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Microbiological examination of food from takeaways and sandwich bars

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					Food     Standards      Agency        Catering    Hygiene      Initiative:    Microbiological
Examination of Food from Take-aways and Sandwich Bars


CL Little1, RT Mitchell1, J Barnes2
1, Environmental Surveillance Unit, PHLS Communicable Disease Surveillance Centre, 61 Colindale
Avenue, London NW9 5EQ.
2, Local Authority Enforcement (Policy) Division, Food Standards Agency, Aviation House, 125
Kingsway, London WC2B 6NH

On behalf of the Food Standards Agency (FSA) and the Public Health Laboratory Service (PHLS).


Summary

During August 2001 a microbiological study of ready-to-eat cooked rice from take-aways,
and chicken sandwiches (without salad) made on the premises from sandwich bars, was
undertaken. The intention was to identify risk factors in the production, storage and handling
of cooked rice and sandwiches and to establish their effect on microbiological quality.

•   Examination of cooked rice revealed that the majority (87%; 442 of 508) were of
    satisfactory/acceptable microbiological quality; 50 (10%) were of unsatisfactory
    microbiological quality and 16 (3%) were of unacceptable microbiological quality
    (Bacillus spp. and Bacillus cereus ≥105 cfu/g). Unsatisfactory results were due to high
    levels of Aerobic Colony Counts (ACC) (≥106 cfu/g), Escherichia coli (≥102 cfu/g), B.
    cereus and other Bacillus spp (≥104 cfu/g).

•   Examination of chicken sandwiches or rolls (without salad) found that most (75%; 335 of
    449) were of satisfactory/acceptable microbiological quality and 114 (25%) were
    unsatisfactory. Unsatisfactory results were due to high levels of Enterobacteriaceae
    (≥104 cfu/g), ACC (≥107 cfu/g), E. coli (≥102 cfu/g) and Staph. aureus (≥102 cfu/g).
    Salmonella spp. and Campylobacter spp. were not detected in any of the samples
    examined.

•   The microbiological quality of cooked rice was significantly associated with cuisine type
    (P<0.00001), rice type (P<0.01), cooking (P<0.00001), serving methods (P<0.01), and
    management food hygiene training (P<0.01).

•   Acceptable microbiological quality of sandwiches was significantly associated with
    sandwich bars that had hazard analysis in place (P<0.05). The microbiological quality of
    chicken sandwiches or rolls was associated with storage, display and serving methods,
    although this was not statistically significant.

•   The microbiological quality of food from both take-aways and sandwich bars was further
    significantly associated with local outlets as indicated by Local Authority Inspectors'
    Consumer at Risk scores (P<0.001).

•   The majority (90%) of premises had hand washing facilities accessible and available for
    use, although only over half (55%) were used as judged by the sampling officer.

•   Significantly, where the manager of the premises had received some form of food
    hygiene training, food safety procedures such as the hazard analysis system were more
    likely to be in place (P<0.0001).


                                                                                                1
Introduction

Catering is one of the largest industries in the UK with over 300,000 outlets, approximately
80% of which are independently owned and operated. The small and medium size
enterprise nature of the catering sector is demonstrated by the simple average that less than
nine staff are employed per outlet1. Eating out has increased considerably over recent
years, with two-thirds of the population in 2000 occasionally or regularly using take-aways to
eat out2. Consumption of ethnic foods (outside the home) continues to increase from 1998
with more purchases of Indian and Chinese dishes, while consumption of sandwiches and
rolls remains similar to 19983. Sandwiches are a popular food; a fifth (20%) of the total
market volume (1,796 million) of sandwiches are purchased from sandwich bars or cafés,
and chicken sandwiches account for the third (12%) most popular sandwich filling4.

The Food Safety (General Food Hygiene) Regulations 19955 implements the European
Community’s Directive on Food Hygiene (93/43/EEC). Caterers must apply the principles of
hazard analysis to their own business. Food hygiene training and instruction for all staff
handling food is also a legal requirement. The UK Catering Guide advises catering
businesses of how to comply with their legal obligations and to ensure food safety6.
Inadequate cooking or reheating (50%), inappropriate storage (45%), and cross-
contamination (39%) have been identified as important contributory factors of foodborne
outbreaks in England and Wales7, highlighting the importance of training food handlers in
good hygiene practices.

Cooked rice was first recognised as a cause of food poisoning through contamination with
Bacillus cereus in 19718. B. cereus can give rise to two distinct forms of foodborne disease,
the emetic and diarrhoeal syndromes. Outbreaks attributed to B. cereus emetic food
poisoning in England and Wales have frequently implicated boiled or fried rice from take-
away outlets as the vehicle7,9,10. Many outbreaks of a similar nature have occurred in
Canada, Finland, the Netherlands, Japan, and the USA11-16. Incidents of rice associated
food poisoning in England and Wales have been linked to the practice of preparing rice, for
serving, in bulk in advance. This practice involves boiling a large quantity of rice, which is
then kept at room temperature before reheating. There has been resistance to the
refrigeration of boiled rice since this, apparently, has an adverse effect on the finished
product17. Uncooked rice frequently contains spores of B. cereus that can survive boiling. If
cooked rice is subsequently stored at room temperature for long enough the heat resistant
spores will germinate, proliferate and may produce emetic toxin in the product18-20.
Reheating the rice prior to serving will not inactivate the emetic toxin and render the product
safe. Levels of B. cereus in foods incriminated in incidents of the emetic form of food
poisoning have ranged from 1.0x103 to 5.0x1010 organisms per gram10. It is only when large
numbers of B. cereus are present or when toxin is produced that B. cereus becomes a
hazard. A LACOTS/PHLS study in 1995 found 6% of cooked rice samples from take-aways
                                                     4                                 5
and restaurants were of unsatisfactory ( 10 cfu/g) or unacceptable ( 10 cfu/g)
microbiological quality21. Cell multiplication during inadequate cooling and storage of cooked
rice is the greatest problem.

The British Sandwich Association (BSA) has provided additional food hygiene guidance for
sandwich manufacturers and sandwich bars22. The preparation of sandwiches involves
much handling during preparation of the filling and sandwich assembly, which adds to the
likelihood of contamination unless high standards of hygiene are maintained. Previous
studies have shown that sandwiches frequently have high levels of microorganisms and,
less frequently, a range of potential pathogens23-25. These studies also highlighted a lack of
awareness among staff concerning the importance of temperature control in the display of




                                                                                             2
sandwiches. Sandwiches have been linked to reported outbreaks of food poisoning, with
outbreaks of Salmonella spp.26,27 and Escherichia coli O15728 traced to sandwiches.

As part of its strategy to reduce foodborne disease29, the Food Standards Agency (FSA) is
planning a national food hygiene campaign to raise awareness and understanding of
effective food safety management systems aimed mainly at small and less developed
catering businesses30. Information to support this campaign will include a study undertaken
on behalf of the FSA on food from take-aways and sandwich bars. The purpose of this study
was to establish the microbiological quality of cooked rice and chicken sandwiches from
take-away and sandwich bar premises, respectively in the UK. In addition, the study sought
to determine the extent to which these catering premises comply with the legal requirements.


Materials and Methods

Sample Collection
Cooked rice and chicken sandwiches collected from take-aways and sandwich bars,
respectively were examined in PHLS and non-PHLS laboratories throughout the UK
between 1st August and 31st August 2001 according to a standardised protocol and
reporting system. Cooked rice samples consisted of freshly or reheated (from pre-cooked
rice) cooked rice collected at the point-of-sale, as if being purchased by the customer. Rice
samples collected included basmati, brown and wild rice. Rice salads, rice dishes, and rice
puddings were all specifically excluded from the study. Chicken sandwich samples included
sandwiches prepared on the premises. Chicken sandwiches containing salad, herbs, and
other ingredients such as shellfish, red meats, and stuffing were all specifically excluded
from the study. Samples were collected by staff from local Environmental Health
Departments in accordance with the Food Safety Act 1990, Code of Practice No. 731.

Information on the takeaway and sandwich bar premises was obtained by observation and
enquiry and recorded on a standard proforma. This included information on the premises
and practices, with specific regard to food safety legislation32. Additional information
collected on cooked rice and chicken sandwiches included how the rice was cooked and
how the sandwiches were made, displayed and served.

Sample Examination
Cooked rice were examined for levels of B. cereus and other Bacillus spp. Escherichia coli
and the Aerobic Colony Count (ACC) to provide an indication of hygiene and levels of
contamination. Chicken sandwich samples were examined for the presence of Salmonella
spp. and Campylobacter spp.        In addition Staphylococcus aureus, E. coli, and
Enterobacteriaceae were enumerated, and the ACC determined to indicate hygiene and
levels of contamination.

The ACC was determined in accordance with PHLS Standard Microbiological Methods for
Food Products F1033 and F1134. Enterobacteriaceae, E. coli, Staph. aureus, B. cereus and
other Bacillus spp., Campylobacter spp., and Salmonella spp. were enumerated or detected
in accordance with PHLS Standard Microbiological Methods35-40. Isolates of B. cereus and
other Bacillus spp. exceeding 104 cfu/g were sent to the Food Safety Microbiology
Laboratory (FSML), at the Central Public Health Laboratory (CPHL) for further
characterisation.




                                                                                           3
Results
A total of 957 cooked rice (508) and chicken sandwich (449) samples were collected by 51
Local Authority Food Liaison Groups, involving 231 Local Authorities, for examination in 35
laboratories (29 PHLS and 6 non-PHLS) in England, Wales, Scotland and Northern Ireland
(Annex 1).


Cooked Rice from Take-aways

Microorganisms isolated from cooked rice from take-aways

Of the 508 cooked rice samples examined, 46 (9%) had ACCs of 106 cfu/g or more (Table
1). E. coli at or greater than 102 cfu/g were present in 15 (3%) samples. B. cereus and
other Bacillus spp. were present at 104 cfu/g or more in 7(1%) and 29 (6%) samples,
respectively. A proportion of these Bacillus isolates were further characterised and typed,
with most (71%; 20/28) shown to be B. subtilis (Table 2). Typing of B. cereus isolates
produced 4 different H serotypes, two of which are types (types 1, 5) most commonly
implicated in food poisoning (Table 2).

Table 1 Microbiological results of cooked rice from take-aways (n=508)

                              <20/        20-<102      102 - <103     103 - <104   104 - <105   105 - <106   106 - <107   ≥107
                              <200†
Aerobic colony count          209a         30           67            88           45           23           21           25
Escherichia coli              490a         3            8             2            3            2
Bacillus spp.                 433b                      23            23           14           9            5            1
Bacillus cereus               485b                      11            5            4            2            1
†, cfu/g
a; lower limit of detection 20 cfu/g, b;lower limit of detection 200 cfu/g.


                                                                                        4
Table 2. Bacillus cereus and other Bacillus spp. isolated at 10 cfu/g or more from cooked rice

Bacillus spp.                                                         No. of isolates

B. cereus                                                             4
B. subtilis                                                           20
B. licheniformis                                                      3
B. pumilis                                                            1
Total                                                                 28

Serotypes of B. cereus
1                                                                     1
5                                                                     1
21                                                                    1
NT                                                                    1



Microbiological quality of cooked rice

Based on the PHLS Microbiological Guidelines for some ready-to-eat foods sampled at the
point of sale41, 409 (81%) of 508 cooked rice samples were satisfactory, 33 (6%) acceptable,
50 (10%) unsatisfactory, and 16 (3%) were of unacceptable microbiological quality (Table 3).
The ACC was the microbiological parameter most often associated with unsatisfactory
results, accounting for over three-quarters (78%; 39/50) of unsatisfactory samples, of which
8 (16%) and 5 (10%) also had unsatisfactory levels of E. coli (≥102 cfu/g) and Bacillus spp.
(≥104 cfu/g), respectively. The remainder (22%; 11) was due to E. coli at 102 cfu/g or more,
and B. cereus and/or other Bacillus spp. in excess of 104 cfu/g. Unacceptable results (16)
were due to high levels ( 105 cfu/g) of Bacillus spp. (94%; 15/16), of which two samples also


                                                                                                                                 4
had unacceptable levels of B. cereus ( 105 cfu/g). The remaining sample had unacceptable
levels of B. cereus ( 105 cfu/g).

Table 3 Key to classification in the PHLS Microbiological Guidelines for Cooked Rice sampled
                     40
at the point of sale

Criterion                             Microbiological Quality (cfu per gram unless stated)
                       Satisfactory        Acceptable        Unsatisfactory          Unacceptable/
                                                                                  Potentially hazardous
Aerobic Colony Count       <105              105 - <106             >106                     N/A
E. coli (total)            <20               20 - <102              >102                     N/A
B. cereus and other        <103              103 - <104           104 - <105                 >105
pathogenic Bacillus
spp#.
*N/A; not applicable



Half the cooked rice samples were boiled or steamed rice (50%) (Table 4).

•   Significantly more samples of pilau rice (27%) were of unsatisfactory or unacceptable
    microbiological quality compared to boiled/steamed (13%), fried (10%) and/or egg fried
    rice samples (4%) (P<0.01). Most pilau rice samples (96%; 75/78) were collected from
    Indian take-aways.


Product history in relation to microbiological quality

Cuisine type of rice
Most cooked rice samples (508) were collected from Chinese (59%) or Indian (35%)
takeaways (Table 4). Significantly more samples from Indian take-aways (29%) were of
unsatisfactory or unacceptable microbiological quality compared with cooked rice from
Chinese take-aways (4%) (P<0.00001).

Cooking and Serving
Over three-quarters (78%) of cooked rice samples were cooked in bulk quantities, and over
half (53%) of the rice samples were served freshly cooked (Table 4).

•   Significantly more rice served reheated from pre-cooked rice (20%) were of
    unsatisfactory or unacceptable microbiological quality compared to those served freshly
    cooked (7%) (P<0.00001). Most rice reheated from pre-cooked rice were cooked in bulk
    quantities (85%; 193/228).

Approximately half (48%) of pre-cooked rice samples were stored at ambient temperature,
and over a third (36%) were last cooked within four hours, prior to being reheated (Table 4).
No significant difference was found between the microbiological quality of pre-cooked rice
samples stored at refrigerated or ambient temperature (Table 4).

•   However, significantly more rice samples reheated from pre-cooked rice that were last
    cooked eight hours or more prior to reheating were of unsatisfactory or unacceptable
    microbiological quality compared to those pre-cooked last cooked within four hours
    (Table 4) (P<0.01).




                                                                                                          5
Table 4 Details of 508 cooked rice samples collected from take-aways

Cooked rice details                      Number of   (%)        Unsatisfactory/   (%)
                                         premises               Unacceptable
                                                                samples
Type of rice
Boiled/Steamed                           253         (50%)      33                (13%)
Fried                                    61          (12%)      6                 (10%)
Egg fried                                112         (22%)      5                 (4%)
Pilau                                    78          (15%)      21                (27%)
Other (Saffron)                          4           (1%)       1                 (25%)

Cuisine type of rice
Indian                                   178         (35%)      51                (29%)
Chinese                                  298         (59%)      12                (4%)
Thai                                     10          (2%)       0
Other (Cantonese, Caribbean, European,   22          (4%)       3                 (14%)
Greek, Lebonese, Nepalese)

Serving rice
Freshly cooked                           264         (53%)      19                (7%)
Reheated from pre-cooked rice            241         (47%)      47                (20%)
Not recorded                             3           (<1%)      0

Storage temperature of pre-cooked rice (n=241)
Refrigerated                              82         (34%)      19                (23%)
Ambient                                   116        (48%)      28                (24%)
Hot                                       35         (15%)      0
Not recorded                              8          (3%)       2                 (25%)

Time since rice last cooked (n=241)
<4 hours                                 87          (36%)      7                 (8%)
4 - <8 hours                             41          (17%)      6                 (15%)
8 - <12 hours                            21          (9%)       7                 (33%)
12 - <24 hours                           61          (25%)      20                (33%)
24 - <48 hours                           15          (6%)       6                 (40%)
  48 hours                               5           (2%)       3                 (60%)
Not recorded                             11          (5%)       0

Quantity rice cooked
Small (serve up to 6 portions)           106         (21%)      12                (11%)
Bulk (serve over 6 portions to 2 kgs)    398         (78%)      54                (14%)
Not recorded                             4           (1%)       0




Chicken sandwiches/rolls (without salad) from sandwich bars

Microorganisms isolated from chicken sandwiches from sandwich bars

Of the 449 chicken sandwich/roll samples examined, 57(13%) had ACCs of 107 cfu/g or
more (Table 5). Enterobacteriaceae at or greater than 104 cfu/g were present in 86 (19%)
samples. E. coli and Staph. aureus were present at 102 cfu/g or more in 15 (3%) samples
and 10 (2%) samples, respectively. Salmonella spp. and Campylobacter spp. were not
detected in any of the samples examined.


Microbiological quality of chicken sandwiches

Based on the PHLS Microbiological Guidelines for some ready-to-eat foods sampled at the
point of sale41, 179 (40%) of 449 chicken sandwich samples were satisfactory, 156 (35%)
acceptable, and 114 (25%) samples were of unsatisfactory microbiological quality. None of
the samples examined were of unacceptable microbiological quality (Table 6).
Enterobacteriaceae was the microbiological parameter most often associated with



                                                                                          6
unsatisfactory results, accounting for three-quarters (75%; 86/114) of unsatisfactory
samples, of which 39 (34%), 10 (9%), and 7 (6%) also had unsatisfactory levels of ACC
(≥107 cfu/g), E. coli ( ≥102 cfu/g) and Staph. aureus (≥102 cfu/g), respectively. The remainder
(25%; 28) was due to unsatisfactory levels of ACC (≥107 cfu/g), E. coli and/or Staph. aureus
(≥102 cfu/g).

Table 5 Microbiological results of chicken sandwiches from sandwich bars (n=449)
                                                                     2             3               4        5             6
                                                                                                                                  ≥10
                                                                                                                                        7
                             ND*        <10/          20-         10 -        10 -           10 -      10 -          10 -
                                            †             2           3           4              5         6             7
                             in 25g     <20           <10         <10         <10            <10       <10           <10
Aerobic colony count                     1a            3           14         99             134       99            42           57
Enterobacteriaceae                       117b          69          96         81             51        23            9            3
Escherichia coli                         419a          15          9          6
                                            a
Staphylococcus aureus                    431           8           6          4
Campylobacter spp.           449
Salmonella spp.              449
*ND; Not detected ;
†, cfu/g
a; lower limit of detection 20 cfu/g, b; lower limit of detection 10 cfu/g.



Table 6 Key to classification in the PHLS Microbiological Guidelines for Chicken Sandwich
                                            40
(without salad) sampled at the point of sale

Criterion                                       Microbiological Quality (cfu per gram unless stated)
                                 Satisfactory              Acceptable         Unsatisfactory              Unacceptable/
                                                                                                       potentially hazardous
Aerobic Colony Count                 <106                     106 - <107                 >107                        N/A
Enterobacteriaceae                   <102                     102 - <104                 >104                        N/A
E. coli (total)                      <20                      20 - <102                  >102                        N/A
Staph. aureus                        <20                      20 - <102                102 - 104                     >104
Salmonella spp.             Not Detected in 25 g                                                                Detected in 25g
Campylobacter spp.          Not Detected in 25 g                                                                Detected in 25g
*N/A; not applicable




Product history in relation to microbiological quality

Preparation, storage and display of sandwiches/rolls
Of the 449 chicken sandwiches or rolls collected, most contained no spices or spiced
ingredients (90%), nor mayonnaise (82%) (Table 7). No significant difference was found
between the microbiological quality of samples with and without spices, or with and without
mayonnaise. Of those sandwiches or rolls (45) that contained spices or spices ingredients,
most contained black pepper (15), tikka seasoning (7), curry seasoning (6), garlic (2), cajun
seasoning (2), mustard (2), ginger (1) paprika (1), coriander (1); for eight samples this
information was not recorded.

The majority (84%) of sandwich bars displayed or stored sandwich or roll fillings at or below
8°C, and two-thirds (66%) of sandwich/roll fillings were stated to be in the food service area
for four hours or less during sandwich/roll preparation (Table 7). Over half (56%) of the
sandwich/roll fillings were covered, and over two-thirds (68%) were protected by a display
screen (Table 7).

•    The majority of sandwiches or rolls were prepared or stored in a visually clean area
     (96%) as judged by the sampling officer (Table 7).




                                                                                                                                        7
    -   The low proportion (2%) of sandwiches or rolls prepared or stored in an area deemed
        visually dirty by the sampling officer (Table 7) meant that statistically significant
        associations could not be drawn between the microbiological quality of the
        sandwiches or rolls and the cleanliness of the surfaces on which they were prepared.

•   Most chicken sandwiches or rolls collected were made on request/at the time of service
    (93%) (Table 7) and were more likely to be of unsatisfactory microbiological quality
    (27%) than those made in advance (11%), although this was not statistically significant.

•   No significant difference was found between the microbiological quality of
    sandwiches/roll samples containing fillings displayed or stored above 8°C (28%)
    compared to those containing fillings that were stored at or below 8°C (25%) (Table 7).

•   Although not statistically significant, sandwiches/rolls containing fillings that were in the
    food service area for more than four hours were more likely be of unsatisfactory
    microbiological quality (33%) compared to those containing fillings that were in the food
    service area for four hours or less (24%) (Table 7).

•   Although not statistically significant, sandwiches/rolls containing fillings that were not
    covered were more likely be of unsatisfactory microbiological quality (30%) compared to
    those containing fillings that were covered (21%) (Table 7).

•   Although not statistically significant, sandwiches/rolls containing fillings that were not
    protected by a display screen were more likely be of unsatisfactory microbiological
    quality (41%) compared to those containing fillings that were protected by a display
    screen (25%) (Table 7).


Serving sandwiches/rolls
Approximately half (48%) of the sandwich bars visited had staff that served sandwiches or
rolls using only bare hands (Table 7).

•   Sandwiches/rolls served by staff using only bare hands, bare hands with other utensils
    (dedicated or shared) or serving methods (29%) were more likely to be of unsatisfactory
    microbiological quality compared to those served by staff using gloves, utensils or
    another serving method (20%) (Table 7). The different ways that staff used to serve
    sandwiches or rolls had no significant effect on the microbiological quality of the food
    with regard to samples of an unsatisfactory microbiological quality (Table 7).

There is no legal requirement to label sandwiches or rolls that are not pre-packed and over
three-quarters (78%) of sandwiches or rolls collected had no product date (Table 7), of which
most were made on request/at the time of service (95%; 333/351).

•   Significantly more sandwiches or rolls served with no product date were of unsatisfactory
    microbiological quality (28%) compared to those with a consume by date (19%) or use
    by date (10%) (P<0.05) (Table 7).




                                                                                               8
Table 7 Details of 449 chicken sandwiches/rolls collected from sandwich bars
Sandwich/Roll details              Number of   (%)           Unsatisfactory    (%)
                                   premises                  samples
Chicken sandwich/roll contained:
No spices/spiced ingredients     404           (90%)         107               (26%)
Spices/spiced ingredients        45            (10%)         7                 (16%)

No mayonnaise                      367         (82%)         97                (26%)
Mayonnaise                         82          (18%)         17                (21%)

Preparation of sandwich/roll
On request/at time of service      415         (93%)         110               (27%)
In advance                         28          (6%)          3                 (11%)
Not recorded                       6           (1%)          1                 (17%)

Preparation/storage area clean     429         (96%)         110               (26%)
Not clean                          9           (2%)          3                 (33%)
Not recorded                       11          (2%)          1                 (9%)

Storage/display of sandwich/roll fillings
Temperature 8°C                     378        (84%)         96                (25%)
Temperature >8°C                    58         (13%)         16                (28%)
Temperature not recorded            13         (3%)          2                 (15%)

Time in food service area
  4 hours                          297         (66%)         72                (24%)
> 4 hours                          46          (10%)         15                (33%)
Not known                          106         (24%)         27                (25%)

Sandwich/roll fillings
Covered                            252         (56%)         53                (21%)
Not covered                        174         (39%)         52                (30%)
Not recorded                       23          (5%)          9                 (39%)

Protected by display screen        304         (68%)         77                (25%)
No display screen present          17          (4%)          7                 (41%)
Not applicable                     112         (24%)         23                (20%)
Not recorded                       16          (4%)          7                 (44%)

Serving sandwich/roll
Bare hand only                     217         (48%)         62                (29%)
Bare hand & dedicated utensil      30          (7%)          9                 (30%)
Bare hand & shared utensil         14          (3%)          4                 (29%)
Bare hand & other serving          3           (<1%)         2                 (67%)
method
Glove/protected hand only          96          (21%)         21                (22%)
Gloved hand & shared utensil       4           (1%)          0
Dedicated serving utensil only     42          (10%)         7                 (17%)
Shared serving utensil only        9           (2%)          2                 (22%)
Other method (paper, pre-          29          (7%)          7                 (24%)
wrapped in clingfilm)
Not recorded                       5           (1%)          0

Product date present
Consume by date                    21          (5%)          4                 (19%)
Use by date                        38          (8%)          4                 (10%)
No date                            351         (78%)         97                (28%)
Not recorded                       39          (9%)          9                 (23%)




Takeaway and sandwich bar premises in relation to microbiological quality

Food Hygiene Inspections
Food hygiene inspections of premises are carried out to assess hygiene and compliance
with public health protection aspects of food law32. 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


                                                                                       9
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 years32. Most sandwich bars (68%) and take-aways
(41%) visited had an Inspection Rating Category C (Table 8), and these had proportionally
fewer unsatisfactory or unacceptable samples (18%) than premises rated B (20%) or A
(24%).

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 accordingly32. Scores range from 0 (very few at risk) to 15 (a substantial number at
risk).

•   The majority of sandwich bars (84%) and take-aways (88%) visited had consumer at risk
    scores of 5, indicative of local outlets (Table 8), and these had significantly more
    unsatisfactory or unacceptable samples (20%) compared to those from larger
    businesses (consumer at risk scores of 10 to 15; 15%) (P<0.001).

Inspectors assess the food business management of food hygiene and score accordingly32.
Confidence in management scores range from 0 (highly confident) to 30 (no confidence).
Most sandwich bars (51%) and take-aways (50%) visited had a confidence in management
score 10 (some confidence) (Table 8), and these had proportionally fewer unsatisfactory or
unacceptable samples (18%) than those rated 20 or above (little or no confidence) (22%).


Hazard analysis system
Approximately a fifth (21%) of premises had a documented hazard analysis system in place,
and a further 30% had an undocumented hazard analysis system in place (Table 8).
However, 44% of premises did not have a hazard analysis system in place and in the
remaining 5%, this was not recorded.

•   Significantly more take-aways (58%) had no hazard analysis system in place compared
    to sandwich bars visited (28%) (P<0.00001) (Table 8).

•   Significantly more unsatisfactory sandwiches/roll samples were collected from sandwich
    bars where there was no hazard analysis system in place (28%) compared to those
    where a documented hazard analysis system was in place (16%) (P<0.05) (Table 8).

•   Although not statistically significant, cooked rice samples collected from take-aways
    where there was no hazard analysis system in place were more likely to be of
    unsatisfactory or unacceptable microbiological quality (15%) compared to those where a
    documented hazard analysis was in place (12%) (Table 8).




                                                                                          10
Table 8 Details of Food Hygiene Inspections of Take-aways and Sandwich Bars

Premises details         Take-aways Unsatisfactory/   Sandwich bars Unsatisfactory   Total no.      Unsatisfactory/
                         (n=508)     unacceptable     (n=449)       samples          premises       unacceptable
                                    samples                                          (n=957)        samples
Inspection rating category
A                        93 (18%)     21 (32%)        26    (6%)     9     (35%)     119   (12%)       28   (24%)
B                        179 (35%)    25 (14%)        81    (18%)    26    (32%)     260   (27%)       51   (20%)
C                        209 (41%)    18 (9%)         306   (68%)    74    (24%)     515   (54%)       92   (18%)
D                        0                            4     (1%)     1     (25%)     4     (0.5%)      1    (25%)
E                        0                            1     (<1%)                    1     (<1%)
F                        0                            3     (1%)     1     (33%)     3     (0.5%)      1    (33%)
Not recorded             27 (6%)      2 (7%)          28    (6%)     5     (18%)     55    (6%)        7    (13%)

Consumer at risk score
0                         7     (2%)    1 (14%)       2     (<1%)                    9     (1%)        1 (11%)
5                         446   (88%)   61 (14%)      377   (84%)    101 (27%)       823   (86%)       162 (20%)
10                        22    (4%)    1 (10%)       37    (8%)     8 (22%)         59    (6%)        9 (15%)
15                        1     (<1%)                 0                              1     (<1%)
Not recorded              32    (6%)    3    (9%)     33    (8%)     5    (15%)      65    (7%)        8    (12%)

Confidence in management score
0                     0                               9     (2%)     1    (33%)      9     (1%)        1    (11%)
5                     53 (10%)          4    (8%)     111   (25%)    24   (22%)      164   (17%)       28   (17%)
10                    253 (50%)         25   (10%)    228   (51%)    65   (29%)      481   (50%)       90   (19%)
20                    153 (30%)         32   (21%)    56    (13%)    17   (30%)      209   (22%)       49   (24%)
30                    21 (4%)           2    (10%)    4     (<1%)                    25    (3%)        2    (8%)
Not recorded          28 (6%)           3    (11%)    41    (9%)     7    (17%)      69    (7%)        10   (14%)

Hazard analysis
In place & documented     43 (8%)       5 (12%)       155   (35%)    25    (16%)     198 (21%)         30 (15%)
In place &                143 (28%)     11 (8%)       149   (33%)    47    (32%)     292 (30%)         58 (20%)
undocumented
Not in place              293 (58%)     44 (15%)      125   (28%)    35    (28%)     418 (44%)         79 (19%)
Not recorded              29 (6%)       6 (21%)       20    (4%)     7     (35%)     49 (5%)           13 (27%)

Management food hygiene training
Received training and    394 (77%)      41 (10%)      382   (85%)    96    (25%)     776 (81%)         137 (18%)
attended a:
  basic 6 hour course    358 (91%)      35 (10%)      309   (81%)    79    (26%)     667   (86%)       114 (17%)
  intermediate course    13 (3%)        1 (8%)        41    (11%)    7     (17%)     54    (7%)        8 (15%)
  advanced course        2   (0.5%)     1 (50%)       5     (1%)     1     (20%)     7     (1%)        2 (28%)
  other recognised       2   (0.5%)                   13    (3%)     4     (31%)     15    (2%)        4 (27%)
  course
  training not specified 19 (5%)        4 (21%)       13    (3%)     5     (38%)     32 (4%)           9 (28%)
No training              80 (16%)       17 (21%)      42    (9%)     8     (19%)     122 (13%)         25 (21%)
Not recorded             34 (7%)        8 (24%)       25    (6%)     10    (40%)     59 (6%)           18 (31%)

Number food handlers employed
<4                    310 (61%)         39   (13%)    185   (41%)    47    (25%)     495   (52%)       86   (17%)
4 - <8                155 (30%)         17   (11%)    179   (40%)    47    (26%)     334   (35%)       64   (19%)
8 - < 12              19 (4%)           4    (21%)    37    (8%)     9    (24%)      56    (6%)        13   (23%)
12 - <20              5    (1%)         1    (20%)    17    (4%)     4     (24%)     22    (2%)        5    (23%)
 20                   1    (<1%)                      6     (1%)                     7     (<1%)
Not recorded          18 (4%)           5    (28%)    25    (6%)     7    (28%)      44    (5%)        12 (27%)

Hand washing facilities
Accessible & available    463 (91%)     61   (13%)    403   (90%)    108 (27%)       866 (90%)         169 (20%)
for use
   And used               254   (55%)   30   (12%)    224   (56%)    53   (24%)      478   (55%)       83   (17%)
   & not used             82    (18%)   7    (9%)     62    (15%)    18   (29%)      144   (17%)       25   (15%)
   Use not recorded       127   (27%)   21   (17%)    117   (29%)    37   (32%)      244   (28%)       58   (24%)
Not accessible &          21    (4%)    2    (10%)    16    (4%)     2    (13%)      37    (4%)        4    (11%)
available for use
Not recorded              24    (5%)    3    (13%)    30    (6%)     4    (13%)      54    (6%)        7    (13%)



Food hygiene training
In the majority of premises (81%) the manager had received some form of food hygiene
training, and most (86%) had attended a six-hour course (Table 8).



                                                                                                                11
•   Significantly more sandwich bars (85%) had managers that had received food hygiene
    training compared to those managers of take-aways (77%) (P<0.01) (Table 8).

•   Significantly more unsatisfactory and unacceptable cooked rice samples were collected
    from take-aways where the manager had received no food hygiene training (21%)
    compared with those take-aways where the manager had received food hygiene training
    (10%) (P<0.01) (Table 8).

•   Significantly, where the manager of the premises had received some form of food
    hygiene training, food safety procedures such as the hazard analysis system were more
    likely to be in place (P<0.0001) (Table 9).

•   Significantly, managers of sandwich bars that had received some form of food hygiene
    training were more likely to have hazard analysis systems in place, either documented or
    undocumented, in premises compared to managers of take-aways that had received
    food hygiene training (P<0.00001) (Table 9).

Table 9 Hazard Analysis System Procedures in relationship to Management Food Hygiene
Training

Premises details                             Food hygiene training received by manager
                                             Yes                              No
Hazard analysis in place & documented
Take-away                                    41/166     (25%)                   2/17    (12%)
Sandwich bar                                 146/282    (52%)                   8/15    (53%)
Hazard analysis in place
Take-away                                    166/394    (42%)                   18/80   (23%)
Sandwich bar                                 282/382    (74%)                   15/41   (37%)



Food Handlers & hand washing facilities
Most premises (87%) visited employed less than eight food handlers (Table 10), indicating
the small and medium size enterprise nature of take-aways and sandwich bars. The
proportion of food premises employing from less than 4 to over 20 food handlers that had
received food hygiene training, ranged from 95% to 100% (Table 10).

Table 10 Number of Foods Handlers employed per premises that have received food hygiene
training

No. food handlers      Proportion of premises with food handlers that have received food hygiene training
employed /
premises               Take-aways                      Sandwich bars                    Total no. premises
                       (n=508)                         (n=449)                          (n=957)
<4                     293/310          (95%)          179/185         (97%)            472/495      (95%)
4 - <8                 149/155          (96%)          172/179         (96%)            321/334      (96%)
8 - <12                18/19            (95%           36/37           (97%)            54/56        (96%)
12 - <20               5/5              (100%)         17/17           (100%)           22/22        (100%)
  20                   1/1              (100%)         6/6             (100%)           7/7          (100%)
Not recorded           3/18             (17%)          2/25            (8%)             5/43         (12%)


•   The majority (90%) of premises had hand washing facilities accessible and available for
    use, although only over half (55%) were used as judged by the sampling officer (Table
    8).




                                                                                                              12
Discussion
This study has shown that most (86%) cooked rice collected from take-aways in the UK were
of satisfactory/acceptable microbiological quality.      However 10% were classed as
unsatisfactory according to published guidelines41. A further 3% of cooked rice samples
were of unacceptable microbiological quality. High ACC, B. cereus and other Bacillus spp.,
and E. coli levels may indicate that the cooking process was inadequate, that post-cooking
contamination had occurred, that the length of time and temperature control in storage
facilities was inadequate to prevent bacterial growth, or that a combination of these factors
was involved. More cooked rice samples from Indian premises were of unsatisfactory or
unacceptable microbiological quality (29%) compared to Chinese premises (4%), and may
reflect the traditionally different rice storage and reheating practices. Contamination may
also have been introduced from spices added to rice, as these are often heavily
contaminated with Bacillus spores42,43.

A LACOTS/PHLS study carried out in 1995 reported that the degree of contamination in
cooked rice with B. cereus and other Bacillus spp. was directly related to the temperature of
storage, and length of time the rice was kept before serving. Evidence from the present
study also indicates that pre-cooked rice should not be stored at ambient temperature for
more than four hours as this would allow heat resistant spores of B. cereus present in pre-
cooked stored rice to germinate and increase to high levels. Although the final heating step
at the point-of-sale would reduce the levels of microorganisms present in rice it would not
inactivate the B. cereus emetic toxin if present. Therefore, it must be assumed that high
counts of B. cereus at 105 cfu/g or more in pre-cooked rice represent a potential risk to
health. Reheating rice before serving will not protect the consumers from heat stable toxins
that were produced previously. Data on the direct relationship between the length of storage
at ambient temperature and the degree of contamination with Bacillus spp. and B. cereus in
cooked rice has been used in conducting hazard analyses of restaurants and take-away
establishments44.

Evidence from England and Wales and other countries indicates that food poisoning
attributed to enterotoxigenic B. cereus continues to occur from consumption of cooked rice.
During 1992 to 2000 in England and Wales there were 12 reported outbreaks where 53
people were affected after consuming rice purchased from Chinese or Indian take-aways
(CDSC, unpublished). The Bacillus spp. predominantly isolated from cooked rice at high
levels ( 104 cfu/g) in the present study was B. subtilis, which has also been associated with
outbreaks of food poisoning where people were affected after consuming rice, but the
incidence is low (2 reported outbreaks between 1992 to 2000; CDSC unpublished). Rice,
and also spices, of good microbiological quality should be used when cooking rice to reduce
the risk of food poisoning from consuming this product. Temperature and storage conditions
under which rice is prepared, cooked and served in take-aways is also still an area of
concern. As large numbers of enterotoxigenic B. cereus are required to cause food
poisoning (≥105 cfu/g) it is therefore essential that control measures should be directed at
preventing the germination and outgrowth of spores in cooked rice. Control measures should
include rapid cooling and ideally refrigeration of the cooked rice in closed containers. The
rice should not be stored for long periods or produced in bulk quantities.

Chicken sandwiches or rolls (without salad) made on the premises in sandwich bars in the
UK were also examined in the present study. Although most (75%) sandwiches or rolls
collected were of satisfactory/acceptable microbiological quality, a quarter (25%) were
classed as unsatisfactory according to published guidelines41.                 High ACC,
Enterobacteriaceae, E. coli, an indicator of faecal contamination, and Staph. aureus levels
may indicate that the temperature of sandwich fillings in storage or on display was




                                                                                          13
inadequate to prevent bacterial growth, and/or that contamination had occurred during
preparation of the filling and sandwich assembly.

This study underlines the fact that sandwiches are a perishable food product. High
standards of hygiene must be observed in their preparation. The BSA food hygiene
guidance for sandwich bars22 advises that food ingredients must be of acceptable
microbiological quality; storage and display temperatures must be correct ( 8°C); there
should be separation of low/high risk areas; direct handling of high risk foods and fillings
must be minimised; frequent hand washing by food handlers must be encouraged to
minimise contamination risks; and there should be effective cleaning procedures.

The Audit Commission noted in their survey of food premises in England and Wales that lack
of adequate hand washing facilities was one of the commonest high risk factors in food
premises45. There should always be adequate sanitary provision, with hand washing
facilities for the staff as required by the Food Safety (General Food Hygiene) Regulations
19955. Although the majority of premises visited in this study did have hand washing
facilities, only approximately half were used. This is entirely inexcusable suggesting that
food handlers are not aware of the importance of hand washing, and/or that proper methods
of hand washing were not used.

Evidence from this study suggests that the lower microbiological quality of food purchased
from some take-aways and sandwich bars may reflect differences with those premises that
had a hazard analysis system present. The lower microbiological quality of food purchased
from some take-aways may also reflect differences with those premises that had
management food hygiene training. Management holds the key to the delivery of food
hygiene training as well as the implementation of the hygiene practices recommended by
such training46. Effective training of all food handlers and managers, may lead to an
improvement in hygienic practices and implementing a hazard analysis system in take-
aways and sandwich bars.



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 examinations. Thanks are
extended to David Lock at LACOTS for co-ordinating the participation of Environmental
Health Officers (EHOs), and to Lilian Hucklesby for entering the data. The laboratory work
was funded by the Food Standards Agency.




                                                                                        14
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                                                                                                 16
Annex 1:         Participating PHLS Groups, Laboratories and Local Authority Food
                 Liaison Groups and number of samples

  Table 1a. Participating PHLS Groups, Public Health Laboratories and number of samples
    PHLS group                 Public Health Laboratory     Sample Type           Number of samples
    East                       Chelmsford                   Cooked rice           20
                               Luton                        Cooked rice           35
                               Norwich                      Chicken sandwiches    34
    London & South east        Ashford                      Cooked rice           38
                               Brighton                     Chicken sandwiches    24
                               London FWE Lab1              Chicken sandwiches    30
                               Reading                      Cooked rice           29
                               WEMS2                        Chicken sandwiches    31
    Midlands                   Birmingham                   Cooked rice           30
                               Coventry                     Chicken sandwiches    30
                               Shrewsbury                   Chicken sandwiches    11
                               Stoke                        Cooked rice           29
    North west                 Chester                      Cooked rice           43
                               Preston                      Chicken sandwiches    38
    North                      Hull                         Chicken sandwiches    32
                               Leeds                        Chicken sandwiches    20
                               Middlesbrough                Cooked rice           33
                               Newcastle                    Cooked rice           37
    South West                 Bristol                      Chicken sandwiches    26
                               Exeter                       Chicken sandwiches    27
                               Hereford                     Cooked rice           28
                               Plymouth                     Cooked rice           19
                               Lincoln                      Chicken sandwiches    30
                               Sheffield                    Cooked rice           30
    Wales                      Bangor                       Chicken sandwiches    37
                               Cardiff                      Cooked rice           27
                               Carmarthen                   Chicken sandwiches    28
                               Rhyl                         Cooked rice           19
    Total                                                                         837
      1, London Food, Water & Environmental Unit, CPHL
      2, Wessex Environmental Microbiological Services




            Table 1b. Participating Non-PHLS Laboratories and number of samples
    Non-Public Health Laboratory                          Sample Type            Number of samples*
    Belfast City Hospital                                 Chicken sandwiches     13
    Dundee Public Analyst                                 Cooked rice            15
    Edinburgh City Council                                Cooked rice            16
    Glasgow Scientific Services                           Chicken sandwiches     46
    Worcester Scientific Services                         Cooked rice            20
                                                          Chicken sandwiches     10
    Total                                                                        120




                                                                                                 17
             Table 1c. Local Authority Food Liaison Groups and number of samples

Local Authority Food Liaison Group                               Number of samples
Berkshire Food Co-ordinating Group                               12
Cambridge Food Liaison Group                                     8
Cheshire Food Liaison Group                                      25
Cornwall CEHOS Food Sub-Group                                    5
Cumbria IEHO Food Safety Group                                   24
Derbyshire Food Liaison Group                                    15
Devon Food Safety Group                                          29
Dorset Food Group                                                9
East Sussex Food Liaison Group                                   8
Essex Food Group                                                 20
Greater Manchester Food Liaison Group                            16
Hampshire & Isle Of Wight Food Advisory Group                    20
Hereford & Worcester CEHOS Food Working Group                    58
Herts & Beds IEHO And Chief Officers Food Group                  29
Humberside Food Liaison Group                                    32
IEHO Buckinghamshire Branch Food Group                           12
Kent Food Technical Group                                        38
Lancashire Assn Of CEHOS, Food Officer Group                     18
LFCG1 North East Sector                                          8
LFCG South East Sector                                           8
LFCG South West Sector                                           4
LFCG North West Sector                                           10
Lincolnshire Co-ordinating Group                                 15
Merseyside Food Sub-Group                                        15
North Yorkshire CEHOS Group                                      31
Northamptonshire                                                 16
Northern Ireland Food Group                                      13
Northumberland Food Safety Group                                 6
Norfolk Food Liaison Group                                       18
Nottingham District Food Group                                   15
Oxfordshire CC Food Sub-Group                                    8
Scottish Food Co-ordinating Committee                            77
Shropshire Food Liaison Group                                    5
Somerset Food Liaison Group                                      12
South Yorkshire Food Forum                                       15
Staffordshire Food Safety Group                                  31
Suffolk Food Liaison Group                                       4
Surrey Food Liaison Group                                        7
Tees Valley Food Safety Group                                    20
Tyne & Wear Food Control Group                                   30
Wales North Group                                                59
Wales South East Group                                           23
Wales South West Group                                           35
Warwickshire Food Liaison Group                                  15
West Midlands Food Liaison Group (inc. Black Country)            36
West of England Food Liaison Group                               11
West Sussex Food Liaison Group                                   11
West Yorkshire Principal Food Officers Group                     3
Wiltshire Food Group                                             18
Total                                                            957
   1, London Food Co-ordinating Group




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