LACOTS/ PHLS Co-ordinated Food Liaison Group Studies:
A Study of Cleaning Standards and Practices in Food Premises
1
SK Sagoo, 1CL Little, 2CJ Griffith, 1RT Mitchell.
1, PHLS Environmental Surveillance Unit, 61 Colindale Avenue, London NW9 5EQ.
2, Food Safety Research Group, University of Wales Institute, Colchester Avenue, Cardiff CF23
9XR
On behalf of the Local Authorities Co-ordinated Body on Food and
Trading Standards and the Public Health Laboratory Service
Summary
Between 18 September and 17 November 2000 a study of cleaning standards and practices in UK
food premises was undertaken. The intention was to determine the microbiological status of surfaces
used in the preparation of ready to eat foods, and to assess cleaning standards and practices in food
premises. A total of 6,533 environmental samples were examined from 1502 catering or retail
premises; 2,033 from chopping/cutting boards, 2,009 from work top surfaces, 1359 from food
containers, and 1,132 cleaning cloths. Cleaning cloths (disposable and reuseable) were more heavily
contaminated with bacteria (Aerobic Colony Count (ACC), Enterobacteriaceae, E. coli, and Staph.
aureus) compared to the surfaces sampled. Campylobacter spp. and Salmonella spp. were detected in
two (0.2%) and one (0.1%) of the cleaning cloths, respectively. Surfaces that were visually dirty, wet,
last cleaned over 24 hours ago, and boards that were scored or damaged were found to have higher
levels of bacteria.
A hazard analysis system was in place in the majority (70%) of food premises visited, and
documented in almost three-quarters (74%) of these. Most managers (89%) had received some form
of food hygiene training. Documented cleaning schedules and cleaning records were only present in
approximately half (55% and 44%, respectively) of the premises. Sixty-one percent of premises had
physically separate areas for raw and ready-to-eat food. Most did not have separate implements for
cleaning raw and ready-to-eat food areas (67%), or stored cleaning equipment for high risk areas
away from those used in low risk areas (70%). Deficiencies in the correct use of cleaning products,
such as the minimum contact time for disinfectants, were identified.
Surface samples
(chopping/cutting boards, worktops, and food containers) and cleaning cloths with ACC levels in
excess of 103 cfu/cm2, swab or ml were associated with premises that did not have management food
hygiene training, hazard analysis, cleaning schedules or cleaning records in place, and with Local
Authority Inspectors' Confidence in Management scores. The results are discussed in relation to food
hygiene training and recommendations for improving cleaning standards are provided.
1
Introduction
Food premises are any premises or areas in premises in which food is prepared, served or stored. The
Food Safety (General Food Hygiene) Regulations 19951 implements the European Community's
Directive on Food Hygiene (93/43/EEC)2. Food premises must apply the principles of hazard analysis
to their own businesses, and also must be kept clean and maintained in good repair and condition1.
Food hygiene training and instruction for all staff handling food is also a legal requirement 1. The UK
Catering and Retail Industry Guides3,4 advise food premises of how to comply with their legal
obligations, including effective cleaning, and to ensure food safety. Cross-contamination has been
identified as an important contributory factor in 39% of foodborne outbreaks in England and Wales 5,
highlighting the importance of training food handlers in good hygiene and cleaning practices.
Raw foods are known to be associated with high levels of microorganisms and the soiling of
equipment and surfaces is unavoidable during the preparation of products for display and sale. The
soiling of cloths, hands, and utensils in food production environments is well documented6,7 and their
potential to cross-contaminate surfaces used for cooked products is well recognised 8,9. Provided that
the equipment and environment are hygienically designed (i.e. with no crevices, dead spaces etc.), an
effective cleaning and disinfection programme is the major method of control of the surface route of
contamination. If the cleaning and disinfection programme in a food premises is not effective, nor
specifies the frequency of cleaning, microorganisms and product residues will remain at
concentrations that may affect the quality and safety of the food product 10. A critical report on the
butcher shop at the centre of the worst outbreak of Escherichia coli O157 food poisoning in the UK
identified a failure to devise or enforce separate cleaning schedules and equipment for the shop as one
of many defects in their system11.
Few standards or guidelines have been published on what is an acceptable level of microorganism
contamination on surfaces. The Swedish Code of Statute SLVSFS 1998 (No.10) provides that less
than (<) 1 cfu/cm2 is an acceptable level for surfaces considered clean, 1-3 cfu/cm2 is acceptable with
notification, and over (>) 3 cfu/cm2 is an unacceptable level for clean surfaces. The EC Decision
laying down rules for the regular checks on the general hygiene carried out by operators of meat
establishments (2001/471/EC)12 provides that cleaned and disinfected surfaces sampled using the agar
contact plate or swab technique should have an acceptable range of 0-10 cfu/cm2 for Total Viable
counts (TVC) and 0-1 cfu/cm2 for Enterobacteriaceae. TVC and Enterobacteriaceae counts above
these ranges are unacceptable and should be clarified by consultation with the cleaning staff. As a
guideline, the US Public Health Service recommends that adequately cleaned and disinfected food
service equipment have not more than 1000 total number of viable microorganisms per square
decimetre sampled13, which is equivalent to not more than 10 cfu/cm2. Microbial target values of
<2.5 cfu/cm2 have been suggested and have been found to be attainable for a range of surfaces that
have been cleaned and disinfected14,15. For recently cleaned surfaces that have been brought into use
in food premises not more than 80 cfu/cm2 is recommended by Herbert et al.16 as a satisfactory level,
80-1000 cfu/cm2 is borderline, and over 1000 cfu/cm2 is an unsatisfactory level.
Therefore,
achievable levels of viable microorganisms immediately after cleaning and disinfection of surfaces
within food premises are ≤10 cfu/cm2, whereas once cleaned surfaces or equipment are brought into
operational use it is more realistic to achieve a target level of <80 cfu/cm2.
Although the cleanliness of various food manufacturing environments has been assessed10, 17-19 there is
relatively little published information on cleaning regimes or standards of cleanliness in food
premises. Food premises throughout the UK were therefore surveyed in this study to determine the
extent of what cleaning and disinfection methods are used in a range of different food premises. In
addition, up to five environmental samples were collected from each premise. Environmental swabs
were taken from a range of surfaces within the premises that were used to prepare ready-to-eat foods.
Cleaning cloths used in ready-to-eat food areas were also included in the study. Swabs were
examined for the presence of Staphylococcus aureus; Escherichia coli and Enterobacteriaceae were
enumerated and Aerobic colony count (ACC) determined to obtain an indication of hygiene and levels
2
of contamination. Cleaning cloths were also examined for these parameters and in addition, were
examined for the presence of E. coli O157, Campylobacter spp., Salmonella spp., and Listeria spp.,
including L. monocytogenes to obtain an indication of hygiene and levels of contamination.
Materials and Methods
Sample Collection
This study took place between 18 September and 17 November 2000 and involved local authorities
and laboratories (PHLS and non-PHLS) in England, Wales, Scotland, and Northern Ireland. A
standardised protocol and reporting system was used. Environmental samples were collected from a
representative cross section of hotels, restaurants, public houses, cafés, residential care homes, staff
restaurants, delicatessens, bakers, butchers, sandwich bars, mobile vendors, and market stalls by staff
from local Environmental Health Departments in accordance with the Food Safety Act 1990, Code of
Practice No. 720. Environmental areas sampled included cutting/chopping boards for ready-to-eat
foods, worktop surfaces adjacent to or in proximity of the cutting/chopping board where open readyto-eat foods are handled, the inside of an empty and clean ready-to-eat food container, and cleaning
cloths used for wiping surfaces in ready-to-eat food areas of the premises. Areas cleaned or
disinfected by the proprietor/manager of the premises immediately before sampling were specifically
excluded from this study. Cleaning cloths soaking in sanitiser/disinfectant or hot water immediately
before sampling were also specifically excluded from this study. Surfaces were sampled by the
surface sponge swab technique using sterile 50cm2 foam sampling sponges (with 5ml neutralising
buffer) in polythene envelopes and sterile templates (10cm x 10cm). For the inside of clean food
containers an area similar to the size of the template was sampled. All environmental sampling
materials were supplied by Technical Services Consultants (TSC) Ltd. Whole cleaning-cloths were
placed into a sterile plastic bag for transport to the laboratory.
Information on the food premises was obtained by observation and enquiry and recorded on a
standard proforma. This included information on the premises and practices, with special regard to
food safety legislation1, 21, and cleaning and disinfection methods used in food premises.
Processing of Environmental Samples
A maximum of four sponge swabs and one cleaning cloth were collected from each premise for
microbiological examination. Sponge swabs and cloths were placed into sterile stomacher bags
containing MRD (100 ml and 150 ml, respectively) and the contents thoroughly mixed to remove
bacteria from the swabs and cloths. Sample eluents were serially diluted in MRD and appropriate
dilutions were used to enumerate ACC, Enterobacteriaceae, E. coli and Staph. aureus (cloths only).
Aliquots (25 ml) of the primary suspension were used for detection of Staph. aureus (both swabs and
cloths), and Salmonella spp. Campylobacter spp., E. coli O157, and Listeria spp. including L.
monocytogenes in cloth samples.
Sample examination
The ACC was determined in accordance with PHLS Standard Microbiological Methods for Food
Products F1022 and F1123. Enterobacteriaceae, E. coli, Staph. aureus, L. monocytogenes and other
Listeria spp., Campylobacter spp., Salmonella spp., and E. coli O157 were enumerated or detected in
accordance with PHLS Standard Microbiological Methods24-30. Staph. aureus was detected by sample
(25ml) enrichment in Buffered Peptone Water (225ml) at 37°C for 24 hours, with subculture to BairdParker agar. Plates were incubated at 37°C for 48 hours. Identification was confirmed using
appropriate biochemical tests26. Isolates of Campylobacter spp. and Salmonella spp. were sent to the
Laboratory of Enteric Pathogens (LEP), Central Public Health Laboratory (CPHL) for further
characterisation.
Statistical Analysis
Chi squared (χ2) analysis was performed using Epi Info version 6.04d31.
3
Results
A total of 6,533 environmental samples from 1502 food premises were examined by 42 laboratories
(32 Public Health Laboratories (PHLS) from all 8 PHLS Groups; 10 non-PHLS) in the UK. Fifty-one
Local Authority Food Liaison Groups participated in this study (Annex 1) and samples were
submitted by 365 Local Authorities. A further 56 samples did not fit the criteria described in the study
protocol and were not included in the analysis.
Among the 1502 food premises visited, samples were collected from restaurants (263; 18%), public
houses (180; 12%), hotels (168; 11%) cafés (162; 11%) sandwich bars (148; 10%), residential care
homes (135; 9%), butchers (98; 7%), delicatessens (80; 5%), bakers (68; 4%), staff restaurants (48;
3%), mobile vendors (23; 2%), and market stalls (2; <1%). Other premises (schools, hospitals,
supermarkets, fast food outlets) accounted for 118 (8%) premises, and for nine (<1%), the type of
premises was not recorded.
Microorganisms isolated from Food Premises
A total of 6,533 environmental samples were examined from ready-to-eat areas within the premises
visited; 2,033 swabs from chopping board surfaces, 2,009 from work top surfaces, 1,359 from clean
empty containers, and 1,132 cleaning cloths.
Chopping/Cutting Boards surfaces
ACC (25%; 498/2033 swab samples) at or greater than 103 cfu/cm2, Enterobacteriaceae (4%; 80
samples) at or greater than 102 cfu/cm2, E. coli (0.9%; 19 samples) at or greater than 20 cfu/cm2, and
Staph. aureus (0.3%; detected in 7 samples) were present on chopping/cutting board surfaces (Table
1).
Work top surfaces
ACC (8%; 150/2009 swab samples) at or greater than 103 cfu/cm2, Enterobacteriaceae (0.9%; 18
samples) at or greater than 102 cfu/cm2, E. coli (0.6%; 13 samples) at or greater than 20 cfu/cm2, and
Staph. aureus (0.3%; detected in 5 samples) were present on work top surfaces (Table 1).
Food Container surfaces
ACC (15%; 208/1359 swab samples) at or greater than 103 cfu/swab, Enterobacteriaceae (3%; 43
samples) at or greater than 102 cfu/swab, E. coli (5%; 66 samples) at or greater than 20 cfu/swab, and
Staph. aureus (0.2%; detected in 3 samples) were present on food container surfaces (Table 1).
Food container surfaces had over five times as much E. coli (faecal indicator organism) present (5%)
compared to other surfaces sampled (chopping/cutting boards (0.9%), work tops (0.6%)) (Table 1).
Cleaning cloths
Campylobacter spp. and Salmonella spp. were detected in two (0.2%; 2/1073) and one (0.1%; 1/1072)
cleaning cloth samples, respectively. E. coli O157 was not detected in any of the cleaning cloths
examined. L. monocytogenes and other Listeria spp. were detected in 5% (57/1070) and 8%
(82/1068) of cleaning cloth samples, respectively. Cleaning cloths were the most heavily
contaminated with ACC (84%; 898/1074 samples) at or greater than 103 cfu/ml cloth eluent,
Enterobacteriaceae (66%; 708/1076 samples) at or greater than 102 cfu/ml cloth eluent, E. coli (30%;
319/1073 samples) at or greater than 20 cfu/ml cloth eluent, and Staph. aureus (2%; detected in
26/1078 samples, and at or greater than 20 cfu/ml cloth eluent in a further 32 samples (3%), indicating
a reservoir of bacteria and an increased risk of cross contamination (Table 1).
Two-thirds (67%; 754/1132) of the cleaning cloths collected were re-useable cloths, and a third (33%)
were disposable cloths. Although not significant, re-useable cloths were slightly more likely to be
4
heavily contaminated with ACC (81%, ≥103 cfu/ml eluent) Enterobacteriaceae (63%; ≥102 cfu/ml
eluent), E. coli (30%; ≥20 cfu/ml eluent), and Staph. aureus (6% ≥20 cfu/ml eluent) than disposable
cloths (77%, 61%, 28%, 4%, respectively). Listeria spp. (including L. monocytogenes) were present
in 12% of both disposable and re-useable cloths. Campylobacter spp. was detected in both disposable
(1; C. jejuni) and re-useable (1) cloths, and Salmonella spp. (S. Ridge) in a re-useable cloth (1).
Table 1 Microbiological results of 6,533 environmental samples from ready-to-eat areas within
food premises
ND*
D‡
<10/
<20†
Chopping/Cutting Boards surfaces (n=2033)
Aerobic colony count
774
Enterobacteriaceae
1898
E. coli
2014
Staph. aureus
2026
7
Work top surfaces (n=2009)
Aerobic colony count
Enterobacteriaceae
E. coli
Staph. aureus
2004
Food Container (n =1359)
Aerobic colony count
Enterobacteriaceae
E. coli
Staph. aureus
1356
1060
1974
1996
10/<20 <102
102 <103
103 <104
104 <105
105 <106
106 <107
107
307
55
12
454
29
6
232
23
1
151
10
77
6
34
3
4
9
361
17
9
438
8
3
100
7
1
33
2
15
1
2
358
24
24
128
9
2
50
7
18
1
8
1
4
1
103
148
95
11
143
170
65
4
158
140
39
2
211
118
22
170
89
15
216
43
3
192
60
40
3
Cleaning Cloth (n= 1132)
Aerobic colony count
41
32
Enterobacteriaceae
270
98
E. coli
2
752
80
Staph. aureus
718
26
302
15
Listeria spp
986
82
L. monocytogenes
1013
57
Campylobacter spp
1071
2
E. coli O157
1069
0
Salmonella spp
1071
1
*ND; Not detected; ‡; detected, §NE, Not examined (full set
due to insufficient sample collected)
†, cfu/cm2, swab or ml
Total
examined
2033
2033
2033
2033
2009
2009
2009
2009
5
601
1256
1293
NE§
1359
1359
1359
1359
58
1074
56
1076
59
1073
54
1078
64
1068
62
1070
59
1073
61
1069
58
1072
of microbiological parameters were not performed on sample
Assessment of cleanliness using total number of microorganisms present
For recently cleaned surfaces in food premises a guideline of over 1000 total number of
microorganisms (ACC) present per cm2 is an unsatisfactory level as recommended by Herbert et al.16.
This guideline was used as a benchmark for analysing and categorising the results from this study.
Cutting/Chopping board surface
 Thirty-nine percent (583/1502) of premises had cutting/chopping boards with surfaces that had an
ACC level of 103 cfu/cm2 or more.
 A quarter (25%) of cutting/chopping boards sampled exceeded the unsatisfactory level of ACC
present (≥103 cfu/cm2) (Table 1), including 22% of boards that were reported as being last cleaned
within the last hour (Table 2).
 Most cutting/chopping boards sampled were plastic (87%). There was no significant difference
between the type of board used and the level of ACC present (≥103 cfu/cm2) (Table 2).
5
Table 2 Details of cutting/chopping boards used within food premises (n=2033)
Cutting/Chopping board
Number (%)
ACC >103 cfu/cm2 (%)
Type
Plastic
Wood
Other (glass, ceramic, steel)
Not recorded
1770
92
135
36
(87%)
(5%)
(7%)
(2%)
444
18
20
10
(22%)
(20%)
(15%)
(28%)
Use
Ready-to-eat food only
Both ready-to-eat and raw food
Not recorded
1671
283
77
(82%)
(14%)
(4%)
346
138
76
(21%)
(49%)
(99%)
Surface Appearance
Visibly clean
Dirty
Not recorded
1417
511
105
(70%)
(25%)
(5%)
289
188
18
(20%)
(37%)
(17%)
533
941*
586*
29
82
(26%)
(46%)
(29%)
(1%)
(4%)
86
226*
236*
14
15
(16%)
(24%)
(40%)
(48%)
(18%)
Presence of Moisture
Wet
Dry
Not recorded
277
1531
225
(14%)
(75%)
(11%)
87
323
126
(31%)
(21%)
(56%)
Board Last Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
436
428
118
76
593
201
181
(21%)
(21%)
(6%)
(4%)
(29%)
(10%)
(9%)
96
88
33
16
130
92
46
(22%)
(21%)
(28%)
(21%)
(22%)
(46%)
(25%)
Board to be Next Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
783
456
200
114
175
38
267
(39%)
(22%)
(10%)
(6%)
(9%)
(2%)
(13%)
174
109
45
23
13
8
127
(22%)
(24%)
(23%)
(20%)
(7%)
(21%)
(48%)
Surface Condition
Good
Scored
Scratched
Chipped
Scuffed
Not recorded
* Cutting/chopping boards that were identified as both scored and scratched (142 samples)
 The majority of boards (82%) sampled were only used for ready-to-eat foods. Over twice as
many boards used for both raw and ready-to-eat foods had an ACC level of 103 cfu/cm2 or more
(49%) compared with those only used for ready-to-eat foods (21%) (P<0.00001) (Table 2).
 Most boards (70%) were visibly clean as judged by the sampling officer. Significantly more
boards that were dirty had an ACC level of 103 cfu/cm2 or more (37%) compared to clean boards
(20%) (P<0.0001) (Table 2).
 Approximately half (46%) of the boards sampled were scored. Significantly fewer boards with a
good surface condition had an ACC level of 103 cfu/cm2 or more (16%) compared with other
surface conditions (24% - 48%) (P<0.00001) (Table 2).
6
 Three-quarters (75%) of boards were dry when sampled. Significantly more boards that were wet
had an ACC level of 103 cfu/cm2 or more (31%) compared with boards that were dry (21%)
(P<0.001) (Table 2).
 Over half (52%) of boards were reported as last cleaned within the previous 10 hours. However,
10% of boards were last cleaned over 24 hours ago (Table 2). Significantly more boards last
cleaned over 24 hours ago had an ACC level in excess of 103 cfu/cm2 (46%) compared to those
boards cleaned within 24 hours (21% - 28%) (P<0.00001) (Table 2). Over a third (39%) of the
boards were reported as to be next cleaned within one hour. There was no significant difference
between when the board would be cleaned next and the level of ACC present (≥10 3 cfu/cm2)
(Table 2).
Work top surface
 Thirteen percent (197/1502) of premises had work top surfaces that had an ACC level of 103
cfu/cm2 or more.
 Over two thirds (68%) of the work top surfaces sampled were used for only ready-to-eat foods.
Significantly more work top surfaces used for only ready-to-eat foods had an ACC level of 103
cfu/cm2 or more (10%) compared with those surfaces used for both raw and ready-to-eat foods
(3%) (P<0.0001) (Table 3).
 Most surfaces (80%) were visibly clean as judged by the sampling officer. More surfaces that
were dirty were likely to have an ACC level of 103 cfu/cm2 or more (10%) compared to clean
surfaces (7%) however, this was not significant (Table 3).
 Almost three-quarters (74%) of the surfaces sampled were in good condition. There was no
significant difference between the condition of the surface and the level of ACC present (≥10 3
cfu/cm2) (Table 3).
 The majority (80%) of surfaces were dry when sampled. Almost twice as many surfaces that
were wet had an ACC level of 103 cfu/cm2 or more (14%) compared with surfaces that were dry
(8%) (P<0.01) (Table 3).
 Approximately two-thirds (65%) of work top surfaces were reported as last cleaned within the
previous 10 hours. However, 6% of surfaces were last cleaned over 24 hours ago (Table 3).
There was no significant difference between when the surface was cleaned last and the level of
ACC present (≥103 cfu/cm2) (Table 3). Most (41%) of the surfaces were reported as to be next
cleaned within one hour. There was no significant difference between when the surface would be
cleaned next and the level of ACC present (≥103 cfu/cm2) (Table 3).
7
Table 3 Details of work top surfaces used within food premises (n=2009)
Work top surface
Number (%)
ACC >103 cfu/cm2 (%)
Use
Ready-to-eat food only
Both ready-to-eat and raw food
Not recorded
1367
551
91
(68%)
(27%)
(5%)
131
19
(10%)
(3%)
Surface Appearance
Visibly clean
Dirty
Not recorded
1674
278
57
(80%)
(14%)
(3%)
121
29
(7%)
(10%)
Surface Condition
Good
Scored
Scratched
Chipped
Scuffed
1480
158
237
22
28
(74%)
(8%)
(12%)
(1%)
(1%)
126
24
22
3
2
(9%)
(16%)
(9%)
(14%)
(7%)
Presence of Moisture
Wet
Dry
Not recorded
160
1598
251
(8%)
(80%)
(12%)
22
128
(14%)
(8%)
Surface Last Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
651
486
104
75
403
117
173
(32%)
(24%)
(5%)
(4%)
(20%)
(6%)
(9%)
69
38
11
9
27
15
4
(11%)
(8%)
(11%)
(12%)
(7%)
(13%)
(2%)
Surface to be Next Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
826
497
174
76
55
47
334
(41%)
(25%)
(9%)
(4%)
(3%)
(3%)
(17%)
78
44
14
7
8
3
12
(10%)
(9%)
(8%)
(9%)
(15%)
(6%)
(4%)
Food Container surface
 Twenty-three percent (346/1502) of premises had food containers that had an ACC level of 103
cfu/swab or more.
 Almost two-thirds (64%) of containers sampled were plastic. Almost twice as many plastic
containers (17%) had an ACC level of 103 cfu/swab or more compared to ceramic containers (9%)
(P<0.05) (Table 4).
 Most containers (90%) were visibly clean as judged by the sampling officer. Significantly more
containers that were dirty had an ACC level of 103 cfu/swab or more (25%) compared to clean
containers (14%) (P<0.01) (Table 4).
 Over three-quarters (77%) of containers were dry when sampled. Containers that were wet were
more likely to have an ACC level of 103 cfu/swab or more (18%) compared with those that were
dry (14%) however, this was not significant (Table 4).
 Over a third (35%) of containers were reported as last cleaned within the previous 10 hours.
However, 12% of containers were last cleaned over 24 hours ago, and for a further 26% of
containers the time of when last cleaned was reported as not known (Table 4). There was no
significant difference between when the container was last cleaned and the level of ACC present
8
(≥103 cfu/swab) (Table 4). A fifth (20%) of the containers were reported as to be next cleaned
within one hour. There was no significant difference between when the container would be
cleaned next and the level of ACC present (≥103 cfu/swab) (Table 4).
Table 4 Details of food containers used within food premises (n=1359)
Food Container
Number (%)
ACC >103 cfu/swab (%)
Type
Plastic
Ceramic
Other (Disposable foil containers, steel)
Not recorded
871
141
299
48
(64%)
(10%)
(22%)
(4%)
145
12
38
13
(17%)
(9%)
(13%)
(27%)
Surface Appearance
Visibly clean
Dirty
Not recorded
1182
108
87
(90%)
(5%)
(6%)
168
27
13
(14%)
(25%)
(15%)
Presence of Moisture
Wet
Dry
Not recorded
229
1043
87
(17%)
(77%)
(6%)
41
149
18
(18%)
(14%)
(21%)
Container Last Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
197
158
71
58
361
163
351
(15%)
(12%)
(5%)
(3%)
(27%)
(12%)
(26%)
23
17
11
9
56
31
89
(12%)
(11%)
(15%)
(16%)
(16%)
(19%)
(25%)
Container to be Next Cleaned
<1hr
1 - <3hrs
3 - <6hrs
6 - <10hrs
10 - <24hrs
> 24hrs
Not known
266
150
99
71
111
53
609
(20%)
(11%)
(7%)
(5%)
(8%)
(4%)
(45%)
50
22
12
11
13
6
94
(19%)
(15%)
(12%)
(15%)
(12%)
(11%)
(15%)
Cleaning Cloths
 Forty-two percent (638/1502) and 22% (323/1502) of premises where re-useable cloths and
disposable cloths, respectively that were sampled had an ACC level of 103 cfu/ml or more.
 Over two-thirds (67%) of cleaning cloths sampled were re-useable cloths (Table 5).
 Most (42%) disposable cleaning cloths were reported to be replaced within 12 hours. However,
13% of disposable cleaning cloths were replaced within 48 hours. Significantly more disposable
cloths replaced between 24 to 48 hours had ACC level in excess of 103 cfu/ml (94%) compared to
those replaced within 12 hours (70%) (P<0.001) (Table 5).
 Whilst 70% of re-useable cleaning cloths were reported as cleaned at least every 24 hours, and of
these 39% were cleaned at least every 10 hours, 15% of re-useable cleaning cloths were cleaned
less frequently than 24 hours (Table 5). There was no significant difference between the
frequency the re-useable cloth was cleaned last and the level of ACC present (≥103 cfu/ml) (Table
5).
 Most re-useable cloths were reported to be cleaned using a washing machine (42%) or sanitiser
rinse (33%). There was no significant difference between the type of method used to clean the reuseable cloth and the level of ACC present (≥103 cfu/ml) (Table 5).
9
Table 5 Details of cleaning cloths used within food premises (n=1132)
Cleaning cloth
Number (%)
ACC >103 cfu/ml (%)
Frequency disposable cloths replaced (n=378)
<12 hrs
160
12 -<24hrs
119
24 -<48hrs
49
Not known
50
(42%)
(31%)
(13%)
(13%)
112
99
46
34
(70%)
(83%)
(94%)
(68%)
Frequency re-useable cloths cleaned (n=754)
< 1hr
118
1 - <3hrs
81
3 - <6hrs
61
6 - <10hrs
33
10 -<24hrs
232
>24hrs
112
Not known
117
(16%)
(11%)
(8%)
(4%)
(31%)
(15%)
(15%)
90
60
54
31
184
91
97
(76%)
(74%)
(84%)
(93%)
(79%)
(81%)
(83%)
251
89
319
69
(33%)
(12%)
(42%)
(9%)
209
72
242
63
(83%)
(81%)
(76%)
(91%)
26
(3%)
21
(81%)
Method to clean re-useable cloth (n=754)
sanitiser-rinse
Boiling
Washing machine
Others (External cleaners/ laundry, soapy
water , dry cleaning)
Not known
Food Premises in relation to separation of Raw and Ready-To-Eat Food Areas
 In 61% of food premises visited, raw and ready-to-eat food areas were physically separated
(Table 6).
 A small proportion (17%) of premises had staff that remained within either the raw or ready-toeat food area (Table 6)
 In approximately half (48%) of the food premises equipment was not transferred from raw to
ready-to-eat food areas. However, equipment, such as chopping boards, were common to both
raw and ready-to-eat food areas in nearly two-thirds (65%) of premises (Table 6).
Table 6 Proportion of food premises with separate facilities for raw and ready-to-eat food areas
and equipment (n=1502)
Premises
Present
Not Present
Not recorded
Physical separation of raw from ready-to-eat food
areas
Staff moving from raw from ready-to-eat food areas
Equipment transferred from raw to ready-to-eat
food areas
Equipment (e.g. chopping boards, telephones,
fridge handles etc.) common to raw and ready-toeat food areas
913 (61%)
547 (36%)
42 (3%)
1214 (81%)
727 (48%)
252 (17%)
722 (48%)
36 (2%)
53 (4%)
973 (65%)
441 (29%)
88 (6%)
Food Premises in relation to cleaning methods and practices
 Most premises did not use external contractors to carry out either routine (89%) and/or deep
cleaning (60%) (Table 7).
10
 Cleaning schedules were used in only approximately two-thirds (65%) of premises. Where
cleaning schedules were used most (89%) covered all areas that needed to be cleaned and were
documented (85%) and monitored by a manager or supervisor (87%) (Table 7).
 Significantly more samples (surfaces of chopping/cutting boards, worktops, and food
containers, and cleaning cloths) with ACC levels in excess of 103 cfu/cm2, swab or ml
were from premises where there was no cleaning schedules in place (37% 642/1719
samples) compared to those where cleaning schedules were in place (31% 537/1719)
(P<0.00001).
 Most cleaning schedules used specified the task to be done (92%), the frequency (88%), the use of
a disinfectant and/or sanitiser (70%), how surfaces are to be cleaned (60%), who carries out the
task (54%), and the removal of visible debris as the first stage of cleaning (52%) (Table 7).
 Less than half of the cleaning schedules used specified the method required for dilution of stock
chemicals (46%), the method (including details of strip down and reassemble of the equipment)
(43%), and the standard expected (41%) (Table 7).
 Over two-thirds (69%) of cleaning schedules used did not specify the contact time for the
disinfectant or sanitiser specified, and most cleaning schedules used (71%) did not specify drying
(Table 10). Where drying was specified (25%; 247), air drying was the main method specified
(41%; 102/247) (Fig. 1).
Fig. 1 Drying method specified in cleaning schedules used in food
premises (n=247)
Other (Tea towel)
13%
Not recorded
2%
Used cloth
5%
Air drying
41%
Paper towel
26%
Disposable cloth
13%
 Effectiveness of cleaning was assessed in most (84%) of food premises and predominantly by
visual assessment (97%) (Table 7 & Fig. 2). Less than half of the premises kept cleaning records
(44%).
 Significantly more samples (surfaces of chopping/cutting boards, worktops, and food
containers, and cleaning cloths) with ACC levels in excess of 103 cfu/cm2, swab or ml were
from premises where there were no cleaning records kept (37% 1021/2774 samples)
compared to those where cleaning records were kept (28% 660/2330) (P<0.00001).
11
Table 7 Details of cleaning methods and schedules used by food premises
Premises
Yes
No
Not recorded
Cleaning methods (n=1502)
Routine cleaning carried out by external contractors
Deep cleaning carried out by external contractors
Cleaning schedules used
120 (8%)
415 (28%)
975 (65%)
1341 (89%)
895 (60%)
475 (32%)
41 (3%)
192 (12%)
52 (3%)
Cleaning schedules (n=975)
Cover all areas that need to be cleaned
Documented
Monitored by manager/supervisor
863 (89%)
830 (85%)
853 (87%)
83
(8%)
120 (12%)
77 (8%)
29 (3%)
25 (3%)
45 (5%)
901
862
583
502
686
451
417
(92%)
(88%)
(60%)
(52%)
(70%)
(46%)
(43%)
29
65
338
412
235
444
479
(3%)
(7%)
(35%)
(42%)
(24%)
(46%)
(49%)
45
48
54
61
54
80
79
524
398
244
247
(54%)
(41%)
(25%)
(25%)
390
506
674
690
(40%)
(52%)
(69%)
(71%)
61 (6%)
71 (7%)
57 (6%)
38 (4%)
1259
662
949
310
397
(84%)
(44%)
(63%)
(21%)
(26%)
219 (15%)
774 (52%)
524 (35%)
1134 (75%)
1048 (70%)
24
66
29
58
57
(1%)
(4%)
(2%)
(4%)
(4%)
439 (29%)
1005 (67%)
58
(4%)
952 (63%)
1397 (93%)
1233 (88%)
501 (34%)
88 (6%)
122 (9%)
49
17
42
(3%)
(1%)
(3%)
708
(51%)
623 (45%)
66
(4%)
1102 (73%)
340 (23%)
60 (4%)
911 (61%)
491 (33%)
100 (6%)
Cleaning schedules specifying the following (n=975):

task to be done

Frequency

how surfaces are to be cleaned

removal of visible debris as first stage of cleaning

use of a disinfectant &/or sanitiser

method required for dilution of stock chemicals

method (including details of strip down & reassembly of
the equipment)

who carries out the task

standard expected

specify contact time for disinfectant/sanitiser specified

specify drying
Cleaning practices (n=1502)
Cleaning effectiveness assessed
Cleaning records kept
Colour coded system used for food utensils/equipment
Colour coded system used for cleaning equipment
Cleaning equipment for low risk stored separately from high
risk areas
Separate cleaning implements for raw and ready-to-eat food
areas
Disposable items (e.g. cloths/paper towels) used for cleaning
Disinfectant/sanitiser used for cleaning
Surface clean visually before use of disinfectant/sanitiser
(n=1397)
Minimum of 2 min contact time for disinfectant/sanitiser
(n=1397)
Staff responsible for cleaning surfaces (n=1502)
Able to distinguish the terms disinfectant/sanitiser and
detergent
Demonstrate awareness of dilution factors and contact times
(5%)
(5%)
(5%)
(6%)
(6%)
(8%)
(8%)
 Nearly two-thirds (63%) of food premises used a colour coded system for food utensils or
equipment, whereas only 21% used a colour coded system for cleaning equipment (Table 7).
 The majority of food premises did not store cleaning equipment for raw, non ready-to-eat food
(low risk) areas separately from ready-to-eat food (high risk) areas (70%), nor did they have
separate cleaning implements for raw and ready-to-eat food areas (67%) (Table 7).
 Disposable items used for cleaning, such as disposable cloths or paper towels, were used in
almost two-thirds (63%) of premises (Table 7).
12
 The majority (93%) of premises used a disinfectant/sanitiser for cleaning in the premises and in
most (88%) of these premises the surface was visually clean before use of the
disinfectant/sanitiser (Table 7).
 Less than half of the premises that used a disinfectant/sanitiser identified the active ingredient
(47%) or gave dilution rates (32%) (Table 7).
 Nearly three quarters (73%) of food premises had a member of staff responsible for cleaning
surfaces that was able to distinguish between the terms disinfectant/sanitiser and detergent,
although over a fifth (23%) had a member of staff responsible for cleaning surfaces that could not
(Table 7).
 Most (61%) food premises had a member of staff responsible for cleaning surfaces that was able
to demonstrate awareness of dilution factors and contact times, although a third (33%) had
members of staff responsible for cleaning surfaces that could not (Table 7).
 Approximately half (51%) of the premises that used a disinfectant/sanitiser to clean had staff that
allowed a minimum of two minutes contact time for the disinfectant/sanitiser (Table 7).
Fig. 2 Method of evaluated cleaning effectiveness in food premises (n=1259)
Visual assessment
96.9%
Other (Colourmetric,
Audit by Company
Representative, External
consultant ) 0.7%
ATP & microbiological
testing
0.2%
Microbiological testing
Visually & microbiological
1.0%
testing
1.3%
Food Premises in relation to Food Hygiene Inspections
Food hygiene inspections of premises are carried out to assess hygiene and compliance with public
health protection aspects of food law21. Some food premises and businesses pose a greater risk to the
consumer than others, which is reflected by the frequency of inspection. The nature of the food and
the degree of handling it receives, the method of processing, the potential number of consumers at
risk, the current level of compliance, and the confidence in management/control systems are all taken
into consideration. Using the above factors, food authorities determine the relative food safety risk a
particular premises poses to the public and allocate the frequency of visits accordingly. Premises
rated Inspection Rating Category A pose the greatest risk and are visited at least once every six
months while premises rated Inspection Rating Category F pose the least risk and are visited at least
once every five years. The food premises visited (1502) were categorised as Inspection Rating
Category A, 216 (14%), B, 477 (32%), C, 684 (46%), D, 28 (2%), E, 5 (<1%), and F, 5 (<1%). For
13
87 (6%) premises the Inspection Rating Category was not recorded. Most outlets had an Inspection
Rating Category C (visited once/18 months), and these had proportionally fewer samples (surfaces of
chopping/cutting boards, worktops, and food containers, and cleaning cloths) with ACC levels in
excess of 103 cfu/cm2, swab or ml (23%) than premises rated B (25%; visited once/12 months) or A
(28%; visited once/6 months).
Inspectors 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 premises, and award a consumer at risk score accordingly21.
Scores range from 0 (very few customers at risk) to 15 (a substantial number of customers at risk).
An addition score of 20 exists for premises serving vulnerable groups (the elderly, the sick, young
children and the immunocompromised). The food premises visited (1502) were categorised in
consumer at risk score 0, 22 (1%), 5, 1004 (67%), 10, 278 (18%), 15, 30 (2%), and 20, 38 (3%). For
130 (9%) premises the consumer at risk score was not recorded. No significant difference with regard
to numbers of samples (surfaces of chopping/cutting boards, worktops, and food containers, and
cleaning cloths) with ACC levels in excess of 103 cfu/cm2, swab or ml was found between local
premises (consumer at risk scores of 0 to 5) (22%) and larger businesses (consumer at risk scores of
10 to 15) (21%).
Inspectors assess the food business management of food hygiene and score accordingly21. Confidence
in management scores range from 0 (highly confident) to 30 (no confidence). Premises visited (1502)
had a confidence in management score 0, 52 (3%), 5, 392 (26%), 10, 655 (43%), 20, 230 (15%), and
30, 28 (2%). For 145 (10%) premises the confidence in management score was not recorded.
Significantly more samples (surfaces of chopping/cutting boards, worktops, and food containers, and
cleaning cloths) that had ACC levels in excess of 103 cfu/cm2, swab or ml were from premises with a
confidence management score of 20 or above (29%; high to some confidence) compared with those
with lower scores (23%; little to no confidence) (P<0.0001).
Hazard analysis system
The majority (1057/1502; 70%) of the food premises visited were recorded as having a hazard
analysis system in place, a quarter (378; 25%) of premises did not have a hazard analysis system in
place, and for 67 (5%) premises this information was not recorded. Where hazard analysis systems
were recorded to be in place, almost three-quarters (786/1057; 74%) were documented, 252 (24%)
were not, and for 19 (2%) this information was not recorded. The proportion of different types of
food premises where hazard analysis was in place (documented or undocumented) ranged from 50%
to 94% (Table 8).
Significantly more samples (surfaces of chopping/cutting boards, worktops, and food containers, and
cleaning cloths) with ACC levels in excess of 103 cfu/cm2, swab or ml were from premises where
there was no hazard analysis system in place (39%; 526/1362 samples) compared to those where a
hazard analysis system was in place (27%; 1016/3726) (P<0.00001).
Food hygiene training
For most (1333/1502; 89%) food premises visited, managers had received some form of food hygiene
training. In 126 (8%) premises the managers had received no food training and in 43 (3%) premises
this information was not recorded. For the majority of managers the food hygiene training received
was a basic 6 hour training (928/1333; 70%), but 235 (18%) and 96 (7%) managers had received
intermediate and advanced food hygiene training, respectively. Alternatively, 70 (5%) managers had
received some other form of food hygiene training (including City and Guilds qualification, National
Vocational Qualification (NVQ), RIPHH, Meat and Livestock Commission (MLC) hygiene training,
and internal company training). For 4 (<1%) premises the level of management training was not
recorded. The proportion of different types of food premises with managers that had received food
hygiene training ranged from 84% to 100% (Table 8).
14
Table 8 Number of premises that had hazard analysis in place and managers who had received
food hygiene training (n=1502)
Type of premises
Hotel (n=168)
Restaurant (n=263)
Public house (n= 180)
Café (n=162)
Residential care home
(n=132)
Staff restaurant (n=48)
Delicatessen (n= 80)
Sandwich bar ((n=148)
Baker (n=68)
Butcher (n=98)
Mobile vendor (n=23)
Market stall (n=2)
Others(schools, hospitals
supermarkets, fast food
outlets) (n=118)
Not recorded (n=9)
Hazard Analysis (%)
Food Hygiene Training (%)
In place
Not in place
Not recorded
Trained
Not trained
Not recorded
132
175
112
90
111
(79%)
(67%)
(62%)
(56%)
(84%)
32
78
58
64
13
(19%)
(30%)
(32%)
(39%)
(10%)
4
10
10
8
8
(2%)
(3%)
(6%)
(5%)
(6%)
153
222
161
143
126
(91%)
(84%)
(89%)
(88%)
(95%)
7
35
15
16
4
(4%)
(14%)
(9%)
(10%)
(3%)
8
6
4
3
2
(5 %)
(2%)
(2%)
(2%)
(2%)
31
62
94
47
92
13
1
81
(65%)
(77%)
(64%)
(59%)
(94%)
(57%)
(50%)
(69%)
16 (33%)
14 (18%)
44 (29%)
16 (24%)
6
(6%)
8
(35%)
1 (50%)
32 (27%)
1
4
10
4
(2%)
(5%)
(7%)
(6%)
1
7
14
6
3
3
(2%)
(9%)
(9%)
(9%)
(3%)
(13%)
(6%)
(2%)
(6%)
(1%)
(3%)
(8%)
5
(4%)
(92%)
(89%)
(85%)
(90%)
(94%)
(87%)
(100%)
(85%)
3
2
9
1
3
2
44
71
125
61
92
20
2
100
18
(15%)
3
(33%)
5
1
(11%)
7
(78%)
1
(11%)
1
(11%)
(56%)
Significantly more samples (surfaces of chopping/cutting boards, worktops, and food containers, and
cleaning cloths) with ACC levels in excess of 103 cfu/cm2, swab or ml were from premises where the
manager had received no food hygiene training (39%; 179/455 samples) than from premises where
the manager had received some form of food hygiene training (32%; 1523/4723) (P<0.01).
Significantly, where the manager of the premises had received some form of food hygiene training,
food safety procedures or activities (such as the presence of a hazard analysis system, cleaning
schedules and records kept) were more likely to be in place (Table 9).
Table 9 Hazard analysis and cleaning schedules in relation to management food hygiene
training
Food hygiene training
No
Premises details
Yes
Hazard analysis in place
Hazard analysis in place &
documented
Cleaning schedules used
Cleaning schedules documented
Cleaning records kept
1003/1040*
754/775**
(96%)
(97%)
286/369
39/44
(77%)
(89%)
<0.00001
<0.01
908/954
819/852
637/649
(95%)
(96%)
(98%)
379/458
127/138
639/748
(82%)
(92%)
(85%)
<0.00001
<0.05
<0.00001
P value
*For 17 premises hazard analysis was in place but information on management training was not recorded
**For 11 premises hazard analysis was in place and documented but information on management training was not recorded
Food Handlers
Over three-quarters of food premises (79%) visited employed less than 10 food handlers (Table 10).
However, no relationship was found between the number of food handlers employed (<10 to up to 80)
within a premise and the proportion of which (83% - 100%) that have received food hygiene training
(Table 10)
15
Table 10 Number of Foods Handlers employed per premises that have received food hygiene
training
No. food handlers
employed
No. premises (%)
Proportion of premises with food handlers that have
received food hygiene training (%)
<10
10 - <20
20 - <30
30 - <40
40 - <50
50 - <60
60 - <70
70 - <80
≥80
Not recorded
Total
1183
197
46
15
7
6
4
2
1
41
1502
1117
184
42
14
7
5
4
2
1
(79%)
(13%)
(3%)
(1%)
(<1%)
(<1%)
(<1%)
(<1%)
(<1%)
(3%)
(94%)
(93%)
(91%)
(93%)
(100%)
(83%)
(100%)
(100%)
(100%)
Discussion
The recent report on consumer attitudes to food standards highlights that the main area of concern
about food premises was cleanliness32. The importance of effective cleaning of food surfaces is well
recognised in reducing the potential for cross-contamination, and is an important component of food
safety management systems3. This study found that cleaning cloths from ready-to-eat food
preparation areas within food premises were more heavily contaminated with bacteria (ACC,
Enterobacteriaceae, E. coli, and Staph. aureus) compared to surfaces sampled (cutting/chopping board
work top, and food container surfaces) that were used in the preparation of ready-to-eat foods. This
provides further evidence that cleaning cloths play a key role in the transfer of bacteria in commercial
kitchens. Of the surfaces, cutting/chopping boards (including those used for ready-to-eat foods only)
had higher levels of microbial contamination compared with work top and food container surfaces.
As in previous studies33-36 cleaning cloths were frequently heavily contaminated with bacteria.
Furthermore, the pathogens Campylobacter spp. and Salmonella spp. were isolated from cleaning
cloths (both disposable and reusable) but not from the surfaces sampled in ready-to-eat food
preparation areas. Humphrey et al.37 reported that Campylobacter spp. seem to be able to persist in
kitchen cloths, and cleaning cloths contaminated with Salmonella spp. have been shown to be
associated with outbreaks of Salmonella infection38. Cleaning cloth hygiene could be improved by
ensuring that only freshly disinfected cloths are used for each operation or by the exclusive use of
disposable cloths that are replaced frequently, or paper towels. Scott and Bloomfield35, and Tebbutt33,
have both emphasised the hazards associated with cleaning cloths that may act both as reservoirs of
bacteria as well as disseminators of microbial contamination if not correctly handled. There is little
point in providing separate surfaces for different preparations if all surfaces are cleaned with the same
contaminated cloth. This is also supported by the findings of the present study.
Chopping/cutting boards are extensively used in food premises for preparing foods. In this study
nearly two-thirds of food premises had chopping/cutting boards that were used in both raw and readyto-eat food areas. A quarter of chopping/cutting board surfaces used in the preparation of ready-to-eat
food were found to have high levels of bacteria (≥103cfu/cm2). Boards used to prepare both raw and
ready-to-eat foods more heavily contaminated with bacteria compared to those used for only ready-toeat foods. Surfaces that were visually dirty, wet, last cleaned over 24 hours ago, and/or scored or
damaged making cleaning very difficult, were shown to have higher levels of bacteria. Scott and
Bloomfield35 have shown that microbial survival is enhanced if the surface is wet. There is evidence
that multiplication of some bacteria can take place on these contaminated surfaces and that sufficient
numbers can be transferred onto food, to represent a potential hazard to food safety35. Cutting boards
contaminated with Salmonella spp. have been shown to be associated with outbreaks of Salmonella
infection39. It is suggested that boards should be cleaned more frequently within a 24-hour period,
16
preferably before and after each use, with a non-residual disinfectant. Separate chopping/cutting
boards should be used for ready-to-eat foods, and scored or damaged boards should be replaced.
Surfaces of clean empty food containers that would be used to hold ready-to-eat food were also found
to have high levels of bacteria (15%; ≥103cfu/cm2). Furthermore, these food containers surfaces had
over five times as much E. coli (faecal indicator organism) present (5%) compared to other surfaces
sampled (chopping/cutting boards (0.9%), work tops (0.6%)). Food containers should be thoroughly
cleaned between each use and stored in a clean dry place.
Various methods of enumerating microbial surface contamination exist although there is no consensus
as to an accepted standard method40. Although conventional hygiene swabbing is widely used, this
method has been reported to recover only a proportion of the total bacterial population present on a
surface. The effective removal of bacteria from the swab has been identified as an important
contributory factor with regard to swab sensitivity. Sampling sponges are very absorbent, and any
bacteria that become dislodged during sampling are likely to be absorbed with the liquid and become
trapped within the sponge matrix41. Recovery of bacteria from sampling sponges may also be affected
with the length of time from sampling to laboratory examination (CJ Griffith, unpublished). The main
disadvantage of traditional based hygiene monitoring techniques, such as swabbing, however is the
time required for results to be obtained. Hazard analysis systems require that monitoring should
provide results in real time for remedial action to be implemented. Low cost non-instrument based
rapid hygiene monitoring kits are now available that can provide a real-time estimate of total surface
contamination resulting in an indication of overall cleaning efficacy40.
The cleanliness of various food production environments has been assessed16,33,42,43. However, there is
relatively little published information on cleaning regimes or standards of cleanliness in food
premises, other than butcher shops prior to the specific implementation of the HACCP system in
these premises44. A lack of written cleaning schedules and records, training in the correct use of
cleaning products and awareness of the importance of cleaning hand contact sites were identified in
butcher shops as common defects. Those findings are also supported in this study, where only
approximately half (55%) of the food premises had documented cleaning schedules, or kept cleaning
records (44%). Most of the food premises visited had physically separate areas for raw and ready-toeat food (61%), although most premises did not have separate cleaning implements for raw and readyto-eat food areas (67%), or stored cleaning equipment for high risk areas separately from those used in
low risk areas (70%). This is a matter of concern that needs to be addressed. Although most staff
responsible for cleaning surfaces within the food premises visited were able to distinguish between
the terms disinfectant/sanitiser and detergent (73%), and demonstrated awareness of dilution factors
and contact times (61%), only a quarter (25%) of the cleaning schedules specified the contact time for
the disinfectant/sanitiser used. Worsfold and Griffith44 identified that the effectiveness of cleaning
assessed in butcher shops was generally underestimated when assessed visually as it is known that
visually clean surfaces may not be microbiologically clean45. In this study visual observation was
most commonly used in food premises (97%) to assess cleaning effectiveness. Visual assessment of
cleanliness has a limited value and should only be used as the first stage in an integrated monitoring
programme14.
Legal requirements (Food Safety (General Food Hygiene) Regulations 19951) relating to food hygiene
training apply only to food handlers. However, industry guidelines suggests that “senior supervisors
who do not actually handle food, but who may have a direct influence on the hygienic operation of the
business should also receive training as a matter of good practice”3,4. A hazard analysis system was in
place in the majority (70%) of food premises visited, and documented in almost three-quarters (74%)
of these, and most managers (89%) had received some form of food hygiene training. Surface
samples (chopping/cutting boards, work tops, food containers) and cleaning cloths with ACC levels in
excess of 103 cfu/cm2, swab or ml collected from food premises were related to poor Local Authority
Inspectors' Confidence in Management/Control Systems scores and food safety procedures, i.e. the
absence of a hazard analysis system, cleaning schedule, and cleaning records, which in turn related to
management food hygiene training. Most food premises visited in this study employed less than 10
food handlers (79%) and had consumer at risk scores of 5 (67%) which is indicative of small outlets.
17
The House of Commons Agriculture Committee on Food Safety46 noted that medium and smaller
sized businesses do not have access to the same level of food safety expertise as larger premises and,
even when undertaken, training may not be of sufficient quality. It is possible that the dynamic nature
of staffing levels in catering premises causes a deficiency in management training, resulting in less
stringent food hygiene procedures and lower cleaning standards. Effective implementation of hazard
analysis system and cleaning schedules depends crucially on well trained managers and employees in
food businesses. Increased awareness, through adequate training of all food handlers and managers,
may lead to an improvement in cleaning standards and practices in food premises.
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 PHLS and non-PHLS laboratories
who performed the microbiological examination. Thanks are extended to LEP (CPHL) for typing
isolates, to David Lock at LACOTS for co-ordinating the participation of Environmental Health
Officers (EHOs), to Mr Raymond Allen from Enfield BC, and the Gloucester Food Safety Group, in
particular to Mrs Dorothy Sharp at Gloucester PHL, for their advice in preparing the sampling
protocol, and to Lillian Hucklesby for entering the data.
References
1. The Food Safety (General Food Hygiene) Regulations 1995. London: HMSO.
2. Council Directive 93/43/EEC of 14 June 1993 on the hygiene of foodstuffs. Official Journal of
the European Communities L175/1-11.
3. Joint Hospitality Industry Congress Food Safety and Hygiene Working Group. Food Safety
(General Food Hygiene) Regulations 1995. Industry Guide to Good Hygiene Practice: Catering
Guide. London: Chadwick House Group, 1997.
4. Food Safety and Hygiene Working Group. Food Safety (General Food Hygiene) Regulations
1995. Industry Guide to Good Hygiene Practice: Retail Guide. London: Chadwick House Group,
1997.
5. Evans HS, Madden P, Douglas C, Adak GK, O'Brien S, Djuretic T, Wall PG, Stanwell-Smith.
General outbreaks of infectious intestinal disease in England and Wales: 1995 and 1996. Comm
Dis Pub Health 1998; 1: 165-171.
6. Scott E, Bloomfield SF. The survival and transfer of microbial contamination via cloths, hands
and utensils. J Appl Bacteriol 1990; 68: 271-278.
7. Tebbutt GM. An evaluation of various working practices in shops selling raw and cooked meats. J
Hyg Camb 1986; 97: 81-90.
8. Humphrey TJ, Martin KW, Whitehead A. Contamination of hands and work surfaces with
Salmonella enteritidis PT4 during the preparation of egg dishes. Epidemiol Inf 1994; 113: 403409.
9. Dawkins HC, Bolton FJ, Hutchinson DN. A study of the spread of Campylobacter jejuni in four
large kitchens. J Hyg Camb 1984; 92: 357-364.
10. Gibson H, Talor JH, Hall KE, Holah JT. Effectiveness of cleaning techniques used in the food
industry in terms of removal of bacterial biofilms. J Appl Microbiol 1999; 87: 41-48.
11. Cox GL. Determination by Graham L Cox, Sheriff Principal of Sherriffdom of South Strathclyde
Dumfries and Galloway. Determination into the E. coli O157 Fatal Accident Inquiry. Sheriffdom
of South Strathclyde, Dumfries and Galloway, 1998.
12. Commission Decision (2001/471/EC) of 8 June 2001 laying down rules for the regular checks on
the general hygiene carried out by operators in establishments according to Directive 64/433/EEC
on health conditions for the production and marketing of fresh meat and Directive 71/118/EEC on
health problems affecting the production and placing on the market of fresh poultry meat. Official
Journal of the European Communities L165/48-53, 21.6.2001.
18
13. Favero MS, Gabis DA, Vesley D. Environmental monitoring procedures. In Compendium of
Methods for the Microbiological Examination of Foods. Ed: Speck ML, pp. 49-54. Washington
DC: APHA.
14. Griffith CJ, Cooper RA, Gilmore J, Davis C, Lewis M. An evaluation of hospital cleaning
regimes and standards. J Hospital Infection 2000; 45: 19-28.
15. Mossel DAA, Jansen JT, Strijk CB. Microbiological safety assurance applied to smaller catering
operations worldwide. Food Control 1999; 10: 195-211.
16. Herbert M, Donovan T, Manger P. A study of the microbiological contamination of working
surfaces in a variety of food premises using the traditional swabbing technique and commercial
contact slides. Ashford, PHLS, 1990.
17. Tebutt GM. A microbiological study of various food premises with an assessment of cleaning and
disinfection practices. J Hyg Camb 1984; 92: 365-375.
18. Odgen K. Practical experience of hygiene control using ATP bioluminescence. J Inst Brewing
1993; 99: 389-393.
19. Worsfold D, Griffith CJ. An assessment of cleanliness in domestic kitchens. Hyg Nutr Food Serv
Catering 1996; 1: 163-173.
20. Food Standards Agency. Food Safety Act 1990, Code of Practice No 7:- Sampling for Analysis
and Examination (Revised October 2000). London: FSA, 2000.
21. Food Standards Agency. Food Safety Act 1990, Code of Practice No 9:- Food Hygiene
Inspections (Revised October 2000). London: FSA, 2000.
22. PHLS. Standard Methods for Food Products. Aerobic Colony Count at 30°C: Surface Plate
Method. Standard Method: F10. London: PHLS, 1998.
23. PHLS. Standard Methods for Food Products. Aerobic Colony Count at 30°C: Spiral Plate
Method. Standard Method: F11. London: PHLS, 1998.
24. PHLS. Standard Methods for Food Products. Enumeration of Enterobacteriaceae by Colony
Count Technique. Standard Method: F23. London: PHLS, 1998.
25. PHLS. Standard Methods for Food Products. Direct Enumeration of Escherichia coli. Standard
Method: F20. London: PHLS, 1998.
26. PHLS. Standard Methods for Food and Dairy Products. Enumeration of Staphylococcus aureus.
Standard Method: F12. London: PHLS, 1998.
27. PHLS. Standard Methods for Food Products. Detection and Enumeration of Listeria
monocytogenes and other Listeria spp.. Standard Method: F19. London: PHLS, 2000.
28. PHLS. Standard Methods for Food Products. Detection of Campylobacter spp. Standard Method:
F21. London: PHLS, 1998.
29. PHLS. Standard Methods for Food Products. Detection of Salmonella spp. Standard Method:
F13. London: PHLS, 1998.
30. PHLS. Standard Methods for Food Products. Detection of Escherichia coli O157 by
Immunomagnetic Bead Separation. Standard Method: F17. London: PHLS, 2001.
31. Centers for Disease Control and Prevention (CDC). Epi Info, version 6.04d: a word processing,
database and statistical programme for epidemiology on computers, 2001.
<http://www.cdc.gov/epiinfo/index.htm>
32. COI Communications and Food Standards Agency. Consumer Attitudes to Food Standards,
January 2001. COI Ref: 4695. Taylor Nelson Sofres plc.
33. Tebbutt GM 1984. A microbiological study of various food premises with an assessment of
cleaning and disinfection practices. J Hyg Camb 1984; 92: 365-75.
34. Tebbutt GM 1986. An evaluation of various working practices in shops selling raw and cooked
meats. J Hyg Camb 1986; 97: 81-90.
35. Scott E, Bloomfield SF. The survival of microbial contamination via cloths, hands and utensils. J
Appl Bacteriol 1990; 68: 271-8.
36. Scott E, Bloomfield SF. An in-use study of the relationship between bacterial contamination of
food preparation surfaces and cleaning cloths. Lett Appl Microbiol 1993; 16: 173-77.
37. Humphrey TJ, Martin KW, Slader J, Durham K. Campylobacter spp. in the kitchen: spread and
persistance. J Appl Microbiol 2001; 91: 115S-120S.
19
38. Holtby I, Tebbutt GM, Grunert E, lyle HJ and Stenson MP. Outbreak of Salmonella Enteritidis
phage type 6 infection associated with food items provided at a buffet meal. Comm Dis Rep
1997;7: 87-90
39. Sanborn WR. The relation of surface contamination to the transmission of disease. Amm J Pub
Health 1963; 53: 1278-83.
40. Moore G, Griffith C. A comparison of surface sampling methods for detecting coliforms on food
contact surfaces. Food Microbiol 2002; In press.
41. Daley EF, Pagotto F, Farber JM. The inhibitory properties of various sponges on Listeria spp.
Letts Appl Microbiol 1995; 20: 195-198.
42. Gibson H, Taylor JH, Hall KE, Holah JT. Effectiveness of cleaning techniques used in the food
industry in terms of the removal of bacterial biofilms. J Appl Microbiol 1999; 87; 41-48.
43. Ogden K. Practical experience of hygiene control using ATP bioluminescence. J Inst Brewing
1993; 99: 389-93.
44. Worsfold D, Griffith CJ. Ann assessment of cleaning regimes and standards in butchers' shops. Int
J Environ Health Res 2001; 11: 245-56.
45. Dillon M, Griffith CJ. Assessing cleanliness, In How to clean - a management guide. Humberside
UK: MD Associates, 1999, pp. 58-74.
46. House of Commons Agriculture Committee Fourth Report (1998) Food Safety. Vol I. 22 April
1998. London: The Stationary Office.
20
Annex 1:
Participating PHLS Groups, Laboratories and Local Authority Food
Liaison Groups and number of premises visited
Table 1a. Participating PHLS Groups, Public Health Laboratories and number of premises visited
PHLS group
Public Health Laboratory No. premises visited
No. samples collected
East
Chelmsford
Luton
Norwich
Ashford
Brighton
London FWE Unit1
Reading
WEMS2
Birmingham
Coventry
Shrewsbury
Stoke
Chester
Preston
Carlisle
Hull
Leeds
Middlesborough
Newcastle
Bristol
Exeter
Gloucester
Hereford
Plymouth
Truro
Leicester
Lincoln
Sheffield
Bangor
Cardiff
Carmarthen
Rhyl
353
331
203
180
406
420
224
241
107
330
198
129
211
182
110
118
129
239
128
261
215
471
127
64
111
137
264
106
56
62
138
56
6307*
London & South east
Midlands
North west
North
South West
Trent
Wales
Total
76
71
43
39
89
97
48
56
21
70
42
28
52
46
22
26
30
51
29
58
47
122
26
15
26
30
61
23
12
15
30
12
1415
1, London Food, Water & Environmental Unit, CPHL
2, Wessex Environmental Microbiological Services
Table 1b. Participating Non-PHLS Laboratories and number of premises
Non-Public Health Laboratory
No. premises visited
No. Samples collected
Belfast City Hospital
City of Edinburgh
Dundee Scientific Services
Fife Area Laboratory, Kirkcaldy
Glasgow Scientific Services
Kings Lynn & West Norfolk
Public Analyst Aberdeen
Royal Alexandra, Paisley
Worcester Royal Infirmary
Worcestershire Scientific
Total
33
5
2
3
14
5
5
1
7
12
87
158
23
13
13
58
19
22
5
44
27
282*
*Includes the 56 samples not included in the analysis
Table 1c. Local Authority Food Liaison Groups and number of premises
21
Local Authority Food Liaison Group
No. premises visited
No. Samples collected
Berkshire Food Co-ordinating Group
Cambridge Food Liaison Group
Cheshire Food Liaison Group
Cornwall CEHOS Food Sub-Group
Cumbria IEHO Food Safety Group
Derbyshire Food Liaison Group
Devon Food Safety Group
Dorset Food Group
Durham Food Liaison Group
East Sussex Food Liaison Group
Essex Food Group
Greater Manchester Food Liaison Group
Gloucester Food Safety Group
Hampshire & Isle Of Wight Food Advisory Group
Hereford & Worcester CEHOS Food Working Group
Herts & Beds IEHO And Chief Officers Food Group
Humberside Food Liaison Group
IEHO Buckinghamshire Branch Food Group
Kent Food Technical Group
Lancashire Assn Of CEHOS, Food Officer Group
Leicestershire Food Liaison Group
LFCG1 North East Sector
LFCG South East Sector
LFCG South West Sector
LFCG North West Sector
Lincolnshire Co-ordinating Group
Merseyside Food Sub-Group
North Yorkshire CEHOS Group
Northamptonshire Food Liaison Committee
Northern Ireland Food Group
Northumberland Food Safety Group
Norfolk Food Liaison Group
Nottingham District Food Group
Oxfordshire CC Food Sub-Group
Scottish Food Co-ordinating Committee
Shropshire Food Liaison Group
Somerset Food Liaison Group
South Yorkshire Food Forum
Staffordshire Food Safety Group
Suffolk Food Liaison Group
Surrey Food Liaison Group
Tees Valley Food Safety Group
Tyne & Wear Food Control Group
Wales South West Group
Wales North Group
Wales South East Group
Warwickshire Food Liaison Group
West Midlands Food Liaison Group (inc. Black Country)
West of England Food Liaison Group
West Sussex Food Liaison Group
West Yorkshire Principal Food Officers Group
Wiltshire Food Group
Total
37
31
27
26
24
12
33
16
17
35
32
24
122
35
55
56
19
19
39
20
30
22
24
28
25
40
18
11
36
33
11
34
22
7
30
12
29
11
34
23
38
29
15
29
31
13
34
44
41
18
29
22
1502
147
140
104
115
86
53
149
61
75
167
179
117
582
160
256
226
95
87
168
73
101
92
111
126
119
181
64
49
170
154
43
109
86
39
138
48
126
29
138
108
167
130
53
132
145
56
162
198
192
73
111
99
6589*
1, London Food Co-ordinating Group
*Includes the 56 samples not included in the analysis
22