LACORS/PHLS Co-ordinated Food Liaison Group Studies: Microbiological Examination of Ready To Eat Cold Sliced Meats and Pâté from Catering and Retail Premises. R Elson, F Burgess, CL Little*, RT Mitchell and the Food, Water and Environmental Surveillance Network†. Environmental Surveillance Unit, Health Protection Agency Communicable Disease Surveillance Centre, 61 Colindale Avenue, London, NW9 5EQ. On behalf of the Local Authorities Co-ordinators of Regulatory Services and the Public Health Laboratory Service. Summary During May and June 2002, a study of ready-to-eat cold sliced meats and pâtés from catering and retail premises was undertaken to determine their microbiological quality. Examination of 4,078 samples of ready-to-eat cold sliced meats and pâtés revealed that most (75%) were of satisfactory/acceptable microbiological quality and 25% were of unsatisfactory quality due to high Aerobic Colony Counts and high levels of Enterobacteriaceae, Escherichia coli or Listeria spp. Two samples (<1%) were of unacceptable microbiological quality due to the presence of Campylobacter jejuni and Listeria monocytogenes in excess of 100 cfu/g. Acceptable microbiological quality of ready-to-eat sliced cold meats and pâtés was associated with premises that had management food hygiene training and hazard analysis in place. Poor microbiological quality was associated with storage or display of meats and pâtés above 8°C, pre-sliced meats, infrequent cleaning of meat slicing equipment, poor physical separation of raw meat and ready to eat meat products and movement of staff between areas used for raw meats and ready-to-eat foods. *Author for correspondence †, FWES Network comprises Laboratories listed in Annex I 1 Introduction Cooked sliced meats and pâtés are regarded as high-risk foods1.Their manufacture and sale is well regulated in the UK, production in approved premises being controlled by the Meat Products (Hygiene) Regulations 1994 (as amended)2 and production in retail premises for sales direct to consumers being controlled by the Food Safety (General Food Hygiene) Regulations 19953 and the Food Safety (Temperature Control) Regulations 19954. In response to the 1996 Central Scotland Escherichia coli O157 outbreak5 and the subsequent inquiries6,7, premises preparing handling, selling and supplying unwrapped raw meat together with ready to eat foods as part of a retail operation in the UK now require a licence, the granting of which is dependent upon enhanced food hygiene requirements3. Meat, including pre-cooked meat, forms an important part of the UK diet and consumption patterns have shown marked changes over the last two decades. Between 1979 and 1999 in the UK, consumption of cooked poultry more than quadrupled and cooked bacon and ham consumption increased by around 10 grams per person per week in the same time period8. The role of cooked sliced meats and pâtés as a vehicle or source of infection of a number of pathogens is well documented9,10. It has been highlighted that in order to work towards a 20% reduction in foodborne disease by April 2006 in line with the Food Standards Agency’s target11, more emphasis needs to be placed on reducing infection with Campylobacter spp.. Although the commonest cause of acute bacterial gastroenteritis, the epidemiology of campylobacter infection remains poorly understood. While the widespread contamination of raw poultry and poultry products with Campylobacter spp. is well documented10,12, the role of other foods as the source of infectious disease is less clear. In May 2000 a population-based sentinel surveillance scheme for campylobacter infection was launched by the Public Health Laboratory Service (PHLS) in England and Wales with the aim of generating hypotheses for campylobacter infection systematically by the integration of standardised epidemiological and microbiological typing data. During the first year of the scheme the study found that indigenous cases infected with C. jejuni were more likely to report the consumption of pre-cooked cold meats13. Cold cooked meats have also been implicated in a US 2 epidemiological study of campylobacter infection. The US researchers found that cases were more likely to report the consumption of chicken luncheon meat and ham than controls14. Cold ready to eat meats, pâtés and similar meat products have also been associated with outbreaks of Listeria monocytogenes15,16. L. monocytogenes, whilst responsible for less morbidity in England and Wales than Campylobacter, remains a cause for concern due to the increased risk posed to vulnerable groups17. L. monocytogenes is ubiquitous in the environment, and its ability to colonise food-processing environments is well recognised18. This pathogen is also able to grow at refrigeration temperatures19. A small proportion of ready-to-eat cold meats and pâté in the UK have been shown to be contaminated with L. monocytogenes and occasionally at levels higher than 102 cfu/g20,21. This study was the first of two studies that formed the 2002/2003 Local Authority Coordinators of Regulatory Services (LACORS)/PHLS Coordinated Food Liaison Group Microbiological Sampling Programme. The study aimed to establish the microbiological quality of ready-to-eat cold sliced meats and pâté from catering and retail premises, and to investigate possible links hypothesised by the PHLS Campylobacter Sentinel Surveillance Scheme between foodborne campylobacter infection and the consumption of cold sliced meats and pâté. Materials and Methods Sample Collection Cold sliced ready to eat meats and pâtés were collected from supermarkets, delicatessens, butchers, market stalls, hotels, public houses, hospitals, residential care homes restaurants, cafés and school and staff restaurants and examined in PHLS and non-PHLS laboratories in the UK between the 1st May and 30th June 2002 using a standardised protocol and reporting system. Samples (100g) consisted of meats and pâté cooked and sliced on or off the premises from where the sample was taken. Fermented, dried and stuffed meats, fish or fish products (except pâtés), frozen samples and unopened packages 3 originating from premises other than those where the sample was taken were specifically excluded from this study. Samples 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.722 and advice provided in the LACORS guidance on microbiological food sampling23. Information on the catering or retail premises was obtained by observation and enquiry and recorded on a standard proforma. This included information on the premises and practices with regard to cooking, slicing and storage of meats and pâté, documentation of a hazard analysis system and the level of food hygiene training received by the manager. 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 Food Safety Act 1990 Code of Practice No 924 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 every 6 months) to F (lowest risk, inspected 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). Isolation of bacteria Aerobic Colony Counts (ACC), Enterobacteriaceae, E. coli, L. monocytogenes and other Listeria spp., and Salmonella spp., were enumerated or detected in accordance with PHLS Standard Microbiological Methods25-30Campylobacter spp. were detected by enrichment in Bolton Selective Enrichment Broth with incubation at 37°C for 4 hours, followed by further incubation at 41.5°C and subculture to Campylobacter selective agar (CCDA) after 44 2 h. Inoculated plates were incubated at 41.5°C for 48 h, and colonies identified as described in PHLS Standard Microbiological Method F2131. Isolates of Campylobacter spp. were sent to the Laboratory of Enteric Pathogens (LEP), Central Public Health Laboratory (CPHL) for confirmation and typing. L. monocytogenes at 4 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 sale32 (Table 1). 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. Statistical analysis Descriptive and statistical analysis of the data was undertaken using Microsoft Excel version 7 and Epi Info version 6.04d. Relative proportions were compared using the Chisquared test (χ2) and χ2 test for trend. A probability value of less than 5% was deemed to be significant. Table 1. Key to classification in the PHLS Microbiological Guidelines for cooked meat and pâté sampled at the point of sale 32 Criterion Microbiological quality (cfu per gram unless stated) Satisfactory Acceptable Unsatisfactory Aerobic Colony Count Cat. 3† <105 105 - <106 ‡ 6 Aerobic Colony Count Cat. 4 <10 106 - <107 2 Enterobacteriaceae <10 102 - <104 Escherichia coli (total) <20 20 - <102 Listeria spp. (total) <20 20 - <102 Listeria monocytogenes <20 20 - <102 Campylobacter spp. Not detected in 25g Salmonella spp. Not detected in 25g †; cooked ham, tongue, ‡; other cooked meats and pâté, *, N/A; Not applicable 106 107 104 102 102 N/A Unacceptable/ potentially hazardous N/A* N/A N/A N/A N/A 102 Detected in 25g Detected in 25g Results A total of 2,894 cold meats and 1,184 pâtés collected from 2288 catering and retail premises were examined in 38 laboratories (31 PHLS and 7 non-PHLS) in England, Wales, Scotland and Northern Ireland. 368 Local Authorities, involving 52 Local 5 Authority Food Liaison Groups, submitted samples (Annex 1). A further 35 samples did not fit the criteria described in the study protocol and were not included in the analysis. Microbiological quality of cold ready to eat sliced meats Over half (54%) of the cooked sliced meat samples were satisfactory, 20% were acceptable, and 26% were of unsatisfactory microbiological quality (Figure 1). However, two (<1%) samples were of unacceptable microbiological quality due to the presence of Campylobacter jejuni HS18 Phage Type 44 (beef sample) and L. monocytogenes serotype 4b at 3.4 x 104 cfu/g (ham sample). Unsatisfactory results were due to high ACCs (≥107 cfu/g for cooked ham and tongue samples; ≥106 cfu/g for other sliced meat samples), or high levels of Enterobacteriaceae (≥104 cfu/g), E. coli (≥102 cfu/g), or Listeria spp. (L. innocua ≥102 cfu/g) (Table 2). Table 2. Microbiological results of 4,078 ready to eat cold meat and pâtés ND* in 25g Cold Meats (n=2894) Aerobic Colony Count Enterobacteriaceae E. coli (total) Listeria spp. (total) -L. monocytogenes Salmonella spp. Campylobacter spp. Pâté (n=1184) Aerobic Colony Count Enterobacteriaceae E. coli (total) Listeria spp. (total) -L. monocytogenes Salmonella spp. Campylobacter spp. 2,694 2,887 2,823 1134 D§ in 25g <10/ <20/ <100† 10/20 -<102 102 <103 103 <104 104 <105 105 <106 106 <107 107 NE¶ 92b 1747a 2805b 60 407 43 3 277 304 26 1 584 213 8 530 127 3 1 1 526 68 357 14 464 10 1 4 4 8 20 20 7 70 75b 892a 1131b 53 99 12 191 94 36 1 272 52 3 177 29 160 17 114 140 2 1 2 6 6 2 16 175c 60c 1 43c 22c 1182 1168 *ND; Not detected; §D, Detected; ¶NE, Not examined (full set of microbiological parameters not performed on sample due to insufficient sample collected) †, cfu/g a, lower limit of detection 10 CFU/g; b, lower limit of detection 20 CFU/g c, detected in 25g and present at <20 cfu/g Meat types sampled included ham (49%), beef (19%), turkey (14%), pork (8%), chicken (4%), and lamb (1%) (Table 3). Other meat types (bacon, gammon, brawn, haslet, 6 luncheon meat tongue, corned beef, duck, venison, pastrami, polony and mixed meats) made up the remaining 5% of samples. The proportion of turkey meat samples of unsatisfactory or unacceptable microbiological quality (40%) was higher when compared to all other meat types (beef; 34%, pork; 34%, chicken; 30%, ham; 16%, and other types; 29%). This finding was significant when comparing turkey with ham (p<0.001), chicken (p=0.04), or other meat types (p=0.03) (Table 3). Figure 1. Microbiological Quality of Cold Sliced Meats and Pâté Samples based on the PHLS Microbiological Guidelines32 Cold Sliced Meats Pate 1% 23% 26% Satisfactory Acceptable Unsatisfactory 53% Unacceptable 15% 20% 62% Microbiological quality of pâté samples Approximately two-thirds (62%) of pâté samples were satisfactory, 15% were acceptable, and 23% were of unsatisfactory microbiological quality. No pâté samples were of unacceptable microbiological quality (Table 4, Figure 1). Unsatisfactory results were due to high ACCs (≥107 cfu/g), or high levels of Enterobacteriaceae (≥104 cfu/g), E. coli (≥102 cfu/g), or Listeria spp. (L. seeligeri; 7 240 cfu/g). (Table 2). Table 3. Microbiological Quality of cold sliced meats based on the PHLS Microbiological Guidelines32 Microbiological Quality Meat Type Satisfactory (%) Acceptable (%) Unsatisfactory Ham 901 (63) 297 (21) 224 Beef 232 (42) 126 (23) 187 Turkey 170 (41) 75 (18) 166 Pork 112 (46) 49 (20) 82 Chicken 64 (53) 21 (17) 36 Lamb 12 (63) 2 (11) 5 Other (bacon, gammon etc.) 78 (60) 15 (11) 38 1569 (54) 585 (20) 738 Total (%) Unacceptable (%) (16) 1 (<1) (34) 1 (<1) (40) 0 (34) 0 (30) 0 (26) 0 (29) 0 (26) 2 (<1) Two-thirds (66%) of pâté samples were meat based, 26% were poultry based, 4% were fish or seafood based, 3% were vegetarian, and 1% were other pâté types (mixed meat and poultry, duck and pork, game, liver and potted meat). For <1% of samples, the pâté type was not recorded. The proportion of vegetarian and fish and seafood-based pâtés of unsatisfactory quality was higher (42% and 31%, respectively) when compared to meat (23%), poultry (21%), other pâté types (7%), and unknown pâté types (17%). This finding was only significant when comparing vegetarian pâtés to meat, poultry, and other pâté types (p<0.02) (Table 4). L. monocytogenes was present in 2% of samples, and at levels below 20 cfu/g. L. monocytogenes was detected in more fish and seafood pâté samples (10%; 4/42) compared to meat (1%; 10/782), poultry (2%; 2/308) and vegetarian (3%; 2/31) pâtés. This finding was significant when comparing fish and seafood pâté samples with meat and poultry based pâtés (p<0.005). 8 Total 1423 546 411 243 121 19 131 2894 Table 4. Microbiological quality of pâté samples based on the PHLS Microbiological Guidelines31 Pâté Type Microbiological Quality Total Satisfactory (%) Acceptable (%) Unsatisfactory (%) Unacceptable (%) Meat based 495 (63) 111 (14) 176 (23) 0 - 782 Poultry based 191 (62) 52 (17) 65 (21) 0 - 308 Fish/Seafood based 17 (40) 12 (29) 13 (31) 0 - 42 Vegetarian 15 (48) 3 (10) 13 (42) 0 - 31 Other (game, mixed meat) 13 (87) 1 (7) 1 (7) 0 - 15 Not recorded 5 (83) 0 1 (17) 0 6 Total 736 (62) 179 (15) 269 (23) 0 - 1184 Product history in relation to microbiological quality Place of cooking cold meats Approximately one third (32%) of cold meat samples were cooked on the premises from which they were sampled, 65% were cooked elsewhere and for 3% of samples, this information was not recorded. The proportion of cold meat samples of unsatisfactory or unacceptable microbiological quality was significantly higher where the meat was cooked elsewhere (27%) compared to meat samples cooked on the premises (21%) (p<0.001). Of the 918 meat samples cooked on the premises, 12% had been cooked within 1 day of sampling, 24% between 1-2 days, 22% between 2-3 days, 13% between 3-4 days, and 23% more than 4 days before sampling. For 4% of samples the time since cooking was not known and for 2%, this information was not recorded. Significantly fewer samples which had been cooked within one day were of unsatisfactory or unacceptable microbiological quality (8%) compared to those which had been cooked and kept for longer than this time (>1 day (21%), >2 days (21%), >3 days (30%), >4 days (24%)) (p<0.01). Almost two-thirds (64%) of meat samples cooked elsewhere were supplied by wholesalers, 9% were from butchers, and 5% were from supermarkets. Other suppliers (including company warehouses, bakeries and sandwich filling suppliers) accounted for 9 16% of samples and this information was not recorded for 6% of samples. Significantly more unsatisfactory or unacceptable samples were supplied by wholesalers (32%) and butchers (29%) than those supplied by supermarkets (15%) and other suppliers (14%) (p<0.01). Over three-quarters (79%) of the cold meat samples were transported to the food premises vacuum wrapped, 3% were wrapped in cling film and <1% were transported in open trays. Other methods of packaging (grease proof paper, cook bags, sealed plastic bag or container, closed trays, aluminium foil, box, modified atmosphere packaging, cans) were used for 6% of samples. For 11% of samples the transportation packaging was not known. The small numbers of cold meats packaged in cling film were more likely to be of unsatisfactory or unacceptable microbiological quality (33%) compared to those packaged in vacuum packing (28%) or other wrapping methods (24%). Slicing cold meats The majority (88%) of cold meat samples were sliced on the premises, 10% were presliced elsewhere, and for 2% of samples, this information was not recorded. The proportion of samples of unsatisfactory or unacceptable microbiological quality was significantly higher where the meat was pre-sliced elsewhere (35%) compared to meat sliced on the premises (24%) (p<0.0001). Where the meat was sliced on the premises, most (81%) were sliced using a meat slicing machine and a further 18% by using a knife. For 1% of samples, this information was not known or not recorded. The proportion of unsatisfactory or unacceptable meat samples sliced using meat slicers was higher (25%) when compared to those sliced with a knife (22%), however this was not significant. Where the meat was sliced using a meat-slicing machine, sampling officers noted that 6% of slicers had damaged carriage guards and 11% were soiled. Proportionally, the number of unsatisfactory or unacceptable meat samples sliced on damaged (29%) or soiled (26%) 10 slicing machines was higher compared to those sliced on unsoiled, undamaged slicing machines (25%), however, this finding was not significant. Most (87%) meat slicing equipment was only used to slice ready-to-eat food, 7% was not, and for 6% of samples this information was not recorded. There was no significant difference in the proportion of unsatisfactory or unacceptable meat samples that had been cut with equipment used for ready to eat food only (24%) when compared to meat cut with equipment that was not dedicated for ready to eat food only (25%). Over three-quarters (78%) of meat slicing equipment was cleaned periodically throughout the day while 16% was cleaned at the end of trading. For 6% of samples, this information was not recorded. Significantly more samples were of unsatisfactory or unacceptable microbiological quality when sliced with equipment cleaned only at the end of trading (30%) than those sliced using equipment cleaned regularly throughout the day (23%) (p=0.005). Manufacture of pâté Almost a fifth (18%) of pâtés were made on the premises from which they were sampled, 80% were made elsewhere and for 2%, this information was not recorded. In contrast to the cold meat samples, there was no significant difference between the proportion of unsatisfactory pâté samples when comparing pâtés made on the premises (24%) with those supplied from elsewhere (22%). Of 180 meat and poultry based pâté samples made on the premises, 41% were made by flash frying the livers followed by further heating and 27% were made by flash frying the livers followed by further processing. Less samples which had been cooked by flash frying the livers followed by further heating were of unsatisfactory microbiological quality (20%) compared to those which had been cooked by flash frying followed by further processing (23%), however this finding was not significant. 11 A garnish or glaze was added to 30% of pâté samples following cooking on the premises, for 64% it was not, and for 6% of samples, this information was not recorded. A higher proportion of pâtés that had a garnish or glaze added after cooking were of unsatisfactory microbiological quality (27%) compared to those that did not have any further ingredients added after cooking (23%) however this finding was not significant Pâté shelf life Of the 209 pâté samples cooked on the premises, approximately three quarters (42%) had an allocated shelf life of less than one week, 15% had less than 2 weeks, 10% had less than 3 weeks, 11% had less than 4 weeks, 12%had between 4 and 8 weeks, 1% had between 8 and 12 weeks, and 1% had a shelf life equal to or exceeding 12 weeks. For 8% of samples, this information was not known. There was no difference in the microbiological quality of pâtés cooked on the premise in relation to their allocated shelf life. For 80% of pâté samples, the period of time remaining until the pâté’s shelf life expired was recorded. The shelf life of 8% of pâté samples expired within 1 day of sampling, 36% expired between 1 and 10 days of sampling and 16% expired over 10 days from sampling. For 20% of samples this information was not known. A higher proportion of the pâté samples sampled over ten days from their expiry date were of unsatisfactory quality (23%) compared to those sampled closer to their expiry date (1-10 days; 20%, <1 day; 18%) although this was not significant. Storage, display and service of cold meats and pâté The majority (92%) of cold ready to eat meat and pâté samples were stored or displayed at or below 8ºC, 5% of samples were stored above 8ºC, and for 3% of samples, this information was not recorded. A significantly higher proportion of cold meat and pâté samples (38%) that were stored above 8ºC were of unsatisfactory or unacceptable microbiological quality compared to those stored below 8ºC (24%) (p<0.0001). 12 Over half (55%) of the meat and pâté samples were covered at the time of sampling, 40% were not and for 5% of samples, this information was not recorded. The proportion of meat and pâté samples that were of unsatisfactory or unacceptable microbiological quality was significantly higher where the meats and pâtés were covered at the time of sampling (26%) compared to those that were not (22%) (p=0.002). Over a third (34%) of cold meat and pâté samples were served using gloved or protected hands, 22% were served with bare hands, 17% were served using a dedicated utensil, 6% were served using shared utensils, 5% were served using the product protective packaging and 4% were served using another method (combination of gloved or bare hand with a dedicated or shared utensil, plastic bag or polythene wrapping). For 12% of samples, this information was not recorded. The proportion of unsatisfactory or unacceptable cold meat and pâté samples was lower when served using a dedicated utensil (21%) compared to service by protected hand (26%), bare hand (25%), shared utensil (25%), packaging (26%) and other methods (24%). This finding was significant when comparing the use of a dedicated utensil with service by protected hand (p=0.03). Catering and retail premises in relation to microbiological quality Type of premises Cold meat and pâté samples were collected from 630 catering and 1658 retail premises. Catering premises comprised of hotels, cafes, public houses, restaurants, (including staff, hospital and school restaurants) prison kitchens, fish and chip shops, takeaways, mobile snack vans and sandwich shops. Retail premises comprised of supermarkets, delicatessens, butchers shops, bakers shops and market stalls. Three-quarters (75%) of the meat and pâté samples were collected from retail premises and 25% from catering premises. Proportionally more unsatisfactory or unacceptable meat and pâté samples were from catering premises (26%) than from retail premises (24%), however this difference was not significant. 13 Significantly more samples from market stalls (43%) and delicatessens (39%) were of unsatisfactory or unacceptable microbiological quality compared with those from other retail premises (butchers 27%, supermarkets 13%, and other premises types 25%) (p<0.04). Significantly more samples from cafes (39%) and other catering premises (35%) (fish and chip shops, takeaways, mobile snack vans, prison kitchens) were of unsatisfactory or unacceptable microbiological quality when compared to hotels (18%), public houses (21%), and restaurants (21%) (p<0.03). Food safety practices in premises handling open raw meat and ready-to-eat food The results presented in this section relate to all premises unless otherwise specified. A detailed breakdown of results relating to catering and retail sectors is provided in Table 5. Over three-quarters (76%) of premises handled open raw meat on the premises, 22% did not and for the remaining 2% of premises, this information was not recorded. Significantly more catering premises (82%) handled open raw meat as well as ready to eat foods when compared to retail premises (74%) (p<0.00001) (Table 5). The proportion of meat and pâté samples of unsatisfactory or unacceptable microbiological quality was significantly lower (23%) from premises that also handled open raw meat when compared to those from premises that only handled ready-to-eat food (32%) (p<0.0001). Physical separation was provided between raw meat and ready to eat food areas in 84% of premises. The practice of separating raw meat and ready to eat foods was significantly higher in retail premises (90%) compared to catering premises (70%) (p<0.00001) (Table 5). Where there was a lack of physical separation, the proportion of unsatisfactory meat and pâté samples was significantly higher (29%) when compared to premises that did provide this separation (22%) (p<0.002) (Figure 2). Most premises visited did not transfer equipment between raw meat and ready-to-eat food areas (74%). However, 22% of premises did transfer equipment between raw meat and ready to eat food areas and this practice was significantly more common in catering premises (43%) compared to retail premises (13%) (p<0.00001) (Table 5). There was no 14 significant difference in the proportion of unsatisfactory samples from premises that transferred equipment (23%) from raw meat to ready-to-eat food areas and those that did not (22%) (Figure 2). Seventy-one per cent of premises had staff that moved between raw meat and ready-toeat food areas and this practice was significantly more common in catering premises (82%) compared to retail premises (66%) (p<0.00001) (Table 5). In 27% of premises visited, staff did not move between raw meat and ready to eat food areas and for 3% of premises, this information was not recorded. Significantly more meat and pâté samples of unsatisfactory or unacceptable microbiological quality were from premises where staff moved between raw and ready-to-eat food areas (26%) compared with those that did not (16%) (p<0.0001) (Figure 2). Figure 2. Food safety practices in premises handling open raw meat and microbiological quality of cold sliced meats and pâté samples Food Safety Practice Physical separation between raw meat and RTE products Equipment transferred from raw meat areas to RTE food areas Yes No Staff move between raw meat and RTE food areas Staff change clothing between raw meat and RTE food areas 0 5 10 15 20 25 30 35 % Unsatisfactory/Unacceptable Samples Of the premises visited where staff moved between raw meat and ready-to-eat food areas, staff did not change their protective clothing in 77% of premises, in 13% of premises they did and for 9% of premises, this information was not recorded. Where staff moved 15 between raw meat and ready-to-eat food areas and did not change their protective clothing, a significantly higher proportion of samples of unsatisfactory or unacceptable quality (27%) were obtained compared to premises that had staff that did change their protective clothing (16%) (p<0.0001). Table 5. Food Safety Practices in premises handling open raw meat and ready to eat foods Food Safety Practice Open raw meat handled Yes on premises No Retail Premises (%) No. Samples No. Samples (% Catering Premises (% Unsatisfactory/ (%) Unsatisfactory/ Unacceptable) Unacceptable) 1222 (74) 2275 (23) 519 (82) 838 (23) 410 (25) 761 (30) 95 (15) 149 (42) 26 (2) 35 (29) 16 (3) 20 (30) Yes Physical separation between raw & ready to No eat foods NR 1104 (90) 2072 (21) 361 (70) 596 (22) 107 (9) 187 (33) 150 (29) 232 (25) 11 (1) 16 (31) 8 (2) 10 (40) Yes 162 (13) 285 (25) 225 (43) 350 (21) No 1018 (83) 1921 (22) 278 (54) 463 (25) NR 42 (3) 69 (30) 16 (3) 25 (20) Staff move between raw Yes meat & ready to eat food No areas NR 807 (66) 1457 (27) 426 (82) 697 (22) 381 (31) 756 (14) 82 (16) 129 (29) 34 (3) 62 (18) 11 (2) 12 (0) Staff change protective clothing when moving between raw meat & ready to eat food areas Yes 111 (14) 220 (20) 53 (12) 104 (9) No 627 (78) 1130 (28) 327 (77) 517 (23) NR 69 (9) 107 (32) 46 (11) 76 (37) NR Equipment transferred between raw meat & ready to eat food areas NR- Not Recorded Food Hygiene Inspections Of the catering and retail premises visited, over half (52%) had an inspection rating category of C, 7% were rated as Category A, 31% B and 3% D, 1% E and <1% as F. This information was not recorded for 6% of premises. A significantly higher proportion of catering premises were rated Category C or below (63%) compared to retailers (54%) (p<0.001) (Table 6). 16 Two thirds (66%) of premises visited had consumer at risk scores of 5. Almost a quarter (23%) had scores of 10, 2% had scores of 15 and <1% had scores of 0. For 9%, the consumer at risk score was not recorded. The proportion of retail premises with a consumers at risk score of 10 or above, indicative of larger businesses, (27%) was higher than catering premises (21%). Twice as many samples obtained from premises with small numbers of customers (29%) were of unsatisfactory or unacceptable microbiological quality when compared to premises with intermediate (15%) or substantial (13%) numbers of customers (p<0.005) (Table 6). Almost half (43%) of the premises visited had a confidence in management score of 10 (some confidence), 5% had a score of 0 (high confidence), 36% had a score of 5 (moderate confidence), 7% a score of 20 (little confidence), and <1% had a score of 30 (no confidence). For 9% of premises visited, this information was not recorded. A significantly higher proportion of catering premises (13%) had a score of 20 or above compared to retail premises (5%) (p<0.0001) The proportion of unsatisfactory or unacceptable samples was higher from premises where there was little or no confidence (27%) compared to premises where there was some, moderate or high confidence in management (24%) although this finding was not significant (Table 6). Hazard Analysis System Over half of the premises visited had a documented hazard analysis system in place (63%) and a further 14% had an undocumented hazard analysis system in place. However, 10% of premises had no hazard analysis system in place and for 12% of premises, this information was not recorded. Retail premises were significantly more likely to have a documented hazard analysis system in place (70%) when compared to catering premises (46%) (p<0.00001). Caterers were significantly more likely to have an undocumented or no hazard analysis system (43%) when compared to retail premises (18%) (p<0.00001) The proportion of samples of unsatisfactory or unacceptable microbiological quality was significantly higher where premises had no hazard analysis system in place (41%) compared to premises with a documented or undocumented (23%) hazard analysis system in place (p<0.00001) (Table 6). 17 Table 6. Details of Food Hygiene inspections in catering and retail premises Premises Details Retail Premises n=1658 Inspection Rating Category A 115 B 543 C 807 D 65 E 21 F 7 Not Recorded 100 Consumers at Risk Score Substantial (15) 25 Intermediate (10) 407 Few (5) 1064 Very few (0) 13 Not Recorded 149 Confidence in Management Score High (0) 86 Moderate (5) 662 Some (10) 663 Little (20) 86 No (30) 5 Not Recorded 156 Hazard analysis In Place and Documented 1157 In Place and Undocumented 175 Not In place 122 Not Recorded 204 Management Food Hygiene training Received Training and attended a 1521 - Basic 6 hour course 643 - Intermediate course 470 - Advanced course 87 - Other recognised course 262 - Not Specified 59 No Training 44 Not Recorded 93 Hand washing facilities Accessible and available for use 1572 - used 1192 - not used 107 - use not recorded 273 Not available and accessible for use 29 Not Recorded 57 No. Samples (% Unsatisfactory/ Unacceptable) Catering Premises n= 630 No. Samples (% Unsatisfactory/ Unacceptable) (7) (33) (49) (4) (1) (0) (6) 216 945 1565 122 41 8 174 (27) (26) (24) (16) (12) (50) (25) 37 160 385 8 2 4 34 (6) (25) (61) (1) (0) (1) (5) 62 250 612 12 3 4 64 (24) (22) (28) (8) (0) (0) (28) (2) (25) (64) (1) (9) 56 813 1921 22 259 (13) (14) (29) (14) (24) 11 118 449 4 48 (2) (19) (71) (1) (8) 20 211 685 6 85 (15) (16) (29) (17) (27) (5) (40) (40) (5) (0) (9) 170 1225 1239 146 12 279 (14) (21) (28) (34) (33) (23) 23 151 320 81 3 52 (4) (24) (51) (13) (0) (8) 47 234 508 120 6 92 (9) (23) (28) (26) (17) (30) (70) (11) (7) (12) 2184 321 220 346 (21) (37) (44) (49) 287 155 116 72 (46) (25) (18) (11) 472 247 184 104 (19) (31) (37) (25) (92) (42) (31) (6) (17) (4) (3) (6) 2835 1221 841 164 493 116 78 158 (24) (26) (20) (19) (27) (16) (38) (26) 571 386 109 41 18 17 35 24 (91) (68) (19) (7) (3) (3) (6) (4) 924 594 186 94 25 25 53 30 (25) (28) (21) (14) (32) (16) (49) (17) (95) (76) (7) (17) (2) (3) 2945 2279 194 472 46 80 (24) (25) (21) (21) (46) (35) 588 430 49 109 17 25 (93) (73) (8) (19) (3) (4) 945 702 82 161 28 34 (26) (26) (33) (24) (14) (32) 18 Food Hygiene Training The majority of premises had managers that had received some form of food hygiene training (91%), 4% did not and for 5% of premises, this information was not recorded. Of those managers with food hygiene training, almost half (49%) had attended a basic 6hour food hygiene course, but 28% were trained to an intermediate and 6% to an advanced level. A further 13% had attended another recognised course (Meat Hygiene Service, Royal Institute of Public Health, Meat and Livestock Commission, vocational qualifications, City and Guilds, higher/ordinary certificate, and in-house training), and for 4% the type of training was not specified. A higher proportion of retail managers were trained to intermediate or advanced level (37%) compared to managers of catering premises (26%) (p<0.0001). A higher proportion of retail managers had attended other recognised training courses (17%) compared to managers of catering premises (3%) (p<0.0001) (Table 6). Significantly more samples of unsatisfactory or unacceptable microbiological quality were taken from premises where the manager had received no form of food hygiene training (43%) compared to premises where the manager had received training (24%) (p<0.0001). Significantly, the proportion of samples of unsatisfactory or unacceptable microbiological quality decreased as the level of training received by the manager increased. (Advanced; 17%, Intermediate; 21%, Basic; 27% (p<0.0001) (Table 6, Figure 3). Hand washing facilities Hand washing facilities were readily accessible and available for use in the vast majority (94%) of premises visited, in 2% they were not and for 4% of premises, this information was not recorded. Where hand-washing facilities were available and accessible for use, they were used by staff, as judged by the sampling officer, in 75% of premises. In 7% of premises they were not used and in 18% of premises, their use was not recorded (Table 6). A higher proportion of samples of unsatisfactory or unacceptable microbiological quality were taken from the small number of premises where hand washing facilities were not 19 available (34%) when compared to premises where these facilities were available (24%). (Table 6). There was no difference in the proportion of samples of unsatisfactory or unacceptable microbiological quality taken from premises where hand washing facilities were utilised (25%) when compared to samples taken from premises where hand washing facilities were not used (24%) (Table 6). Figure 3. Level of management food hygiene training and microbiological quality of cold sliced meats and pâté samples % Unsatisfactory/Unacceptable Samples 30 25 20 Retail Premises 15 Catering Premises All Premises 10 5 0 Basic Intermediate Advanced Level of Management Food Hygiene Training Discussion This study has shown that the majority of ready-to-eat cold sliced meats (74%) and pâtés (77%) collected from catering and retail premises in the UK were of satisfactory or acceptable microbiological quality. However, approximately a quarter of meat (26%) and pâté (23%) samples were of unsatisfactory quality according to published microbiological guidelines31. Unsatisfactory results were due mainly to high ACC, Enterobacteriaceae and E. coli counts. High ACC, Enterobacteriaceae 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 or display facilities was inadequate to prevent bacterial growth, or that a combination of these 20 factors was involved. No pâté samples were of unacceptable microbiological quality, however, two cold meat samples were of unacceptable quality. Of these, one sample was unacceptable due to the presence of Campylobacter jejuni and one sample was unacceptable due to the presence of Listeria monocytogenes at a level in excess of 100 cfu/g. It was beyond the scope of this study to determine where in the food chain this contamination may have taken place and in the absence of detailed consumption data, it is not possible to estimate the risk of exposure to Campylobacter or L. monocytogenes infection from consuming these or similar products. Meat products that are adequately cooked, stored and protected from post cooking contamination present little risk of Campylobacter infection, however, this study has shown that ready-to-eat meats available for consumption can become contaminated with pathogens either during production, storage or preparation for sale. However, it remains that epidemiological studies14 and surveillance systems13 have hypothesised an association between cold cooked meats and Campylobacter infection highlighting the need for further work in this area. This study shows a continued decline in the proportion of pâté samples contaminated with L. monocytogenes since 1989 in the UK (1989; 10%, 1990; 4%, 1994; 3% and 2002; 2%)20,33. However, the proportion of fish and seafood based pâtés with low levels of L. monocytogenes present still remains comparatively higher than meat, poultry and vegetarian pâtés. In contrast, there has been little change in the proportion of cold sliced ready-to-eat meat samples of unsatisfactory or unacceptable microbiological quality from catering premises since 199821 (1998; 26%, 2002; 28%). Unsatisfactory or unacceptable microbiological quality of meats in both the present and 1998 studies were associated with meat cooked or sliced elsewhere, meat supplied from butchers or wholesalers, and meat cooked and kept longer than one day. Other significant risk factors associated with the microbiological quality of cold sliced meats and pâtés in this study were storage or display at a temperature above 8°C, the use of shared meat slicing equipment, the use of meat slicing equipment cleaned only at the end of the trading session, a lack of physical separation between raw meat and ready to eat foods and the movement of staff between areas used for raw meats and ready-to-eat foods. The risk of cross-contamination from open raw meat or other sources could be reduced by improving the separation of open 21 raw meat and ready to eat foods, reducing or eliminating staff movement between raw meat areas and ready to eat food areas, using routinely cleaned equipment to slice meats and by serving ready to eat meat products with a utensil dedicated to this purpose. Two findings were unexpected. Firstly, samples that were covered at the time of sampling were more likely to be of unsatisfactory microbiological quality (26%) compared with those that were not covered (22%). This result highlights an area for further work to determine whether in some circumstances, the use of certain food coverings may encourage the growth of certain bacteria. Secondly, samples taken from premises handling open raw meat and ready-to-eat foods were less likely to be of unsatisfactory microbiological quality (23%) than those taken from premises selling ready to eat foods only (32%). This result may indicate an increased awareness of the hazards associated with raw meats resulting in greater vigilance and higher standards of cleanliness in the premises in question. It is possible that this finding is influenced by other factors and should not be used to minimise the importance of key practices to prevent cross contamination within premises that handle both open raw meat and ready to eat foods. The UK Food Standards Agency’s Hygiene Campaign was launched in April 2002 and forms part of a raft of measures to reduce foodborne illness by 20% by 200611. Part of the campaign is specifically aimed at the catering sector. This study has shown that the proportion of unsatisfactory or unacceptable samples was slightly higher from catering premises (26%) when compared to retail premises (24%). Catering premises were more often associated with food safety practices that are, or are reasonably expected to be, associated with poor microbiological quality. For example, when compared to retail premises, catering premises were significantly more likely to handle open raw meat, less likely to provide physical separation between raw meat and cooked foods and significantly more likely to allow staff and equipment to be transferred between areas used for raw meat and ready to eat food. Significantly, catering premises visited were more likely to be smaller premises where there was less confidence in the management, 22 had no hazard analysis system in place, and had lower numbers of managers trained in food hygiene. Management food hygiene training and the presence of hazard analysis systems in food premises, has been shown to make a significant contribution to an improvement in the microbiological quality of ready to eat foods34. This study has shown that managers in retail premises were more likely to have been trained in food hygiene to an intermediate or advanced level compared to managers in catering premises, who were more likely to be trained to a basic level. Gillespie et al.21 showed that significantly fewer sliced meat samples of unsatisfactory or unacceptable microbiological quality were from premises where the manager had received advanced food hygiene training (14%) compared to those premises where the manager had received intermediate (23%), basic (26%) or no (33%) food hygiene training. The present study has also shown that the proportion of sliced meat and pâté samples of unsatisfactory or unacceptable microbiological quality, in both catering and retail premises, significantly decreased as the level of management training increased suggesting that progressive training of management can make a significant contribution to food safety. The implementation of HACCP or similar food safety plans in food premises provides a pragmatic framework for good hygienic practice. Current EU proposals to consolidate food hygiene directives currently envisage the application of food safety management procedures based upon HACCP principles, including documentation and verification, to all sectors of the food chain, with the exception of primary production35. In this study, samples taken from premises with a documented hazard analysis system were significantly less likely to be of unsatisfactory or unacceptable quality than from premises without any form of hazard analysis system. The implementation of HACCP or similar food safety systems in catering and retail premises, combined with adequate training and the application of basic principles of food hygiene, could make a significant contribution to ensuring the satisfactory microbiological quality of ready to eat foods. 23 Acknowledgements The authors would like to thank all the staff in the Environmental Health Departments throughout the UK who collected samples for this study, all the staff in both PHLS and non-PHLS laboratories who performed microbiological examination. Thanks are also extended to LEP and FSML (CPHL) for typing isolates, to David Lock at LACORS for coordinating the participation of Environmental Health Officers and advice from the LACORS Food Examination Focus Group, to the PHLS Group FWE Coordinators Forum for their comments, in particular Melody Greenwood and Heather Aird, for their advice in preparing the sampling protocol, and to Lilian Hucklesby, Phil Evans and Nicholas Kephalas for entering the data. 24 References (1) MAFF. A National Study on Ready to Eat Meat and Meat Products. 1995. Microbiological Food Safety Surveillance. (2) The Meat Products (Hygiene) Regulations 1994. 1994. The Stationery Office, London. (3) The Food Safety (General Food Hygiene) (Butchers' Shops) Amendment Regulations 2000. The Stationery Office, London (4) The Stationery Office L. Food Safety (Temperature Control) Regulations 1995. 1995. The Stationery Office, London (5) Cowden J, Ahmed D, Donaghy M, Riley A. Epidemiological investigation of the central Scotland outbreak of Escherichia coli O157 infection, November to December 1996. Epidemiology and Infection 2001; 126(3): 335-41. (6) The Pennington Group. Report on the circumstances leading to the 1996 outbreak of infection leading to the 1996 outbreak of E.coli 0157 in Central Scotland, the implications for food safety and lessons to be learned. ISBN 011 4958513. 2003. (7) Cox G. Determination into the E.coli O157 fatal accident inquiry. 1998. Dumfries and Galloway, Sherrifdom of South Strathclyde. (8) Ministry of Agriculture Fisheries and Food (MAFF), National Food Survey 1999,. 59-72. 2000. The Stationery Office, London. (9) Smerdon W, Adak G, O'Brien S, Gillespie I, Reacher M. General Outbreaks of Infectious intestinal disease linked with red meat, England and Wales, 1992-1999. Communicable Disease and Public Health 2001; 4:259-267. (10) Kessel A, Gillespie I, O'Brien S, Adak G, Humphrey T, Ward L. General Outbreaks of infectious intestinal disease linked with poultry, England and Wales, 1992-1999. Communicable Disease and Public Health 2001; 4:171-177. (11) Food Standards Agency. A strategy for meeting the Agency's Foodborne Disease Target. FSA 01/03/02a. 2001. (12) Rodrigues L, Cowden J, Wheeler J. The study of infectious intestinal disease in England: risk factors for cases of infectious intestinal disease with Campylobacter jejuni infection. Epidemiology and Infection 2000; 127:185-193. (13) Campylobacter Sentinel Surveillance Scheme Collaborators. Ciprofloxacin resistance in Campylobacter jejuni: case-case analysis as a tool for elucidating risks at home and abroad. Journal of Antimicrobial Chemotherapy 2002; 50:561568. 25 (14) Klatka L, Hawkins M, Pass M, Angulo F, Rohn D, Morris J et al. Risk factors for sporadic Campylobacter infections in Maryland. Avaialble at http://www cdc gov/foodnet/pub/iceid/2002/klatka_1 htm 2002. (15) Frye D, Zweig R, Sturgeon J, Tormey M, LeCavalier M, Lee I et al. An outbreak of febrile gastroenteritis associated with delicatessen meat contaminated with Listeria monocytogenes. 2002 Oct 15;35(8):943-9. Clin Infect Dis 2002; Oct 15(35(8)):943-949. (16) de Valk H, Vaillant V, Jacquet C, Rocourt J, Le Querrec F, Stainer F et al. Two consecutive nationwide outbreaks of Listeriosis in France, October 1999-February 2000. Am J Epidemiol 2000; Nov 15(154(10)):944-950. (17) Anonymous. Listeria Found in Pate. DoH Press Release 82/299. 12-7-1989. (18) Hall,K, Bird, J and Holah, J. Persistent Environemntal Pathogens. Poster Presentation, Campden Day 2002. (19) Glass K, Doyle M. Fate of Listeria monocytogenes in processed meat products during refrigerated storage. Applied and Environmental Microbiology 2003; 1989(June):1565-1569. (20) Nichols G, Mc Lauchlin J, De Louvois J. The contamination of Pate with Listeria monocytogenes - Results from the 1994 European Community Coordinated Food Control Program for England and Wales. Journal of Food Protection 1998; 61(10):1299-1304. (21) Gillespie I, Little C, Mitchell R. Microbiological examination of cold ready-to-eat sliced meats from catering establishments in the United Kingdom. Journal of Applied Microbiology 2000; March 200(88(3)): 467-474. (22) Food Standards Agency. Food Safety Act 1990 (as amended) Code of Practice No.7 Sampling for Analysis and Examination (Revised October 2000). 2000. (23) LACORS. LACOTS Guidance on Food Sampling for Microbiological Examination. 2002. Available at www.lacors.com. (24) Food Standards Agency. Food Safety Act 1990 (as amended) Code of Practice No.9 Food Hygiene Inspections (Second Revision October 2000). 2000. (25) Public Health Laboratory Service. Methods for Food Products - Aerobic Plate Count at 30 Deg: Surface Plate Method. Standard Method F10. 1998. (26) Public Health Laboratory Service. Methods for Food Products - Aerobic Plate Count at 30 deg C: Spiral Plate Method. Standard Method:F11. 1998. (27) Public Health Laboratory Service. Methods for Food Products - Enumeration of Enterobacteriaceae by Colony Count Technique. Standard Method:F23. 1998. 26 (28) Public Health Laboratory Service. Methods for Food Products - Direct Enumeration of Eschericia coli. Standard Method:F20. 1998. (29) Public Health Laboratory Service. Methods for Food Products - Detection and Enumeration of Listeria monocytogenes and other Listeria Species. Standard Method:F19. 2003. (30) Public Health Laboratory Service. Methods for Food and Dairy Products Detection of Salmonella species. Standard Method:F13. 1998. (31) Public Health Laboratory Service. Methods for Food and Dairy Products Detection of Campylobacter species. Standard Method:F21. 1998. (32) Gilbert R, De Louvois J, Donovan T, et al. Guidelines for the microbiological quality of some ready to eat foods sampled at the point of sale. Communicable Disease and Public Health 2000; 3(3):163-167. (33) Gilbert R, Mc Lauchlin J, Velani S. The contamination of pate by Listeria monocytogenes in England and Wales in 1989 and 1990. Epidemiology and Infection 1993; 110:543-551. (34) Little C, Lock D, Barnes J, Mitchell R. The microbiological quality of food in relation to hazard analysis systems and food hygiene in UK catering and retail premises. Communicable Disease and Public Health 2003; Submitted. (35) Food Standards Agency. Strategy for Wider Implementation of HACCP. FSA 01/07/02. 2001. 27 Annex 1 Table I. Participating PHLS Groups, Public Health Laboratories and number of meat and pâté samples PHLS Group East London and South East Midlands North West North South West Trent Wales Public Health Laboratory Chelmsford Norwich Ashford Brighton London FWEL Reading WEMS Birmingham Coventry Shrewsbury Stoke Chester Preston Carlisle Hull Leeds Middlesbrough Newcastle Bristol Exeter Gloucester Hereford Plymouth Truro Leicester Lincoln Sheffield Bangor Cardiff Carmarthen Rhyl Total 28 Meat Samples 92 76 103 184 312 83 101 60 135 130 47 119 83 48 71 39 60 115 110 71 43 35 25 73 112 162 109 25 47 63 32 Pâté Samples 38 40 31 71 91 51 58 25 63 24 12 51 75 15 43 18 16 67 26 39 27 17 18 32 23 36 33 16 15 32 10 Total Samples 130 116 134 255 403 134 159 85 198 154 59 170 158 63 114 57 76 182 136 110 70 52 43 105 135 198 142 41 62 95 42 2765 1113 3878 Table II. Participating Non PHLS Laboratories and number of meat and pâté samples. Meat Samples 8 57 9 20 22 6 7 129 Non Public Health Laboratory Aberdeen City Council Public Belfast City Hospital Dundee Scientific Services Edinburgh Analytical & Scientific Glasgow Scientific Services Kings Lynn & West Norfolk Royal Alexandra, Paisley Total 29 Pâté Samples 7 30 3 13 12 5 1 71 Total 15 87 12 33 34 11 8 200 Table III. Participating Food Safety Liaison Groups, number of premises visited and number of cold meat and pâté samples taken. Food Liaison Group Berkshire Buckinghamshire Cambridgeshire Cheshire Chester Cornwall Cumbria Derbyshire Devon Dorset Durham East Sussex Essex Gloucestershire Greater London NW Sector (LFCC*) Greater London SE Sector (LFCC*) Greater London SW Sector (LFCC*) Greater London NE Sector (LFCC*) Greater Manchester Hampshire & Isle Of Wight Hereford & Worcestershire Hertfordshire & Bedfordshire Humberside Kent Lancashire Leicestershire Lincolnshire Merseyside Norfolk North Yorkshire Northamptonshire Northumberland Norwich Nottinghamshire Oxfordshire Shropshire Somerset South Yorkshire Staffordshire Suffolk Surrey Tees Valley Tyne & Wear Warwickshire West Midlands West Of England West Sussex West Yorkshire Wiltshire Northern Ireland Food Group Scottish Food Liaison Group Wales Total *LFCC – London Food Coordinating Committee Premises 22 32 13 65 10 61 43 50 58 44 26 64 42 39 48 31 37 21 39 64 50 62 40 85 49 49 70 31 5 38 63 23 36 47 26 29 31 16 55 39 48 24 58 61 63 40 46 9 39 52 52 143 2288 30 Meat Samples Pâté Samples Total Samples 35 11 46 33 17 50 13 6 19 56 25 81 12 4 16 73 32 105 53 20 73 81 33 114 68 40 108 44 20 64 36 5 41 74 27 101 53 22 75 42 26 68 63 20 83 36 14 50 55 9 64 42 3 45 37 33 70 58 40 98 59 27 86 80 33 113 62 37 99 103 31 134 41 37 78 112 23 135 88 13 101 39 16 55 7 2 9 36 28 64 77 37 114 29 14 43 48 24 72 68 17 85 27 19 46 28 15 43 29 17 46 34 6 40 56 17 73 38 19 57 67 25 92 32 7 39 67 49 116 63 30 93 124 24 148 64 7 71 59 28 87 23 4 27 53 25 78 57 30 87 66 36 102 194 80 274 2894 1184 4078