Report of the Cheshire, Cumbria, Greater Manchester, Lancashire and
Merseyside Food Liaison Groups and FEMS North West
Survey of the Microbiological Examination of Fresh Cream Cakes
K Williamson, G Allen, F J Bolton
FEMS North West
Date of Report: 15 September 2008
Survey No: 804001
Introduction
A wide variety of fresh cream cakes are consumed in the UK and outbreaks of food
poisoning associated with cream cakes have been recorded worldwide, many due to
Salmonella. Several local authorities have expressed concern relating to the
frequency of high aerobic colony counts and unsatisfactory levels of indicator
organisms in routine samples of cakes containing dairy cream. Poor hygiene practices
have also been observed during inspection of premises retailing cream cakes in
relation to temperature control, improper use of equipment and handling. Local
authorities have also questioned whether the four hour temperature regulations
exemption rule which is applicable to cream cakes could affect the microbiological
quality, and whether category 3 of the PHLS ready to eat food guidelines (1) is
suitable for assessing the microbiological quality of cakes filled with fresh cream.
Hence the purpose of this survey was to determine and compare the microbiological
quality of cream cakes sampled from refrigerated and ambient display units in a wide
range of retail and catering premises. Additionally a questionnaire relating to
premises, preparation and display conditions was analysed so that risk factors
associated with microbiological quality and safety could be identified.
Materials and Methods
Sample Collection
This survey was carried out as part of the Cheshire, Merseyside, Cumbria, Greater
Manchester and Lancashire Food Liaison Groups sampling programme in coordination with FEMS-NW laboratories during March – June 2008. Additionally
Flintshire participated from the North Wales Food Liaison Group.
Samples of any type of cake containing dairy cream were purchased/sampled from a
wide range of catering and retail premises. The cakes were served/collected from
either refrigerated or ambient display in their usual retail packaging. The samples
were placed in food grade plastic bags and transported to the laboratory at 0-8C.
Information relating to premises, preparation and display unit was recorded onto a
modified FEMS-NW request form (Appendix 1).
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Sample Examination
A total of 571 cream cake samples were submitted by 42 North West authorities to
their FEMS-NW testing laboratory (Appendix 2). Samples were examined using
UKAS accredited test methods for aerobic colony count/g (ACC),
Enterobacteriaceae/g, E. coli/g, Staphylococcus aureus/g, Bacillus cereus/g, Bacillus
spp/g, L. monocytogenes/g, Listeria spp/g and for the detection of Salmonella/25g and
Listeria/25g. Isolates of L. monocytogenes were referred to HPA, Colindale for
epidemiological typing.
Microbiology Results
Table 1.
Microbiology Results (n = 571)
Detected
Not
detected
<10, <20
ACC/g
Enterobacteriaceae/g
292
557
564
E.coli/g
S.aureus/g
Bacillus cereus/g
Bacillus spp(not B.cereus)/g
L.monocytogenes/g/in 25g
Listeria spp (total)/g/in 25g
Salmonella in 25g
13
26
0
Table 2.
558
545
571
568
568
10,20-<102
102-<103
103-<104
104-<105
105-<106
106-<107
107-<108
>108
26
119
7
4
555
532
3
3
73
84
7
2
14
30
0
0
132
50
0
0
1
5
0
0
78
21
0
1
0
2
0
0
102
5
0
0
1
1
0
0
67
0
0
0
0
0
0
0
89
0
0
0
0
0
0
0
4
0
0
0
0
1
0
0
Relevant parameters in Category 3 of PHLS guidelines (1)
Microbiological quality (cfu/g) unless stated
Satisfactory
<105
Aerobic colony count
Acceptable
Unsatisfactory
105 - <106
4
106
Unacceptable/Potentially
Hazardous
N/A
104
N/A
104
Enterobacteriaceae
<100
100 - 10
E. coli
<20
20 - <100
S. aureus
<20
20 - <100
100
100 - <104
Bacillus cereus and other
pathogenic Bacillus spp
<103
103 - <104
104 - <105
105
Listeria monocytogenes
<20
20 - <100
N/A
Listeria spp (total)
<20
20 - <100
100
100
N/A
Salmonella
N/A
Not detected/25g
Table 3.
Microbiological results using
microbiological guidelines (1)
Satisfactory
Acceptable
271 (47.5%)
131 (23%)
Table 4.
Detected/25g
Unsatisfactory
166 (29%)
Listeria spp. identification (n = 26)
Identification
L. monocytogenes
L. innocua
L. seeligeri
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Category
No. of isolates
13
8
5
Page 2 of 9
3
of
the
PHLS
Unacceptable/potentially
hazardous
3 (0.5%)
Table 5.
Listeria monocytogenes serotype (n = 13)
Serotype
1/2a
4
1/2c
1/2b
Not typable
No. of isolates
6
2
2
1
2
Tables 1 and 3 summarise the microbiology results and demonstrate that 30% of
samples were of unsatisfactory quality based on Category 3 of the PHLS guidelines
(1). The ACC of >106 in 160/571 (28%) was the main cause of unsatisfactory results.
Other unsatisfactory results were due to high levels of: Enterobacteriaceae 26/571
(4.5%), E. coli 7/571 (1.2%), Bacillus spp 4/571 (0.7%) and Staphylococcus aureus
3/571 (0.5%). Three samples were of unacceptable and potentially hazardous quality
due to high levels of pathogenic Bacillus spp, (B. subtilis >105/g, B. cereus >105/g,
and one sample with B. subtilis >105/g, and Staphylococcus aureus at >104/g).
No samples were unsatisfactory due to Listeria spp and Salmonella was not detected
in any of the samples. Listeria spp was detected at low levels in 26 (4.6%) samples
with L. monocytogenes detected in 13 (2.3%) (10 at <10/g and 3 at 10-100/g). The
most common serotype was 1/2a (6 isolates), as demonstrated in Table 5.
Questionnaire results
The questionnaire results were related to the microbiological quality in the following
tables.
Table 6.
Q.1
Microbiological quality related to type of premises (n = 571)
Baker (n=370)
Café (n=54)
Corner shop (n=6)
Delicatessen (28)
Local branded grocer (n=13)
Market stall (n=10)
Mobile vendor (n=1)
Public house (n=3)
Restaurant (n=10)
Supermarket (n=68)
Not stated (n=8)
TOTAL (n=571)
Satisfactory
Acceptable
Unsatisfactory
156 (42%)
29 (54%)
2
8 (28.5%)
7 (54%)
1 (10%)
1
2
5 (50%)
55 (81%)
5
99 (27%)
7 (13%)
1
7 (25%)
2 (15%)
4 (40%)
0
0
0
9 (13%)
2
113 (30.5%)
17 (31.5%)
3
13 (46.5%)
4 (31%)
5 (50%)
0
1
5 (50%)
4 (6%)
1
Unacceptable/potentially
hazardous
2 (0.5%)
1 (1.5%)
0
0
0
0
0
0
0
0
0
271 (47.5%)
131 (23%)
166 (29%)
3 (0.5%)
Market stalls and restaurants produced the highest proportion of unsatisfactory results (both 50%)
although sample numbers were low (n = 10). In comparison 94% of the samples from
supermarkets were acceptable/satisfactory.
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Table 7.
Q2.
Was the cream cake refrigerated? (n = 554)
Yes
No
537
17
Information not
supplied
17
The majority of businesses (97%) served the cake from a refrigerated display.
Table 8.
Q.3.
Microbiological quality – temperature of the display cabinet/area
(n = 542)
Refrigerated and displayed at
0-8oC (n=457)
Refrigerated and displayed at
>8oC (n=74)
Not refrigerated and displayed
at >8oC (n=11)
Satisfactory
Acceptable
Unsatisfactory
220 (48%)
107 (23.5%)
128 (28%)
Unacceptable/potentially
hazardous
2 (0.5%)
32 (43%)
16 (22%)
25 (34%)
1 (1%)
5 (46%)
2 (18%)
4 (36%)
0
86% of the refrigerated display units were operating between 0-8C. An increase in
unsatisfactory results was demonstated with an increase in display temperature.
Table 9.
Q.4.
If not refrigerated, how long had the product been on display? (n = 17)
Less than 4 hours
12
Greater than 4 hours
0
Information not supplied
5
From the information supplied no samples had been displayed/stored at ambient temperature for
>4 hours.
Table 10. Q.5.
Microbiological quality – was the cream cake prepared on the premises?
(n = 539)
Yes (n=210)
No (329)
Satisfactory
Acceptable
Unsatisfactory
90 (43%)
160 (49%)
53 (25%)
71 (21.5%)
65 (31%)
97 (29.5%)
Unacceptable/potentially
hazardous
2 (1%)
1 (<1%)
68% of cream cakes prepared on the premises were satisfactory/acceptable and 70.5% when prepared
offsite.
Table 11. Q.6.
Microbiology quality – how was the cream applied to the cream cake?
(n = 209)
Dispenser (n=48)
Piped manually (n=146)
Utensil (n=15)
Satisfactory
Acceptable
Unsatisfactory
23 (48%)
58 (40%)
8 (53%)
8 (23.5%)
43 (29.5%)
2 (13%)
17 (28%)
43 (29.5%)
5 (33%)
Unacceptable/potenti
ally hazardous
0
2 (1%)
0
71.5% of cream cakes produced using a dispenser were satisfactory/acceptable, 69.5% when
piped manually and 68.5% when utensils used. Sample numbers were too low to draw
conclusions. Both of the unacceptable/potentially hazardous results were obtained from the
manual piping method.
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Discussion
The results of this study indicate that 30% of the samples were of unsatisfactory
(29%) or unacceptable microbiological quality (0.5%) according to category 3 of the
PHLS guidelines (1). The ACC was the parameter most often associated with
unsatisfactory results however interpretation of the high ACC’s was limited in this
study due to not identifying the predominant organism. Although a high ACC does
not constitute a risk to health, it may sometimes indicate a general lack of hygiene.
The frequency of the high ACC results is of concern. Category 3 allows an ACC of
up to 106/g before being unsatisfactory and is supported as a valid and good indicator
level because 94% of cream cakes from supermarkets were <106/g. If supermarkets
can achieve this level, it has to be questioned why other premises cannot. For example
only 70% of bakers were able to produce cream cakes with ACC’S <106/g. If
category 2 had been used, 85% of supermarkets and only 50% of bakers would have
produced satisfactory/acceptable cream cakes indicating that category 2 may be too
stringent.
One authority reported that high ACC’s were observed when the cream cakes were
made offsite and transported, however this study does not support this view (Table
10).
Unsatisfactory Enterobacteriaceae results were obtained from 4.5% of samples with
the faecal indicator E. coli in 1.2% and Staphylococcus aureus in only 0.5%.
Unsatisfactory results were often followed up by repeat sampling including a cream
sample. However there is no cream category in the PHLS guidelines and no ACC
parameter for cream in EC 2073 for samples from producers. This causes difficulty in
interpretation of ACC’s and Enterobacteriaceae from cream at retail.
EC 2073 food process criteria may be used to interpret Enterobacteriaceae counts in
cream samples from the primary producer (<5/g = satisfactory) but again ACC’s
would be difficult to interpret because of the lack of an ACC parameter. Hence
although the ACC is a good hygiene indicator in cream cakes, there is a need to be
able to interpret ACC and other indicators such as E. coli, Staphylococcus aureus and
Bacillus spp in the bulk cream used to fill the cakes. The ACC and other indicator
results for the bulk cream can only be used comparatively with the final cream cake
product. The presence of Enterobacteriaceae, E. coli and Staphylococcus aureus in
cream are indicators of post pasteurisation contamination and in cream cakes may also
be derived from subsequent poor environmental and equipment cleaning or poor
handling practices.
Bacillus cereus and other Bacillus spp are common in milk and its endospores are able
to survive pasteurisation. Some strains are also pschrotrophic and capable of growth
in refrigerated cream. Although Bacillus food poisoning associated with cream is not
frequently reported, three cream cake samples in this study contained unacceptable/
potentially hazardous levels of Bacillus spp (Table 1) and were of concern. The three
unacceptable results were further investigated by the local authorities. There was no
link established between the samples but all reported possible hygiene failures related
to the handling of the bulk cream. In particular one authority reported that the
cleaning of the Carpegiani cream dispenser was only carried out on the day following
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Page 5 of 9
use. Although residual cream was maintained cooled in the refrigerated unit of the
Carpegiani machine overnight, the cream in the exit piping and nozzles was at room
temperature allowing bacterial growth. Subsequent cleaning was probably not
sufficient to remove the high levels of Bacillus spp. Action – machine, piping and
nozzles are now cleaned daily – problem resolved. It was also reported by one of the
authorities that residual cream was refrigerated overnight and used again in further
batches of cream cakes. Action – residual cream is now discarded at the end of each
day of use – problem resolved.
High moisture products such as cream cakes are likely to present food safety concerns
as they will support the growth of a wide range of bacteria. There are a number of
inherent factors and practices in cream cake production that increase the potential for
cross contamination. These include potential contaminated areas, frequent handling,
potential cross contamination from raw products such as eggs and potential cross
contamination through the re-use of equipment such as piping bags and contaminated
nozzles, etc. Further problems may also relate to temperature control because this
study has also highlighted that 74/537 (14%) of refrigerated units were operating at
>8.0C.
In the past, cream filled confectionery were a common cause of food poisoning but
the situation has improved with the use of refrigerated display counters. Although
cream cakes sampled from ambient displays in this study were only at room
temperature for less than 4 hours (as allowed by temperature regulation exemption
rule), the microbiological quality was still worse than those from refrigerated
displays. Hence, potential pathogens such as Staphylococcus with a minimum growth
temperature of about 10C would multiply. Good catering/retail practice advice
would therefore be to store cream cakes at 0-8C from process to retail.
The control of temperature is essential in restricting the growth of bacteria thus
minimising the risk of food poisoning. For high risk foods like cream and cream
cakes, keeping them chilled is probably the single most important control in ensuring
their safety.
However even with good temperature control 2 samples in this study were potentially
hazardous highlighting the need to monitor all risk factors carefully.
Conclusion




It is of concern that based on category 3 of the PHLS guidelines (1), 30% of
samples examined in this study were unsatisfactory, predominantly caused by
high ACC’s.
The majority (94%) of samples collected from supermarkets were of satisfactory
microbiological quality, indicating the need for careful risk assessments and
hygiene inspections at other premises producing the higher proportion of
unsatisfactory results (Table 6).
Category 3 of the PHLS guidelines (1) is considered a suitable category for the
interpretation of the microbiological quality of cream cakes and highlighting
potential hygiene or cream supply problems.
It is of concern that 14% of refrigerated display units were operating at >8.0C.
KW/KLM (27/08)
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
The 4 hour temperature regulation exemption rule applicable for cream cakes is
not be be encouraged, due to evidence that these samples produced more
unsatisfactory results (Table 8).
Future work

Survey of the bulk cream used to fill cream cakes in order to establish if the poor
final product quality is due to processing and handling or the cream supply and to
identify the predominant organisms responsible for high ACC’s.
References
(1)
Guidelines for microbiological quality of some ready to eat foods sampled at
point of sale, PHLS, ACFDP, Communicable Disease and Public Health. Sept
2000, Vol .3, No.3: 163-167.
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Appendix 1 – Request Form
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Page 8 of 9
Appendix 2 - Participants
Authority
Allerdale
Carlisle
Copeland
Eden
CUMBRIA TOTAL
Chester
Congleton
Crewe & Nantwich
Ellesmere Port & Neston
Halton
Macclesfield
Vale Royal
Warrington
CHESHIRE TOTAL
Bolton
Bury
Manchester
Oldham
Rochdale
Salford
Stockport
Tameside
Trafford
Wigan
GREATER MANCHESTER TOTAL
Barrow
Blackburn
Blackpool
Burnley
Chorley
Fylde
Hyndburn
Lancaster
Pendle
Preston
Ribble Valley
Rossendale
South Lakes
South Ribble
West Lancs
Wyre
LANCASHIRE TOTAL
Knowsley
Liverpool
St Helens
Sefton
Wirral
MERSEYSIDE TOTAL
Flintshire
Wrexham
NORTH WALES TOTAL
Total for Cumbria, Cheshire, Greater
Manchester, Lancashire, Merseyside,
North Wales
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Number of samples examined
9
12
8
10
39
13
6
11
9
18
11
10
2
80
12
12
0
15
10
12
16
20
18
19
134
10
11
14
0
20
14
18
16
8
12
16
11
19
4
25
20
218
8
4
20
45
6
83
17
0
17
Page 9 of 9
571