REPORT OF THE GREATER MANCHESTER/LANCASHIRE/PHLS
LIAISON GROUP SURVEY ON THE MICROBIOLOGICAL
EXAMINATION OF MEAT/SALAD SANDWICHES FROM SMALL RETAIL
PREMISES
K Williamson, G Allen, F J Bolton, PHLS North West FESL – Preston PHL
Date of report 6/3/00
Survey Code No. 904009
A wide range of retail outlets serve sandwiches in a `takeaway’ form. In order to
achieve a satisfactory level of microbiological quality, there are certain basics that
must be controlled in the production and retail of sandwiches. The food ingredients
must be of good quality and stored correctly, and storage temperatures and hygiene
practices must be satisfactory from production to retail.
Environmental health officers from the Greater Manchester and Lancashire Food
Liaison Groups considered sandwiches produced and/or retailed in supermarkets to be
generally of a satisfactory quality. This assumption was derived from the results of
routine samples submitted for examination, and inspection of larger retail premises.
However, sandwiches were not often routinely sampled from small corner shops,
kiosks and garage forecourt shops, etc. The risk for a basic hygiene breakdown was
thought to be more likely in such premises especially when the sandwich ingredients
included salad, and ambient temperatures were high during summer months.
Hence the purpose of this survey was to establish the microbiological quality of
meat/salad sandwiches from the point of sale in small retail shops and to assess in
particular the storage conditions and type of retail packaging. Additionally, the
survey aimed to determine the extent of sandwich container labelling with a health
mark for approved premises.
Materials and Methods
Sample collection
This survey was carried out as part of the Greater Manchester FLG/Lancashire
FOG/Preston PHL sampling programme during July – December 1999. Samples
consisted of white or brown sliced bread, baps or barmcake, prepacked sandwiches
containing a cooked meat filling and salad, including lettuce, tomato, cucumber,
onion, etc. The samples were collected from retail shops by local authority sampling
officers according to a standard protocol (Appendix 1). Information relating to the
premises and product including a between pack temperature was obtained and
recorded on a standard questionnaire (Appendix 1).
Microbiological examination
A total of 383 sandwich samples were submitted and examined from 25/26 authorities
in Greater Manchester and Lancashire as detailed in Appendix 1.
KW/KLM (182000)
1
Samples were examined for aerobic colony count (ACC), Enterobacteriaceae, E. coli,
Staphylococcus aureus, Listeria spp and Salmonella spp using UKAS accredited
PHLS-NW FESL food methods.
Results
Microbiological results
Table 1
Microbiological results of meat/salad sandwich samples (n = 383).
Detected
Not
detected
<10,<20
10-<102
102-<103
103-<104
104-<105
105-<106
106-<107
107
52
358
370
376
1
37
15
11
6
11
78
7
2
1
41
101
2
0
0
73
65
1
0
0
89
31
0
0
0
80
12
0
0
0
88
7
0
0
0
o
ACC/g 30 C 48h
Enterobacteriaceae/g
E.coli/g
S.aureus/g
Listeria spp/g
Salmonella/25g
0
383
The results were assessed using category 4 of the PHLS microbiological guidelines
for some ready to eat foods (1) and the Preston PHL proposed guidelines for
Enterobacteriaceae (2). This combination of guidelines are referred to as RTEFG in
this study.
Table 2
Relevant parameters in category 4 of the RTEFG1+2
Microbiological quality (cfu/g) unless stated
Satisfactory
Borderline
limit of
acceptability
Unsatisfactory
Unacceptable
potentially
hazardous
<106
106 - <107
107
-
Enterobacteriaceae
<500
500 – 104
104
-
E. coli
<20
20 - <100
100 - <104
104
Staphylococcus aureus
<20
20 - <100
100 - <104
104
Not detected
in 25g
Present in
25g - <200/g
200 - <104
104
Not detected
in 25g
-
-
Present in 25g
Aerobic colony
(ACC) (30°C/48h)
Listeria spp
Salmonella spp
KW/KLM (182000)
count
2
Table 3
Category 4
Microbiological quality of meat/salad sandwiches using Category 4
of the RTEFG1+2
Satisfactory (%)
Borderline (%)
Unsatisfactory (%)
Unacceptability (%)
75 (20)
153 (40)
154 (40)
1(<1)
Table 3 demonstrates that based on category 4 of the PHLS RTEFG (1) and (2) 40%
of samples were of unsatisfactory microbiological quality.
The Enterobacteriaceae (30%) and aerobic colony count (ACC) (23%) parameters
were most often associated with unsatisfactory results. E. coli was detected at >100/g
in 10 (2.7%) of the samples and only 2 (0.5%) produced Staphylococcus aureus
counts of >100/g. Listeria spp were not detected at an unsatisfactory level, and
Salmonella spp were not detected in any of the samples.
Discussion
`Ready to use’ vegetable salads retain much of their indigenous microflora after
minimal processing. Minimally processed salads include lettuce simply stripped of its
outer leaves or trimmed, peeled, sliced/shredded and washed and/or disinfected
salads. This type of ready to use salad is often incorporated into sandwiches, and has
been reported to harbour large and diverse populations of microorganisms with counts
of 105-107 cfu/g. (3). Minimal processing damages salad tissues resulting in leakage
of cellular fluids containing nutrients and intracellular enzymes (4) creating a
favourable environment for microbial growth.
However, minimally processed salads have a good track record in terms of food safety
due to good hygiene, harvesting and production practices. Enterobacteriaceae such as
Enterobacter and Erwinia spp are major components of the microflora of some salad
materials. Some salad materials in particular carry a high microbial load often due to
the problems in washing, because of the physical nature of the salad and difficulty in
penetrating the salad structure.
Therefore, high levels of Enterobacteriaceae are probable in unprepared and
minimally processed vegetable salads, and some microbiologists recommend that
Enterobacteriaceae and aerobic colony counts should not be used as an indication of
microbiological quality on the examination of salad materials (5). Levels of E. coli
are considered to be a better food safety indicator for salads, which have been linked
to the presence of pathogens such as Salmonella (6).
Hence it may be recommended to interpret sandwiches incorporating salad using
category 5 of the PHLS RTEFG (1) which omits the ACC and Enterobacteriaceae
parameters.
If category 5 is applied to the results of the 383 samples examined in this study, 371
(97%) would be interpreted as acceptable (89% satisfactory and 8% borderline) and
only 12 (3%) as unsatisfactory.
KW/KLM (182000)
3
However the use of ACC and Enterobacteriaceae as hygiene indicators in this study
demonstrated that temperature either during preparation, transport or storage had a
significant effect on their counts.
The percentage of unsatisfactory samples using the ACC parameter (>107/g),
Enterobacteriaceae (>104/g) and the RTEFG was recorded for each month (July –
December 1999). Figure 1 demonstrates the seasonality trend with increased
unsatisfactory results in the warmer months of July, August and September.
Figure 1
Seasonality related to unsatisfactory microbiological quality of
meat/salad sandwiches
70.0
60.0
% UNSATISFACTORY
50.0
40.0
ACC only (>1.0x10+E7cfu/g)
Enterobacteriaceae only (>1.0x10+E4cfu/g)
RTEFG WITH Enterobacteriaceae
30.0
20.0
10.0
0.0
Jul-99
Aug-99
Sep-99
Oct-99
Nov-99
Dec-99
MONTH SAMPLED
The ACC and Enterobacteriaceae levels may therefore be of use for hygiene quality
assessment, but of limited or of no food safety value related to likely presence of
pathogens.
Questionnaire results
Questionnaire results were analysed in relation to microbiological quality using
category 4 of the PHLS RTEFG unless otherwise stated. A copy of the questionnaire
is available in Appendix 1.
KW/KLM (182000)
4
Q.1
Premise details (n = 379)
Local
branded
grocer
149 (39%)
Garage
shop
Kiosk
Newsagent
140 (37%)
9 (2%)
81 (21%)
Sandwiches purchased from newsagent shops produced the greatest percentage of
unsatisfactory results (52%), whereas 63/149 grocers (44%), 46/140 garage shops
(33%) and 4/9 kiosks (44%) sold unsatisfactory quality sandwiches.
The ten unsatisfactory results due to E. coli counts of >100/g were not predominantly
obtained from any type of premises.
Q2. Was the sandwich made on the premises? (n=380)
Yes
48 (13%)
No
332 (87%)
Of the 48 sandwiches made on the premises 17 (37%) produced unsatisfactory results.
Of the 332 sandwiches purchased from premises using an outside supplier, 138 (41%)
produced unsatisfactory results.
Q3. Where was the purchased sandwich displayed/stored? (n=380)
Refrigerated
source
353 (93%)
Ambient
display
27 (7%)
The majority (353 (93%)) of sandwiches were displayed/stored refrigerated and 143
(41%) produced unsatisfactory results. A similar percentage (41%) of unsatisfactory
results was obtained from the 27 sandwiches stored at room temperature.
However 60 (18%) of the refrigerated sources (n=340) produced in between sandwich
pack temperatures of >8°C.
Thirty-two sandwiches (53%) from these 60
unsatisfactory refrigerated sources produced unsatisfactory results, whereas 106 of the
280 (38%) refrigerated sources at 8°C gave unsatisfactory results. The percentage of
refrigerated sources producing in between sandwich pack temperatures of >8°C each
month from July – December 1999 is demonstrated in Figure 2. The seasonality trend
demonstrates cooling problems associated with refrigerated displays during summer
months.
KW/KLM (182000)
5
Figure 2
Seasonality related to refrigerator temperatures greater than 8°C
30
% REFRIGERATOR TEMPERATURES >8C
25
20
15
10
5
0
Jul-99
Aug-99
Sep-99
Oct-99
Nov-99
Dec-99
MONTH
Q4. What was the in-between pack temperature of sandwiches in the display?
(n=367)
0 - 5oC
129 (35%)
5oC – 8oC
156 (43%)
>8oC
82 (22%)
N.B. These results include both refrigerated and ambient displays/storage. The
duration of storage prior to recording in between pack temperatures is not known.
Unsatisfactory results were obtained from 107/285 (38%) sandwiches with in between
pack temperatures of 8°C compared to 44/82 (54%) at >8°C.
Similarly, unsatisfactory results due to E. coli counts of >100/g were more prevalent
(5%) when sandwiches were >8°C as opposed to 2.1% at 8°C.
Q5. Is there a display/storage temperature monitoring system? (n=381)
Yes
298 (78%)
No
83 (22%)
Process information only, results not related to microbiological quality.
KW/KLM (182000)
6
Q6. Are the display/storage temperature monitoring records available for
inspection? (n=298)
Yes
204 (68%)
No
87 (29%)
Not stated
7
Process information only, results not related to microbiological quality.
Q7. How long has the purchased sandwich been stored/displayed at the
premises? (n=383)
1st day
228 (60%)
2nd day
124 (32%)
3rd day
7 (2%)
>3 days
2 (1%)
Not known
22 (5%)
Unsatisfactory results were obtained from 88/228 (39%) of the first day
storage/display sandwiches and 43% of second day storage. There were insufficient
numbers of third and >3 days storage sandwiches for analysis.
Q8. Is the purchased sandwich beyond its use by date? (n=368)
Yes
7 (2%)
No
361 (98%)
There were an insufficient number of sandwiches purchased beyond its use by date
for analysis.
Q9. Is the sandwich container labelled with a health mark for approved
premises? (n=371)
Yes
134 (36%)
No
237 (64%)
The majority of sandwich containers were not labelled with a health mark for
approved premises and 113/237 (48%) of sandwiches in these containers produced
unsatisfactory results, as opposed to 38/134 (28%) when labelled.
Further analysis demonstrates the usage of labelled containers in the four types of
premises.
Grocers
shop
Garage
shop
Kiosk
Newsagent
Number of premises
149
140
9
81
Number of sandwich
containers labelled
66
53
4
11
44%
38%
44%
14%
% labelled
KW/KLM (182000)
7
Q10. Type of retail packaging (n=373)
Plastic
mould with
snap on lid
101 (27%)
Plastic
mould with
heat sealed
lid
180 (48%)
‘Cling’ film
Cellophane
bag
12 (3%)
80 (22%)
The plastic mould with heat sealed lid was the most common type of container used
for sandwiches purchased in this survey (48%); they also produced the least number
of unsatisfactory results 57/180 (32%). The other three types of containers produced
higher and similar levels of unsatisfactory results (50%).
Conclusions
(1)
Based on category 4 of the PHLS microbiological guidelines for some ready to
eat foods (1) and the Preston PHL proposed guidelines for Enterobacteriaceae,
40% of samples examined in this survey are unsatisfactory. However
Salmonella spp were not detected in any of the samples. Only 2.7% of
samples contained E. coli, 0.5% Staphylococcus aureus and no samples
contained Listeria spp at unsatisfactory levels.
(2)
The majority of sandwich containers were not labelled with a health mark for
approved premises. Sandwiches in these containers produced significantly
more unsatisfactory results (48%) than those in labelled containers (28%).
(3)
Newsagent shops as well as producing the majority of unsatisfactory results
(50%) were also the premises most often not retailing sandwiches in
containers labelled with a health mark for approved premises.
(4)
The plastic mould container with a heat sealed lid prevents physical and
microbiological contamination and is tamper-evident in comparison with the
other containers. Sandwiches examined from this type of container produced
the least number of unsatisfactory results.
(5)
The aerobic colony count and Enterobacteriaceae acted as good hygiene
quality indicators in this study. However the interpretation levels may need
revision due to naturally high counts in some salad materials. A seasonality
trend was demonstrated in relation to these indicator organism counts, the
greater counts occurring in the summer months when display refrigeration
temperatures were proven to be more frequently sub optimum (<8°C).
(6)
It is proposed that the use of the aerobic colony count and Enterobacteriaceae
counts in the interpretation of sandwiches containing salads is reviewed by the
members of the PHLS Food and Environmental Co-ordinators Forum.
(7)
If category 5 of the guidelines are used for interpretation, only 3% of the total
samples examined are unsatisfactory.
KW/KLM (182000)
8
(8)
It is proposed that meat/salad sandwiches should be examined for: E. coli,
Staphylococcus aureus, Listeria monocytogenes and Salmonella spp.
Interpretation of the results of these microbiological parameters would give a
good indication of the potential hazards in the salad sandwich manufacturing
operation.
(9)
Although the majority of sandwiches (93%) were stored/displayed
refrigerated, 18% produced in between pack temperatures of >8°C. Overall
38% of sandwiches with in between pack temperatures of <8°C produced
unsatisfactory results compared with 54% when >8°C. Hence it is strongly
recommended that refrigerated conditions are used from production to retail,
and in particular refrigerated sources should be capable of maintaining <8°C
during the summer months.
KW/KLM (182000)
9
References
(1)
PHLS 1996. Microbiological Guidelines for some Ready-to-Eat Foods
sampled at the Point of Sale – an Expert opinion from the PHLS. PHLS
Microbiological Digest 13: 41-43.
(2)
Suggested Guidelines for Enterobactericeae Counts in Food Samples. G.
Allen, F J Bolton, K Williamson, Preston PHL. PHLS Annual Scientific
Meeting, September 1998, Poster presentation.
(3)
Francis, G A, Thomas, C, Obeirne D, 1999. The microbiological Safety of
Minimally Processed Vegetables. Int J of Food Science and Technology 34:
1-22.
(4)
G Heard, 2000. Microbial Safety of Ready-to-Eat Salads and Minimally
Processed Vegetables and Fruits. Food Science and Technology Today 14,
15-21.
(5)
Nguyen-the et al. 1994. The Microbiology of Minimally Processed Fresh
Fruits and Vegetables. Crit. Rev. Food Sci. Nutr. 34: 371-401.
Acknowledgements
The authors would like to thank Anne McEvoy (Wigan MBC) and Elaine Buckley,
(Wyre EHD) for their assistance in producing the questionnaire and protocol and for
their support and advice.
KW/KLM (182000)
10
APPENDIX 1
KW/KLM (182000)
(A)
Survey participants
(B)
Survey protocol
(C)
Survey questionnaire
11
APPENDIX A
Tested July 1999 to January 2000.
A total of 383 samples were tested from 25 authorities.
Authority
Barrow
Blackpool
Burnley
Chorley
Fylde
Hyndburn
Lancaster
Pendle
Preston
Ribble Valley
Rossendale
South Lakes
South Ribble
West Lancs
Wyre
Bolton
Bury
Manchester
Oldham
Rochdale
Salford
Stockport
Tameside
Trafford
Wigan
TOTAL
KW/KLM (182000)
Number of
samples
14
13
20
13
18
11
18
14
19
17
11
19
15
19
20
21
11
17
13
18
18
13
14
6
11
383
12
APPENDIX B
KW/KLM (182000)
13
KW/KLM (182000)
14
KW/KLM (182000)
15
APPENDIX C
KW/KLM (182000)
16