.European Commission Co-ordinated Programme for the Official Control of
Foodstuffs for 2002: Microbiological Examination of Pre-cut Fruit, Sprouted Seeds,
and Unpasteurised Fruit and Vegetable Juices from Production and Retail Premises
in the United Kingdom
CL Little and RT Mitchell
Health Protection Agency, Environmental Surveillance Unit, CDSC, 61 Colindale Avenue,
London NW9 5EQ
On behalf of the Food Standards Agency, Local Authorities Co-ordinated Body of Regulatory
Services, and the Public Health Laboratory Service.
Summary
The European Commission Recommendation 2002/66/EC required Member
States to carry out a co-ordinated programme in 2002 of sampling and testing ready-toeat pre-cut fruits, vegetables, sprouted seeds, and unpasteurised fruit and vegetable juices
from establishments of production and retail for Salmonella spp., Escherichia coli O157,
and Listeria monocytogenes, and to verify the application of Hazard Analysis and Critical
Control Points (HACCP) procedures by food operators.
In the UK examination of ready-to-eat pre-cut fruit, sprouted seeds, and
unpasteurised fruit and vegetable juices and comparison with PHLS Microbiological
Guidelines
revealed
that
the
satisfactory/acceptable quality.
vast
majority
(99%;
2075/2096)
were
of
However, two (0.1%) samples (melon medley;
beansprouts) were of unacceptable microbiological quality due to the presence of L.
monocytogenes in excess of 102 cfu/g while a further 19 (0.9%) were unsatisfactory due
to Escherichia coli levels in the range of 102 to 106 cfu/g. Salmonella spp. and E. coli
O157 were not detected in any of the samples examined. A hazard analysis system was
in place in most (85%) production and retail premises visited, of which 80% had
documented systems, and most managers (83%) had received some form of food hygiene
training.
The findings from the UK contribution to the EU study concur with previous UK
LACORS/PHLS studies on prepared ready-to-eat salad vegetables in that most bacteria
of concern with regard to human health are relatively rare in raw ready-to-eat produce
indicating that overall conditions during pre- and post-harvest operations were good.
1
Introduction
The recognition of the public health benefits of consumption of fresh fruit and vegetables,
together with a marked increase in the year-round availability of fresh produce from a
global market, has contributed to the substantial increase in consumption of fresh fruits
and vegetables in the UK over the last decade1. In addition, ready-to-eat fruit and
vegetables requiring minimal or no further processing prior to consumption have seen
rapid year-on-year growth since their introduction due no doubt to their convenience to
the consumer2.
Raw ready-to-eat fruit and vegetables have been implicated as vehicles for transmission
of infectious microorganisms particularly in Europe, United States, Canada and Japan,
although the frequency of foodborne outbreaks of gastrointestinal illness associated with
fruit and vegetables appears to be low compared to products of animal origin3,4.
Nonetheless, the EC Scientific Committee on Food (SCF) report on a risk profile on the
microbiological contamination of fruits and vegetables eaten raw notes that foodborne
illnesses associated with fruit and vegetables in many countries appear to be increasing.
The reason for this is not clear but factors include improved reporting, increased
consumption, new commodities and changes in production practices3. The large outbreak
of Escherichia coli O157 in Japan in 1996 linked to sprouted radish illustrates the
potential for serious public health problems arising from the contamination of ready-toeat fruit and vegetables5.
Guidance documents have been developed to help producers and retailers minimise
microbiological hazards for fresh fruit and vegetables. They incorporate control strategies
based on the principles of the Hazard Analysis Critical Control Point system (HACCP),
good handling practices, and good hygienic practices6-10. Food businesses must apply the
hazard analysis principles in their own premises, which also must be kept clean and
maintained in good repair and condition11. Legislation also requires proprietors to ensure
that food handlers are appropriately supervised and instructed and/or trained in food
hygiene11. Nevertheless, cross-contamination and infected food handlers were the two
contributory factors most commonly reported in fruit and vegetable outbreaks of
2
infection in England and Wales4, highlighting the importance of training food handlers in
good hygiene practices.
A number of ready-to-eat commodities of special concern were identified by the SCF.
These include sprouted seeds and fruit juices that have not undergone a treatment to kill
or remove pathogenic microorganisms3.
Sprouted seeds exhibit a unique hazard
potential, since the germination stage breaches the inhibitory barrier of the seed coat,
allowing pathogens, which may be present to grow on nutrients from the sprouted plant.
No effective decontamination process has been identified that will substantially reduce or
eliminate contaminating pathogens. Nevertheless, by washing seeds with chlorinated
water a degree of reduction can be achieved12,13. Historically, unpasteurised juice had
been considered non-hazardous because of its acidic properties. However, the acid
tolerance of E. coli O157 and Salmonella spp. is of particular concern, as it allows them
to survive in foods, such as fruit juices, that might seem unlikely. The acidity of fruit
juices prevents the multiplication of organisms, but contamination at low levels with
pathogens whose infective dose is low, such as E. coli O157, can lead to outbreaks13,14.
The SCF recommended that there is a need to carry out further studies on the
microbiological status of various pathogens in/on raw fruit and vegetables3.
The
European Commission (EC) Recommendation 2002/66/EC15, made under Article 14(3)
of the Official Control of Foodstuffs Directive 89/397/EEC16, therefore required Member
States to carry out a co-ordinated programme of sampling and testing pre-cut fruits,
vegetables, sprouted seeds, and unpasteurised fruit and vegetable juices from
establishments of production and retail for Salmonella spp., E. coli O157, and Listeria
monocytogenes to assess their microbiological safety, and to verify the application of
HACCP procedures by food operators. In addition, Enterobacteriaceae, E. coli and other
Listeria spp. were enumerated to obtain an indication of hygiene and levels of
contamination.
In the UK, the programme was guided by the Food Standards Agency, and co-ordinated,
on behalf of the Agency, by the Public Health Laboratory Service (PHLS) and the Local
Authorities Co-ordinators of Regulatory Services (LACORS), in collaboration with
3
Environmental Health Departments and Official Food Control Laboratories in England,
Wales, Scotland, and Northern Ireland. The Food Standards Agency submitted the UK
information to the European Commission. Reported here is a more detailed analysis of
the UK results from the 2002 EC co-ordinated food sampling programme.
Materials and Methods
Sample Collection
Pre-cut fruit, sprouted seeds, and unpasteurised fruit and vegetable juices collected from
production establishments (factories, packing centres) and retail premises were examined
in PHLS and non-PHLS laboratories in the UK between 1 July and 31 December 2002
according to a standardised protocol. Single or mixed pre-cut ready-to-eat fruit, prepared
sprouted seeds, and unpasteurised fruit and vegetable juices included in the study were
those that could be consumed without any cooking or further preparation by the
consumer. Pre-cut fruit, sprouted seeds, and unpasteurised juice samples (~100g/ml)
were collected by staff from local Environmental Health Departments and were
transported to the laboratory in accordance with the Food Safety Act 1990, Code of
Practice No 717 and advice provided in the LACORS guidance on microbiological food
sampling18.
Information on the samples and premises was obtained by observation and enquiry and
recorded on a standard proforma. This included information on the premises with regard
to documentation of a hazard analysis system, presence of an approved voluntary
industry guide to good hygiene practice6,7, the level of food hygiene training received by
the manager, and food safety legislation. Food hygiene inspections are carried out in a
way that focuses enforcement authority resources on premises presenting most risk to
consumers. To do this, food hygiene inspections are carried out in accordance with the
Food Safety Act 1990 Code of Practice No 919 which specifies that, amongst other
factors, the number of consumers at risk and confidence in management control systems
(including the application of HACCP based systems) should be assessed to produce a risk
rating of the premises. The risk rating determines the frequency of inspection and ranges
from Category A (highest risk, inspected at least every 6 months) to F (lowest risk,
4
inspected at least every 5 years). Consumer at risk scores range from 0 (very few) to 15
(substantial) and confidence in management ranges from 0 (high Confidence) to 30 (no
Confidence). Additional information collected on pre-cut fruit, sprouted seeds, and juices
included type, country of origin, product packaging, and display temperature.
Sample Examination
Enterobacteriaceae, E. coli, L. monocytogenes and other Listeria spp., Salmonella spp.,
and E. coli O157 were enumerated or detected in accordance with PHLS Standard
Microbiological Methods20-24.
Fruits are typically acidic, therefore to neutralise the
antibacterial effect of acid, for pre-cut fruit and unpasteurised fruit juice samples the
homogenate and pre-enrichment broths, containing bromocresol purple as a pH indicator,
were adjusted to pH 6.8 using 1N NaOH. L. monocytogenes at levels at 102 cfu/g or
more were sent to the Food Safety Microbiology Laboratory (FSML), CPHL for further
characterisation. Microbiological results were compared to the PHLS Guidelines for the
microbiological quality of some ready-to-eat foods sampled at the point of sale (Table
1)25. Satisfactory results indicate good microbiological quality, acceptable results are an
index reflecting a borderline limit of microbiological quality, whereas unsatisfactory
results indicates that further sampling may be necessary and that environmental health
officers may wish to undertake a further inspection of the premises concerned to
determine whether hygiene practices for food production or handling are adequate or not.
An unacceptable microbiological result indicates that urgent attention is needed to locate
the source of the problem. There are no guidelines for Enterobacteriaceae in fresh fruit
and vegetables as these products often carry high levels of these organisms as part of
their normal flora25.
Table 1. PHLS guidelines for the microbiological quality of some ready-to-eat foods
sampled at the point of sale: Key to classification for fresh fruit and vegetables25
Criterion
Escherichia coli
Listeria spp. (Total)
Listeria monocytogenes
Salmonella spp.
Escherichia coli O157
Microbiological quality (cfu per gram/ml unless stated)
Satisfactory
Acceptable
Unsatisfactory
<20
<20
<20
Not detected in 25g/ml
Not detected in 25g/ml
20 - <102
20 - <102
20 - <102
102
102
N/A
Unacceptable/
potentially
hazardous
N/A*
N/A
102
Detected in 25g/ml
Detected in 25g/ml
*, N/A, Not applicable
5
Results
Forty-five Local Authority Food Liaison Groups participated in this study and 248 Local
Authorities submitted samples.
A total of 2096 pre-cut fruit, sprouted seeds, and
unpasteurised fruit and vegetable juice samples were examined by 32 laboratories (24
Public Health Laboratories (PHLS) from all 8 PHLS Groups; 8 non-PHLS) in England,
Wales, Scotland and Northern Ireland. A further 11 samples did not fit the criteria
described in the study protocol and were not included in the analysis.
Microorganisms isolated from open pre-cut ready-to-eat fruit, prepared sprouted seeds,
and unpasteurised juices
Salmonella spp. and E. coli O157 were not detected in any of the pre-cut fruit, sprouted
seeds, or unpasteurised fruit and vegetable juice samples examined (Table 2).
Total Listeria spp. (including L. monocytogenes) were detected in 9% (86/997), 8%
(66/808), and 0.7% (2/291) of pre-cut fruit, sprouted seeds, and unpasteurised juice
samples examined, respectively and were present at 102 cfu/g or more in 0.1% (1) of precut fruit and 0.1% (1) of sprouted seeds samples (Table 2).
L. monocytogenes was detected in 8% (78/997), 3% (28/808), and 0.7% (2/291) of precut fruit, sprouted seeds, and unpasteurised juice samples examined, respectively and was
present at 102 cfu/g or more in 0.1% (1; 260 cfu/g) of pre-cut fruit and 0.1% (1; 100
cfu/g) of sprouted seeds samples (Table 2). The L. monocytogenes isolates in excess of
102 cfu/g were L. monocytogenes serotype NT (non-typeable).
E. coli was present in 0.3% (3/997), 4% (32/808), and 0.3% (1/291) of pre-cut fruit,
sprouted seeds, and unpasteurised juice samples examined, respectively and was present
at 102 cfu/g or more in 0.3% (3) of pre-cut fruit and 2% (16) of sprouted seeds samples
(Table 2).
Enterobacteriaceae were present in 60% (594/997), 95% (765/808), and 27% (78/291) of
pre-cut fruit, sprouted seeds, and unpasteurised juice samples examined, respectively and
6
were present at 104 cfu/g or more in 11% (111), 84% (676), and 4% (12) of the pre-cut
fruit, sprouted seeds, and unpasteurised juice samples, respectively (Table 2). There are
however no EU or US guidelines for Enterobacteriaceae in fresh vegetables or fruit as
these products often carry high levels of these organisms as part of their normal flora26.
Table 2. Microbiological results of 2096 pre-cut fruits, sprouted seeds, and
unpasteurised fruit and vegetables juices
ND*
in
25g
Pre-cut fruit (n=997)
Enterobacteriaceae
Escherichia coli
Listeria spp. (total)
-L. monocytogenes
Salmonella spp.
Escherichia coli O157
Sprouted seeds
(n=808)
Enterobacteriaceae
Escherichia coli
Listeria spp. (total)
-L. monocytogenes
Salmonella spp.
Escherichia coli O157
Unpasteurised fruit
and vegetable juices
(n=291)
Enterobacteriaceae
Escherichia coli
Listeria spp. (total)
-L. monocytogenes
Salmonella spp.
Escherichia coli O157
911
997
997
728
808
808
289
291
291
D§
in
25g
86
78
0
0
66
28
0
0
2
2
0
0
cfu/g or ml
<10/
<20
10/20
-<102
102 <103
103 <104
104 <105
105 <106
106 <107
107
NE¶
396a
994b
84b
76 b
191
0
1
1
160
2
1
1
132
0
55
1
40
9
7
7
38a
776b
9
16
17
11
1
1
63
2
146
1
298
2
128
104
5
28
8
27b
213a
289b
2b
2b
30
1
14
6
5
1
2
1
*ND; Not detected; §D, Detected; ¶NE, Not examined (full set of microbiological parameters not performed on sample due to
insufficient sample collected)
a, lower limit of detection 10 cfu/g; b, lower limit of detection 20 cfu/g
Microbiological quality of pre-cut ready-to-eat fruit, prepared sprouted seeds, and
unpasteurised juices
Based on the PHLS microbiological guidelines for some ready-to-eat foods at the point of
sale (Table 1)25, 99.5% (992/997) of pre-cut fruit were satisfactory, 0.1% (1) were
acceptable, and 0.3% (3) were of unsatisfactory microbiological quality due to the
7
presence of E. coli in the range of 102 to 105 cfu/g. However, one (0.1%) sample (melon)
was of unacceptable microbiological quality due to the presence of L. monocytogenes at
260 cfu/g (Fig. 1).
Of the sprouted seeds examined, 96.1% (776/808) were satisfactory, 1.9% (16) were
acceptable, and 1.9% (16) were of unsatisfactory microbiological quality due to the
presence of E. coli in the range of 102 to 106 cfu/g. However, one (0.1%) sample
(beansprouts) was of unacceptable microbiological quality due to the presence of L.
monocytogenes at 100 cfu/g (Fig. 1).
Most (99.6%; 290/291) of the unpasteurised juices examined were satisfactory and 0.4%
(1) were of acceptable microbiological quality. None of the unpasteurised juice samples
were of unsatisfactory or unacceptable microbiological quality (Fig. 1).
Fig. 1 Microbiological quality of pre-cut fruit, sprouted seeds, and
unpasteurised juices
Satisfactory
Acceptable
Unsatisfactory
Unacceptable
0.0%
Unpasteurised juices
0.0%
0.4%
99.6%
0.1%
Sprouted seeds
1.9%
1.9%
96.1%
0.1%
Pre-cut fruit
0.3%
0.1%
99.5%
Samples (%)
8
Product and premises information
A major feature of the data is that almost all pre-cut fruit, sprouted seeds, and
unpasteurised fruit and vegetable juices (99%; 2075/2096) were of satisfactory or
acceptable microbiological quality. As there were so few samples of unsatisfactory or
unacceptable microbiological quality (1%) an association could not be found between
microbiological quality and the product information collected (presented below).
Pre-cut ready-to-eat fruit
Forty-five percent (449/997) of the samples collected consisted of a single type of fruit,
and 55% (548) consisted of mixed fruit types. The breakdown of samples (449) that
consisted of a single type of pre-cut fruit was: melon (42%; 189), pineapple (28%; 126),
grapes (8%; 36), apple pieces (5%; 25), and watermelon (3%; 15). Other samples (12%;
58) included mango, raspberries, strawberries, and orange pieces. Of the samples (548)
that consisted of mixed fruit types, 9% (50) consisted of two different fruit types, 23%
(127) of three fruit types, 37% (201) of four fruit types, 22% (119) of five fruit types, and
9% (47) of more than five fruit types. For <1% (4) of samples, this information was not
recorded.
Of the pre-cut fruit sampled (997), most (82%; 813) were pre-packed and 16% (161)
were open. For the remaining 23 (2%) of samples this information was not recorded.
Most pre-cut fruit (90%; 893) were stored or displayed at or below 8C, 7% (68) were
stored or displayed above 8C, and for the remaining samples (4%; 36) this information
was not recorded
Prepared sprouted seeds
Most (88%; 713/808) of the samples collected consisted of a single sprouted seed type,
and 12% (95) consisted of mixed sprouted seed types. The breakdown of samples (713)
that consisted of a single sprouted seed type was: beansprouts (55%; 388), salad cress
(24%; 171), mustard cress (9%; 65), mung beans (5%; 34), alfalfa sprouts (4%; 28),
sunflower sprouts (1%; 8), radish sprouts (1%; 6), aduki beans (<1%; 2), and chick pea
sprouts (<1%; 2). For 1% (9) of samples, this information was not recorded. Of the
9
samples (95) that consisted of mixed sprouted seeds, 63% (60) consisted of two different
sprouted seed types, 6% (6) of three sprouted seed types, 19% (18) of four sprouted seed
types, and 3% (3) of five sprouted seed types. For 9% (8) of samples, this information
was not recorded.
Of the sprouted seeds sampled (808), approximately two-thirds (64%; 512) were prepacked, 31% (253) were packed and unsealed, and 1% (10) was open. For the remaining
4% (33) of samples, this information was not recorded. Over a third (39%; 295/765) of
the packed sprouted seeds had preparation instructions on the label to rinse or wash in
water before eating or use, 12% (94) were labelled as washed and ready-to-eat, 6% (45)
had no preparation instructions, and for 43% (331) of samples, this information was not
recorded.
The majority (93%; 13/14) of sprouted seeds samples that were of
unsatisfactory or unacceptable microbiological quality had preparation instructions on the
label to rinse or wash in water before eating or use. Most sprouted seeds (72%; 581)
were stored or displayed at or below 8C, 23% (183) were stored or displayed above 8C,
and for the remaining samples (5%; 44) this information was not recorded.
Unpasteurised fruit and vegetable juices
Most (81%; 236/291) of the samples collected consisted of a single juice type, and 19%
(55) consisted of mixed juice types. The breakdown of samples (236) that consisted of a
single juice type was: orange (74%; 174), apple (11%; 27), carrot (4%; 9), grapefruit
(3%; 8), and tomato (1%; 3). Other samples (6%; 14) included mandarin, pineapple, and
cranberry. For <1% (1) of single juice type samples, this information was not recorded.
Of the samples (55) that consisted of mixed juice types, 44% (24) consisted of two
different juice types, 33% (18) of three juice types, 13% (7) of four juice types, 2% (1) of
five juice types, and 4% (2) of more than five juice types. For 4% (3) of samples, this
information was not recorded.
Of the unpasteurised juices sampled (291), over two-thirds (68%; 198) were bottled or in
a carton, 25% (72) were extracted and served at the point of sale, and for the remaining
7% (21) of samples, this information was not recorded. Most unpasteurised juices (68%;
10
198) were stored or displayed at or below 8C, 20% (59) were stored or displayed above
8C, and for the remaining samples (12%; 34) this information was not recorded. Almost
three-quarters of unpasteurised juices (73%; 211) were not labelled or advertised as being
unpasteurised, 16% (46) were and for 12% of samples, this information was not recorded.
Country of Origin
Of the 2096 pre-cut fruit, sprouted seeds, and unpasteurised juices sampled a third (33%;
689) were produced in the UK (Table 3). Fifteen percent (325) of samples were not of
UK origin, i.e. grown in other EU or Third countries. The country of origin was not
known for over half (52%; 1082) of the samples, of which eight were labelled as packed
in the UK.
Table 3. Country of origin of pre-cut fruit, sprouted seeds, and unpasteurised juices
collected (n=2096)
Country of Origin
Pre-cut fruit
UK
Other EU
- Belgium
- Denmark
- Germany
- Greece
- Ireland
- Italy
- Netherlands
- Spain
More than one country (EU &
Third country)
Third countries
- Brazil
- China
- Costa Rica
- Cuba
- Ghana
- Israel
- Ivory Coast
- South Africa
- USA
- Zimabwe
Not Known
- Packed in the UK
Total
174 (18%)
21 (2%)
1
Number of Samples (%)
Sprouted seeds Unpasteurised
juices
408 (50%)
107 (37%)
9
(1%)
15 (5%)
Total
689 (33%)
45 (2%)
1
3
2
7
1
1
10
253 (25%)
2
4
4
13 (2%)
6
14
(5%)
280 (13%)
2
1
155 (53%)
1082 (52%)
291
2096
28
1
19
1
2
38
6
68
3
549 (55%)
6
997
378 (47%)
2
808
11
Production method
Over three-quarters (79%; 1664/2096) of the samples collected were produced using
conventional farming methods, 6% (117) of samples were produced using organic
farming methods, and for 15% (315) of samples this information was not recorded (Table
4).
Table 4. Production method of pre-cut fruit, sprouted seeds, and unpasteurised juices
collected (n=2096)
Production Method
Conventional
841 (84%)
Number of Samples (%)
Sprouted seeds Unpasteurised
juices
612 (76%)
211 (73%)
Organic
16
77
(9%)
24
(8%)
117
(6%)
Not Known
140 (14%)
119
(15%)
56
(19%)
315
(15%)
Total
997
808
Pre-cut fruit
(2%)
291
Total
1664 (79%)
2096
Type of premises
Most (97%; 2036/2096) samples of pre-cut fruit, sprouted seeds, and unpasteurised juices
were collected from retail premises, of which over three-quarters (77%; 1579/2036) were
from supermarkets (Fig. 2). A small proportion of samples (3%; 60) were collected from
production establishments.
Fig. 2 Pre-cut fruit, sprouted seeds, and unpasteurised juices
collected from retail premises (n=2036)
Supermarket
77%
Greengrocer
8%
Not Recorded
1%
Delicatessen
1%
Health Food Shop
3%
Market Stall
Juice Bar 2%
1%
Coffee Bar
2%
Other
3%
Farm Shop
2%
12
Food Hygiene Inspections
Over half (55%; 1162) of the premises visited were categorised as Inspection Rating
Category C (inspected at least every 18 months) (Fig. 3). Most of the premises visited
were categorised in consumer at risk score 5 (few numbers of customers, 45%; 933) and
10 (intermediate numbers of customers, 41%; 866) (Fig. 4). Most of the premises visited
had a confidence in management score 5 (moderate confidence in management/control
systems, 44%; 931) and 10 (some confidence in management/control systems 31%; 654)
(Fig. 5).
Fig.3. Inspection Rating Category of premises (n=2096)
C
55%
D
13%
B
12%
A
3%
Not Recorded
7%
F
2%
E
8%
Fig.4. Consumers at Risk score of premises (n=2096)
15 (Substantial)
Not Recorded
0 (Very few)
5 (Few)
10 (Intermediate)
13
Fig.5. Confidence in management score of premises (n=2096)
30 (No confidence)
1%
Not Recorded
9%
0 (High confidence)
12%
20 (Little confidence)
3%
10 (Some
confidence)
31%
5 (Little confidence)
44%
Hazard Analysis System and Industry Guide to Good Hygiene Practice
Over two-thirds (68%; 1430/2096) of premises visited had a documented hazard analysis
system in place, and a further 17% (346) had an undocumented system in place (Table 5).
Nine percent (190) of premises had no hazard analysis system in place and for 6% (130)
of premises, this information was not recorded.
Forty-one percent of premises visited
had an approved voluntary industry guide to good hygiene practice (Table 5).
Food Hygiene Training
The majority of premises had managers that had received some form of food hygiene
training (83%; 1733/2096), 8% (170) had not and for 9% (193) of premises, this
information was not recorded (Table 5). Of those managers with food hygiene training,
approximately half (46%; 796) were trained to a basic level, but 27% (465) and 12%
(201) were trained to an intermediate or advanced Level, respectively. A further 6%
(111) had attended another recognised course (HACCP, in-house training), and in 9%
(160) the type of training was not specified (Table 5).
Significantly, where managers had received some form of food hygiene training, hazard
analysis systems were more likely to be in place and documented (82%) compared to
those managers that had not received training (32%) (P<0.00001) (Table 6).
14
Table 5. Hazard analysis systems and management food hygiene training in premises
Hazard analysis
In place & documented
In place &
undocumented
Not in place
Not recorded
Retail Premises (%)
(n=2036)
Production
establishments (%)
(n=60)
Total premises (%)
(n=2096)
1395
341
(68%)
(17%)
35
5
(58%)
(8%)
1430
346
(68%)
(17%)
184
116
(9%)
(6%)
6
14
(10%)
(23%)
190
130
(9%)
(6%)
40
(67%)
1733
(83%)
24
10
4
(60%)
(25%)
(10%)
796
465
201
111
(46%)
(27%)
(12%)
(6%)
2
6
14
(5%)
(10%)
(23%)
160
170
193
(9%)
(8%)
(9%)
15
26
19
(25%)
(43%)
(32%)
852
669
575
(41%)
(32%)
(27%)
Management food hygiene training
Received training and
1693 (83%)
attended a:
basic 6 hour course
772
(46%)
intermediate course
456
(27%)
advanced course
197
(12%)
other recognised
111
(6%)
course
training not specified
158
(9%)
No training
164
(8%)
Not recorded
179
(9%)
Industry Guide to good hygiene practice
Present
837
(41%)
Not present
643
(32%)
Not recorded
556
(27%)
Table 6. Hazard analysis in place and documented in relation to management food hygiene
training
Premises details
Food hygiene training
Yes
No
Hazard analysis in place and documented
1348/1649 (82%)
16/ 50
(32%)
<0.00001
Hazard analysis in place and undocumented
114/1649
(7%)
30/ 50
(60%)
<0.00001
Hazard analysis not in place
66/1733
(4%)
119/ 170 (70%)
<0.00001
P value
Significantly more managers from premises with a consumer at risk score of 0-5 (15%;
141/961) had received no food hygiene training compared to managers in premises
scoring 10 or above (2%; 20/952) (P <0.00001). In addition more managers of premises
with confidence scores of 20 and above (16%; 16/97) had received no food hygiene
training compared with those premises with confidence scores of 10 or less (8%;
142/1820) (P <0.01).
15
Discussion
This study has shown that the vast majority (99%) of pre-cut ready-to-eat fruit, sprouted
seeds, and unpasteurised fruit and vegetable juices sampled at production and retail
premises in the UK were of satisfactory/acceptable microbiological quality. Two (0.1%)
of the samples were unacceptable, and 19 (0.9%) were classified as unsatisfactory
according to published microbiological guidelines25. Unacceptable results were due to
the presence of L. monocytogenes at 102 cfu/g or more while unsatisfactory results were
due to E. coli levels in the range of 102 to 106 cfu/g. E. coli is a faecal organism and is an
environmental microorganism found in soil and water. Therefore, fruit and vegetables
may easily become contaminated with these bacteria. However, the absence of the
pathogens Salmonella spp. and E. coli O157 and the low incidence of E. coli (1.7%) and
L.monocytogenes (5%) associated with these products indicate that agricultural,
harvesting, hygiene and production practices were good overall. The findings from this
study concur with that of recent UK LACORS/PHLS microbiological studies on various
prepared ready-to-eat salad vegetables27-30 and the US FDA survey of domestic fresh
produce (salad vegetables and fruit)31, in that most bacteria of concern with regard to
human health are relatively rare in raw ready-to-eat produce. However, the FDA survey
of imported fresh produce undertaken in 199932 found that 4% of fresh produce were of
unacceptable microbiological quality due to the presence of salmonellas or Shigella spp.
and may reflect differences in conditions during pre- and post-harvest operations, and the
origin of the produce in question.
Vegetables carry a natural non-pathogenic epiphytic microflora, the majority of which
consists of Gram-negative bacteria belonging to either the Enterobacteriaceae or the
Pseudomonas group. The numbers of bacteria present will vary depending on seasonal
and climatic variation and may range from 104 to 108 per gram26. The findings from this
and previous studies29,30,33,34 have shown that high levels of Enterobacteriaeae are normal
in fruit, salad vegetables and sprouted seeds, therefore levels of faecal indicator
organisms such as E. coli are a better indication of contamination and hygienic quality.
Levels of E. coli in raw ready-to-eat fruit and vegetables however should be kept to a
minimum.
16
The SCF report concludes that Good Agricultural Practice and Good Hygiene Practice
are the basis for the safe production of fresh produce, and that the most efficient way to
improve the safety of produce is to rely on a proactive system reducing risk factors
during production and handling3. A fifth (20%) of pre-cut fruit, sprouted seeds, and
unpasteurised juices were stored or displayed at above 8°C. Where prepared ready-to-eat
fresh produce and juices are being stored they should be kept at or below 8°C to satisfy
the legal requirements of the Food Safety (Temperature Control) Regulations 199511. As
a matter of good practice it is recommended that such fresh produce should also be kept
at or below 8°C during display for sale. Voluntary industry guides have been produced
to help minimise microbial food safety hazards from farm to fork, i.e. from produce
suppliers to food handlers.
A hazard analysis system was in place in most (85%)
production and retail premises visited, of which 80% had documented systems, and most
managers (83%) had received some form of food hygiene training. As shown in a metaanalysis of UK food studies35, high confidence in the food business management of food
hygiene, as indicated by Local Authority Inspectors' Confidence in Management scores,
and food safety procedures, i.e. the presence of a hazard analysis system, was in turn
related to management food hygiene training. There is growing acceptance throughout
the European Community and in many other countries of the value of the application of
HACCP principles in ensuring the microbiological safety of foods. Implementing and
maintaining food safety procedures based on HACCP principles is expected to become a
European legal requirement for all food businesses regardless of size36.
Although the results from this study indicate that overall pre-cut fruit, sprouted seeds and
unpasteurised fruit and vegetable juices from production and retail premises were of
satisfactory/acceptable quality, occasional outbreaks of salmonellosis, E. coli O157, and
L. monocytogenes in Europe, US, Canada, and Japan have been linked to a diversity of
fresh fruit and vegetables3,4, including a variety of sprouted seeds (cress, clover, mung
bean, alfalfa, radish), melons, and unpasteurised orange and apple juices12-14 and
demonstrate that major health problems can arise from consumption of contaminated
fresh produce if hygiene practices break down. It follows that the need for a sound
approach to food safety management cannot be overemphasised.
17
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 microbiological examination. Thanks are
extended to John Barnes at the Food Standards Agency for guidance on carrying out the
microbiological component of the EC Recommendation 2002/66/EC, David Lock at
LACORS for coordinating the participation of Environmental Health Officers and advice
from the LACORS Food Examination Focus Group, FSML (CPHL) for typing isolates,
the PHLS Group FWE Coordinators Forum, in particular Melody Greenwood, for their
advice in preparing the sampling protocol, and to Lilian Hucklesby for entering the data
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20
Annex 1: Participating PHLS Groups, Laboratories and Local Authority Food
Liaison Groups
Table 1a. Participating PHLS Groups, Public Health Laboratories and number of samples
PHLS Group
Public Health Laboratory
East
Chelmsford
Norwich
Ashford
Brighton
London FWEML1
WEMS2
Birmingham
Coventry
Shrewsbury
Stoke
Chester
Preston
Hull
Leeds
Middlesborough
Newcastle
Bristol
Exeter
Gloucester
Hereford
Plymouth
Lincoln
Sheffield
Cardiff
London & South east
Midlands
North west
North
South West
Trent
Wales
Total
Number of samples*
129
131
89
213
23
93
37
144
24
61
163
158
78
52
50
82
54
33
17
48
21
164
65
11
1940
1, London Food, Water & Environmental Microbiology Laboratory, FSML CPHL
2, Wessex Environmental Microbiological Service
Table 1b. Participating Non-PHLS Laboratories and number of samples
Non-Public Health Laboratory
Belfast City Hospital
City of Edinburgh
Dundee Scientific Services
Dumfries Galloway
Glasgow Scientific Services
Kings Lynn & West Norfolk
Public Analyst Aberdeen
Royal Alexandra, Paisley
Total
Number of Samples*
95
14
8
2
33
7
5
3
167
*Includes the 11 samples not included in the analysis.
21
Table 1c. Local Authority Food Liaison Groups and number of samples
Local Authority Food Liaison Group
Berkshire Food Co-ordinating Group
Cambridge Food Liaison Group
Cheshire Food Liaison 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
Gloucester Food Safety Group
Greater Manchester Food Liaison Group
Hampshire & Isle Of Wight Food Advisory Group
Hereford & Worcester CEHOS Food Working Group
Humberside Food Liaison Group
Kent Food Technical Group
Lancashire Assn Of CEHOS, Food Officer Group
LFCG1 North East Sector
LFCG South West Sector
Lincolnshire Co-ordinating Group
Merseyside Food Sub-Group
North Yorkshire CEHOS Group
Northamptonshire Food Liaison Committee
Northern Ireland Food Group2
Northumberland Food Safety Group
Norfolk Food Liaison Group
Nottingham District Food Group
Scottish Food Enforcement Liaison Committee3
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
Number of Samples*
2
67
87
16
31
48
20
17
73
55
17
77
51
48
77
89
65
10
13
81
73
34
79
95
12
93
88
65
4
6
29
65
34
80
34
57
1
13
6
64
67
30
70
30
34
2107
1, London Food Co-ordinating Group
2, Northern Ireland Food Group comprises of the Eastern, Northern, Southern and Western Groups
3, SFELG comprises of Central Scotland, Fife & Tayside, Lothian & Scottish Borders, North Scotland, and West of Scotland
*
Includes the 9 samples not included in the analysis.
22