises (74%) (p<0.00001) (Table 5). The proportion
of meat and pâté samples of unsatisfactory or unacceptable microbiological quality was
significantly lower (23%) from premises that also handled open raw meat when
compared to those from premises that only handled ready-to-eat food (32%) (p<0.0001).
Physical separation was provided between raw meat and ready to eat food areas in 84%
of premises. The practice of separating raw meat and ready to eat foods was significantly
higher in retail premises (90%) compared to catering premises (70%) (p<0.00001) (Table
5). Where there was a lack of physical separation, the proportion of unsatisfactory meat
and pâté samples was significantly higher (29%) when compared to premises that did
provide this separation (22%) (p<0.002) (Figure 2).
Most premises visited did not transfer equipment between raw meat and ready-to-eat food
areas (74%). However, 22% of premises did transfer equipment between raw meat and
ready to eat food areas and this practice was significantly more common in catering
premises (43%) compared to retail premises (13%) (p<0.00001) (Table 5). There was no
14
significant difference in the proportion of unsatisfactory samples from premises that
transferred equipment (23%) from raw meat to ready-to-eat food areas and those that did
not (22%) (Figure 2).
Seventy-one per cent of premises had staff that moved between raw meat and ready-toeat food areas and this practice was significantly more common in catering premises
(82%) compared to retail premises (66%) (p<0.00001) (Table 5). In 27% of premises
visited, staff did not move between raw meat and ready to eat food areas and for 3% of
premises, this information was not recorded. Significantly more meat and pâté samples of
unsatisfactory or unacceptable microbiological quality were from premises where staff
moved between raw and ready-to-eat food areas (26%) compared with those that did not
(16%) (p<0.0001) (Figure 2).
Figure 2. Food safety practices in premises handling open raw meat and
microbiological quality of cold sliced meats and pâté samples
Food Safety Practice
Physical separation between
raw meat and RTE products
Equipment transferred from
raw meat areas to RTE food
areas
Yes
No
Staff move between raw meat
and RTE food areas
Staff change clothing between
raw meat and RTE food areas
0
5
10
15
20
25
30
35
% Unsatisfactory/Unacceptable Samples
Of the premises visited where staff moved between raw meat and ready-to-eat food areas,
staff did not change their protective clothing in 77% of premises, in 13% of premises they
did and for 9% of premises, this information was not recorded. Where staff moved
15
between raw meat and ready-to-eat food areas and did not change their protective
clothing, a significantly higher proportion of samples of unsatisfactory or unacceptable
quality (27%) were obtained compared to premises that had staff that did change their
protective clothing (16%) (p<0.0001).
Table 5. Food Safety Practices in premises handling open raw meat and ready to eat
foods
Food Safety Practice
Open raw meat handled Yes
on premises
No
Retail Premises
(%)
No. Samples
No. Samples
(%
Catering Premises
(%
Unsatisfactory/
(%)
Unsatisfactory/
Unacceptable)
Unacceptable)
1222
(74)
2275
(23)
519
(82)
838
(23)
410
(25)
761
(30)
95
(15)
149
(42)
26
(2)
35
(29)
16
(3)
20
(30)
Yes
Physical separation
between raw & ready to No
eat foods
NR
1104
(90)
2072
(21)
361
(70)
596
(22)
107
(9)
187
(33)
150
(29)
232
(25)
11
(1)
16
(31)
8
(2)
10
(40)
Yes
162
(13)
285
(25)
225
(43)
350
(21)
No
1018
(83)
1921
(22)
278
(54)
463
(25)
NR
42
(3)
69
(30)
16
(3)
25
(20)
Staff move between raw Yes
meat & ready to eat food No
areas
NR
807
(66)
1457
(27)
426
(82)
697
(22)
381
(31)
756
(14)
82
(16)
129
(29)
34
(3)
62
(18)
11
(2)
12
(0)
Staff change protective
clothing when moving
between raw meat &
ready to eat food areas
Yes
111
(14)
220
(20)
53
(12)
104
(9)
No
627
(78)
1130
(28)
327
(77)
517
(23)
NR
69
(9)
107
(32)
46
(11)
76
(37)
NR
Equipment transferred
between raw meat &
ready to eat food areas
NR- Not Recorded
Food Hygiene Inspections
Of the catering and retail premises visited, over half (52%) had an inspection rating
category of C, 7% were rated as Category A, 31% B and 3% D, 1% E and <1% as F. This
information was not recorded for 6% of premises. A significantly higher proportion of
catering premises were rated Category C or below (63%) compared to retailers (54%)
(p<0.001) (Table 6).
16
Two thirds (66%) of premises visited had consumer at risk scores of 5. Almost a quarter
(23%) had scores of 10, 2% had scores of 15 and <1% had scores of 0. For 9%, the
consumer at risk score was not recorded. The proportion of retail premises with a
consumers at risk score of 10 or above, indicative of larger businesses, (27%) was higher
than catering premises (21%). Twice as many samples obtained from premises with
small numbers of customers (29%) were of unsatisfactory or unacceptable
microbiological quality when compared to premises with intermediate (15%) or
substantial (13%) numbers of customers (p<0.005) (Table 6).
Almost half (43%) of the premises visited had a confidence in management score of 10
(some confidence), 5% had a score of 0 (high confidence), 36% had a score of 5
(moderate confidence), 7% a score of 20 (little confidence), and <1% had a score of 30
(no confidence). For 9% of premises visited, this information was not recorded. A
significantly higher proportion of catering premises (13%) had a score of 20 or above
compared to retail premises (5%) (p<0.0001) The proportion of unsatisfactory or
unacceptable samples was higher from premises where there was little or no confidence
(27%) compared to premises where there was some, moderate or high confidence in
management (24%) although this finding was not significant (Table 6).
Hazard Analysis System
Over half of the premises visited had a documented hazard analysis system in place
(63%) and a further 14% had an undocumented hazard analysis system in place.
However, 10% of premises had no hazard analysis system in place and for 12% of
premises, this information was not recorded. Retail premises were significantly more
likely to have a documented hazard analysis system in place (70%) when compared to
catering premises (46%) (p<0.00001). Caterers were significantly more likely to have an
undocumented or no hazard analysis system (43%) when compared to retail premises
(18%) (p<0.00001) The proportion of samples of unsatisfactory or unacceptable
microbiological quality was significantly higher where premises had no hazard analysis
system in place (41%) compared to premises with a documented or undocumented (23%)
hazard analysis system in place (p<0.00001) (Table 6).
17
Table 6. Details of Food Hygiene inspections in catering and retail premises
Premises Details
Retail
Premises
n=1658
Inspection Rating Category
A
115
B
543
C
807
D
65
E
21
F
7
Not Recorded
100
Consumers at Risk Score
Substantial (15)
25
Intermediate (10)
407
Few (5)
1064
Very few (0)
13
Not Recorded
149
Confidence in Management Score
High (0)
86
Moderate (5)
662
Some (10)
663
Little (20)
86
No (30)
5
Not Recorded
156
Hazard analysis
In Place and Documented
1157
In Place and Undocumented
175
Not In place
122
Not Recorded
204
Management Food Hygiene training
Received Training and attended a
1521
- Basic 6 hour course
643
- Intermediate course
470
- Advanced course
87
- Other recognised course
262
- Not Specified
59
No Training
44
Not Recorded
93
Hand washing facilities
Accessible and available for use
1572
- used
1192
- not used
107
- use not recorded
273
Not available and accessible for use 29
Not Recorded
57
No. Samples
(%
Unsatisfactory/
Unacceptable)
Catering
Premises
n= 630
No. Samples
(%
Unsatisfactory/
Unacceptable)
(7)
(33)
(49)
(4)
(1)
(0)
(6)
216
945
1565
122
41
8
174
(27)
(26)
(24)
(16)
(12)
(50)
(25)
37
160
385
8
2
4
34
(6)
(25)
(61)
(1)
(0)
(1)
(5)
62
250
612
12
3
4
64
(24)
(22)
(28)
(8)
(0)
(0)
(28)
(2)
(25)
(64)
(1)
(9)
56
813
1921
22
259
(13)
(14)
(29)
(14)
(24)
11
118
449
4
48
(2)
(19)
(71)
(1)
(8)
20
211
685
6
85
(15)
(16)
(29)
(17)
(27)
(5)
(40)
(40)
(5)
(0)
(9)
170
1225
1239
146
12
279
(14)
(21)
(28)
(34)
(33)
(23)
23
151
320
81
3
52
(4)
(24)
(51)
(13)
(0)
(8)
47
234
508
120
6
92
(9)
(23)
(28)
(26)
(17)
(30)
(70)
(11)
(7)
(12)
2184
321
220
346
(21)
(37)
(44)
(49)
287
155
116
72
(46)
(25)
(18)
(11)
472
247
184
104
(19)
(31)
(37)
(25)
(92)
(42)
(31)
(6)
(17)
(4)
(3)
(6)
2835
1221
841
164
493
116
78
158
(24)
(26)
(20)
(19)
(27)
(16)
(38)
(26)
571
386
109
41
18
17
35
24
(91)
(68)
(19)
(7)
(3)
(3)
(6)
(4)
924
594
186
94
25
25
53
30
(25)
(28)
(21)
(14)
(32)
(16)
(49)
(17)
(95)
(76)
(7)
(17)
(2)
(3)
2945
2279
194
472
46
80
(24)
(25)
(21)
(21)
(46)
(35)
588
430
49
109
17
25
(93)
(73)
(8)
(19)
(3)
(4)
945
702
82
161
28
34
(26)
(26)
(33)
(24)
(14)
(32)
18
Food Hygiene Training
The majority of premises had managers that had received some form of food hygiene
training (91%), 4% did not and for 5% of premises, this information was not recorded.
Of those managers with food hygiene training, almost half (49%) had attended a basic 6hour food hygiene course, but 28% were trained to an intermediate and 6% to an
advanced level. A further 13% had attended another recognised course (Meat Hygiene
Service, Royal Institute of Public Health, Meat and Livestock Commission, vocational
qualifications, City and Guilds, higher/ordinary certificate, and in-house training), and for
4% the type of training was not specified. A higher proportion of retail managers were
trained to intermediate or advanced level (37%) compared to managers of catering
premises (26%) (p<0.0001). A higher proportion of retail managers had attended other
recognised training courses (17%) compared to managers of catering premises (3%)
(p<0.0001) (Table 6).
Significantly more samples of unsatisfactory or unacceptable microbiological quality
were taken from premises where the manager had received no form of food hygiene
training (43%) compared to premises where the manager had received training (24%)
(p<0.0001). Significantly, the proportion of samples of unsatisfactory or unacceptable
microbiological quality decreased as the level of training received by the manager
increased. (Advanced; 17%, Intermediate; 21%, Basic; 27% (p<0.0001) (Table 6, Figure
3).
Hand washing facilities
Hand washing facilities were readily accessible and available for use in the vast majority
(94%) of premises visited, in 2% they were not and for 4% of premises, this information
was not recorded. Where hand-washing facilities were available and accessible for use,
they were used by staff, as judged by the sampling officer, in 75% of premises. In 7% of
premises they were not used and in 18% of premises, their use was not recorded (Table
6).
A higher proportion of samples of unsatisfactory or unacceptable microbiological quality
were taken from the small number of premises where hand washing facilities were not
19
available (34%) when compared to premises where these facilities were available (24%).
(Table 6).
There was no difference in the proportion of samples of unsatisfactory or unacceptable
microbiological quality taken from premises where hand washing facilities were utilised
(25%) when compared to samples taken from premises where hand washing facilities
were not used (24%) (Table 6).
Figure 3. Level of management food hygiene training and microbiological quality of
cold sliced meats and pâté samples
% Unsatisfactory/Unacceptable Samples
30
25
20
Retail Premises
15
Catering Premises
All Premises
10
5
0
Basic
Intermediate
Advanced
Level of Management Food Hygiene Training
Discussion
This study has shown that the majority of ready-to-eat cold sliced meats (74%) and pâtés
(77%) collected from catering and retail premises in the UK were of satisfactory or
acceptable microbiological quality. However, approximately a quarter of meat (26%)
and pâté (23%) samples were of unsatisfactory quality according to published
microbiological guidelines31. Unsatisfactory results were due mainly to high ACC,
Enterobacteriaceae and E. coli counts. High ACC, Enterobacteriaceae and E. coli levels
may indicate that the cooking process was inadequate, that post cooking contamination
had occurred, that the length of time and temperature control in storage or display
facilities was inadequate to prevent bacterial growth, or that a combination of these
20
factors was involved. No pâté samples were of unacceptable microbiological quality,
however, two cold meat samples were of unacceptable quality. Of these, one sample was
unacceptable due to the presence of Campylobacter jejuni and one sample was
unacceptable due to the presence of Listeria monocytogenes at a level in excess of 100
cfu/g. It was beyond the scope of this study to determine where in the food chain this
contamination may have taken place and in the absence of detailed consumption data, it
is not possible to estimate the risk of exposure to Campylobacter or L. monocytogenes
infection from consuming these or similar products. Meat products that are adequately
cooked, stored and protected from post cooking contamination present little risk of
Campylobacter infection, however, this study has shown that ready-to-eat meats available
for consumption can become contaminated with pathogens either during production,
storage or preparation for sale. However, it remains that epidemiological studies14 and
surveillance systems13 have hypothesised an association between cold cooked meats and
Campylobacter infection highlighting the need for further work in this area.
This study shows a continued decline in the proportion of pâté samples contaminated
with L. monocytogenes since 1989 in the UK (1989; 10%, 1990; 4%, 1994; 3% and 2002;
2%)20,33. However, the proportion of fish and seafood based pâtés with low levels of L.
monocytogenes present still remains comparatively higher than meat, poultry and
vegetarian pâtés. In contrast, there has been little change in the proportion of cold sliced
ready-to-eat meat samples of unsatisfactory or unacceptable microbiological quality from
catering premises since 199821 (1998; 26%, 2002; 28%). Unsatisfactory or unacceptable
microbiological quality of meats in both the present and 1998 studies were associated
with meat cooked or sliced elsewhere, meat supplied from butchers or wholesalers, and
meat cooked and kept longer than one day. Other significant risk factors associated with
the microbiological quality of cold sliced meats and pâtés in this study were storage or
display at a temperature above 8°C, the use of shared meat slicing equipment, the use of
meat slicing equipment cleaned only at the end of the trading session, a lack of physical
separation between raw meat and ready to eat foods and the movement of staff between
areas used for raw meats and ready-to-eat foods. The risk of cross-contamination from
open raw meat or other sources could be reduced by improving the separation of open
21
raw meat and ready to eat foods, reducing or eliminating staff movement between raw
meat areas and ready to eat food areas, using routinely cleaned equipment to slice meats
and by serving ready to eat meat products with a utensil dedicated to this purpose.
Two findings were unexpected. Firstly, samples that were covered at the time of
sampling were more likely to be of unsatisfactory microbiological quality (26%)
compared with those that were not covered (22%). This result highlights an area for
further work to determine whether in some circumstances, the use of certain food
coverings may encourage the growth of certain bacteria. Secondly, samples taken from
premises handling open raw meat and ready-to-eat foods were less likely to be of
unsatisfactory microbiological quality (23%) than those taken from premises selling
ready to eat foods only (32%). This result may indicate an increased awareness of the
hazards associated with raw meats resulting in greater vigilance and higher standards of
cleanliness in the premises in question. It is possible that this finding is influenced by
other factors and should not be used to minimise the importance of key practices to
prevent cross contamination within premises that handle both open raw meat and ready to
eat foods.
The UK Food Standards Agency’s Hygiene Campaign was launched in April 2002 and
forms part of a raft of measures to reduce foodborne illness by 20% by 200611. Part of the
campaign is specifically aimed at the catering sector. This study has shown that the
proportion of unsatisfactory or unacceptable samples was slightly higher from catering
premises (26%) when compared to retail premises (24%). Catering premises were more
often associated with food safety practices that are, or are reasonably expected to be,
associated with poor microbiological quality. For example, when compared to retail
premises, catering premises were significantly more likely to handle open raw meat, less
likely to provide physical separation between raw meat and cooked foods and
significantly more likely to allow staff and equipment to be transferred between areas
used for raw meat and ready to eat food. Significantly, catering premises visited were
more likely to be smaller premises where there was less confidence in the management,
22
had no hazard analysis system in place, and had lower numbers of managers trained in
food hygiene.
Management food hygiene training and the presence of hazard analysis systems in food
premises, has been shown to make a significant contribution to an improvement in the
microbiological quality of ready to eat foods34. This study has shown that managers in
retail premises were more likely to have been trained in food hygiene to an intermediate
or advanced level compared to managers in catering premises, who were more likely to
be trained to a basic level. Gillespie et al.21 showed that significantly fewer sliced meat
samples of unsatisfactory or unacceptable microbiological quality were from premises
where the manager had received advanced food hygiene training (14%) compared to
those premises where the manager had received intermediate (23%), basic (26%) or no
(33%) food hygiene training. The present study has also shown that the proportion of
sliced meat and pâté samples of unsatisfactory or unacceptable microbiological quality, in
both catering and retail premises, significantly decreased as the level of management
training increased suggesting that progressive training of management can make a
significant contribution to food safety.
The implementation of HACCP or similar food safety plans in food premises provides a
pragmatic framework for good hygienic practice. Current EU proposals to consolidate
food hygiene directives currently envisage the application of food safety management
procedures based upon HACCP principles, including documentation and verification, to
all sectors of the food chain, with the exception of primary production35. In this study,
samples taken from premises with a documented hazard analysis system were
significantly less likely to be of unsatisfactory or unacceptable quality than from premises
without any form of hazard analysis system. The implementation of HACCP or similar
food safety systems in catering and retail premises, combined with adequate training and
the application of basic principles of food hygiene, could make a significant contribution
to ensuring the satisfactory microbiological quality of ready to eat foods.
23
Acknowledgements
The authors would like to thank all the staff in the Environmental Health Departments
throughout the UK who collected samples for this study, all the staff in both PHLS and
non-PHLS laboratories who performed microbiological examination. Thanks are also
extended to LEP and FSML (CPHL) for typing isolates, to David Lock at LACORS for
coordinating the participation of Environmental Health Officers and advice from the
LACORS Food Examination Focus Group, to the PHLS Group FWE Coordinators
Forum for their comments, in particular Melody Greenwood and Heather Aird, for their
advice in preparing the sampling protocol, and to Lilian Hucklesby, Phil Evans and
Nicholas Kephalas for entering the data.
24
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27
Annex 1
Table I. Participating PHLS Groups, Public Health Laboratories and number of
meat and pâté samples
PHLS Group
East
London and South East
Midlands
North West
North
South West
Trent
Wales
Public Health Laboratory
Chelmsford
Norwich
Ashford
Brighton
London FWEL
Reading
WEMS
Birmingham
Coventry
Shrewsbury
Stoke
Chester
Preston
Carlisle
Hull
Leeds
Middlesbrough
Newcastle
Bristol
Exeter
Gloucester
Hereford
Plymouth
Truro
Leicester
Lincoln
Sheffield
Bangor
Cardiff
Carmarthen
Rhyl
Total
28
Meat
Samples
92
76
103
184
312
83
101
60
135
130
47
119
83
48
71
39
60
115
110
71
43
35
25
73
112
162
109
25
47
63
32
Pâté
Samples
38
40
31
71
91
51
58
25
63
24
12
51
75
15
43
18
16
67
26
39
27
17
18
32
23
36
33
16
15
32
10
Total
Samples
130
116
134
255
403
134
159
85
198
154
59
170
158
63
114
57
76
182
136
110
70
52
43
105
135
198
142
41
62
95
42
2765
1113
3878
Table II. Participating Non PHLS Laboratories and number of meat and pâté
samples.
Meat
Samples
8
57
9
20
22
6
7
129
Non Public Health Laboratory
Aberdeen City Council Public
Belfast City Hospital
Dundee Scientific Services
Edinburgh Analytical & Scientific
Glasgow Scientific Services
Kings Lynn & West Norfolk
Royal Alexandra, Paisley
Total
29
Pâté
Samples
7
30
3
13
12
5
1
71
Total
15
87
12
33
34
11
8
200
Table III. Participating Food Safety Liaison Groups, number of premises visited
and number of cold meat and pâté samples taken.
Food Liaison Group
Berkshire
Buckinghamshire
Cambridgeshire
Cheshire
Chester
Cornwall
Cumbria
Derbyshire
Devon
Dorset
Durham
East Sussex
Essex
Gloucestershire
Greater London NW Sector (LFCC*)
Greater London SE Sector (LFCC*)
Greater London SW Sector (LFCC*)
Greater London NE Sector (LFCC*)
Greater Manchester
Hampshire & Isle Of Wight
Hereford & Worcestershire
Hertfordshire & Bedfordshire
Humberside
Kent
Lancashire
Leicestershire
Lincolnshire
Merseyside
Norfolk
North Yorkshire
Northamptonshire
Northumberland
Norwich
Nottinghamshire
Oxfordshire
Shropshire
Somerset
South Yorkshire
Staffordshire
Suffolk
Surrey
Tees Valley
Tyne & Wear
Warwickshire
West Midlands
West Of England
West Sussex
West Yorkshire
Wiltshire
Northern Ireland Food Group
Scottish Food Liaison Group
Wales
Total
*LFCC – London Food Coordinating Committee
Premises
22
32
13
65
10
61
43
50
58
44
26
64
42
39
48
31
37
21
39
64
50
62
40
85
49
49
70
31
5
38
63
23
36
47
26
29
31
16
55
39
48
24
58
61
63
40
46
9
39
52
52
143
2288
30
Meat Samples Pâté Samples Total Samples
35
11
46
33
17
50
13
6
19
56
25
81
12
4
16
73
32
105
53
20
73
81
33
114
68
40
108
44
20
64
36
5
41
74
27
101
53
22
75
42
26
68
63
20
83
36
14
50
55
9
64
42
3
45
37
33
70
58
40
98
59
27
86
80
33
113
62
37
99
103
31
134
41
37
78
112
23
135
88
13
101
39
16
55
7
2
9
36
28
64
77
37
114
29
14
43
48
24
72
68
17
85
27
19
46
28
15
43
29
17
46
34
6
40
56
17
73
38
19
57
67
25
92
32
7
39
67
49
116
63
30
93
124
24
148
64
7
71
59
28
87
23
4
27
53
25
78
57
30
87
66
36
102
194
80
274
2894
1184
4078