Microbiological Quality of Ready-to-Eat Food Served in Schools in Wales, United Kingdom

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1 197 Journal of Food Protection, Vol. 72, No. 1, 2009, Pages Copyright, International Association for Food Protection Research Note Microbiological Quality of Ready-to-Eat Food Served in Schools in Wales, United Kingdom R. J. MELDRUM, 1 * P. T. MANNION, 2 AND J. GARSIDE, 3 ON BEHALF OF THE WELSH FOOD MICROBIOLOGICAL FORUM 1 Public Health Laboratory, National Public Health Service for Wales, Llandough Hospital, Penlan Road, Penarth CF64 2XX, UK; 2 National Public Health Service Microbiology Rhyl, Glan Clwyd Hospital, Rhyl LL18 5UJ, UK; and 3 Blaenau Gwent County Borough Council, Civic Centre, Ebbw Vale NP23 6XB, UK MS : Received 2 June 2008/Accepted 25 July 2008 ABSTRACT A survey of the general microbiological quality of ready-to-eat food served in schools was undertaken across Wales, United Kingdom. Of the 2,351 samples taken, four were identified as containing unsatisfactory counts of Escherichia coli, four contained unsatisfactory counts of Staphylococcus aureus, and one contained an unacceptable count of Bacillus cereus when compared with guidelines for the microbiological quality of ready-to-eat food published by the United Kingdom Public Health Laboratory Service in No samples contained detectable levels of Salmonella, Listeria species, or Clostridium perfringens. When compared with data on the general microbiological quality of food available in Wales, the food sampled from schools was of relatively better microbiological quality. The provision of food to schoolchildren in the United Kingdom is an area that has generated a significant amount of public interest in recent years. Most of that interest has focused on the nutritional quality of the food served in state schools (13, 17). Several high-profile initiatives have been proposed to ensure that children eat enough fruit and vegetables, drink plenty of water, and avoid foods that are considered to be unhealthy while at school (13, 17). The Welsh Food Microbiological Forum (WFMF) is a collaborative group that includes environmental health practitioners, microbiologists, and epidemiologists, as well as representatives from the United Kingdom Food Standards Agency and the Welsh Assembly Government (10, 14). The remit of this group is to consider food safety issues of relevance to Wales, a devolved part of the United Kingdom with a population of approximately 3 million. One of the main functions of the WFMF is to coordinate largescale food surveys across the whole of Wales. These surveys normally involve the 22 Welsh Local Authorities and the four food examination laboratories of the National Public Health Service for Wales. These surveys are based on epidemiological evidence from local outbreaks, general trends in foodborne disease in the United Kingdom and Europe or local pilot surveys. The aim of these surveys is to identify foods that might be associated with foodborne disease and develop and implement control measures. In 2006, the WFMF agreed to carry out a survey of school food with the aim of assessing the general microbiological quality of food served to children of school age (5 to 18 * Author for correspondence. Tel: ; Fax: ; richard.meldrum@nphs.wales.nhs.uk. years) across Wales. The rationale for carrying out this survey was an outbreak of Escherichia coli O157 in South Wales in September 2005, which was epidemiologically linked to cooked, sliced meats supplied to schools across the region. This outbreak was the largest ever seen in Wales and involved 157 cases. In light of this outbreak, it was decided by the WFMF members that it was important to assess the general microbiological quality of food served in schools in Wales to identify any further hazards present. A number of other outbreaks associated with food served in schools has been reported. In Japan, outbreaks of Salmonella, Campylobacter jejuni, Escherichia coli, and Staphylococcus aureus have been linked to school food (1, 12). In Wales the responsibility for education lies with the Welsh Assembly Department of Education, Lifelong Learning and Skills. This department of the Welsh Assembly Government provides funding for state education for the whole of Wales, oversees the curriculum, and maintains educational standards (3). However, the responsibility for public spending in individual schools lies with the Local Education Authorities (LEAs), which are part of each Local Authority. Wales has 22 LEAs, each with the legal responsibility for the provision of school meals within each Local Authority area. This responsibility can lie directly with the LEA itself or can be delegated by the LEA to an individual school, when it is then the responsibility of the school governors to provide school food. This responsibility includes ensuring that the food served in school meets certain nutritional standards (13, 17). The organization of school catering depends on the school and LEA concerned and varies across Wales. For example, some schools act independently

2 198 MELDRUM ET AL. J. Food Prot., Vol. 72, No. 1 and source their own supplies, whereas some LEAs have created large consortia to purchase food in bulk so that each school within those areas receive food from the same supplier(s). Sixteen Welsh Local Authorities use a third party verification system that requires suppliers to be accredited before they can supply food to any local authority premises, including schools. This accreditation service is provided in most cases by a single company. The accreditation process involves, variously, desk-top risk assessments, scrutiny of previous food hygiene inspection reports and visits to premises by competent inspectors. Annual revisits are made to accredited premises to ensure hygiene standards are maintained at an acceptable level. In Wales, with 1,555 primary schools (ages 5 to 12 years), 224 secondary schools (ages 12 to 18 years), and 43 special schools (15), no statistics are available for the number of school meals served in Wales, but data collected in January 2006 reported that from a total school pupil population of 495,000, 77,627 pupils were entitled to free school meals (15). MATERIALS AND METHODS Sampling. The members of the WFMF coordinated the survey, producing a survey protocol that was distributed to all Local Authorities in Wales. Samples were taken from schools within each Local Authority by authorized environmental health officers or technical officers. No particular food types were specified for sampling, and officers were instructed to randomly sample the range of ready-to-eat foods available to pupils from the point of service. Samples were then transported under temperature-controlled conditions to one of the four National Public Health Service food examination laboratories in Wales. Samples were processed on the day of delivery. Results were reported back to each individual Local Authority for action (if necessary) and were also collated centrally for analysis of the whole dataset. Sample preparation. Twenty-five grams of each sample ( 1 g) was aseptically removed from the packaging and placed into a sterile plastic bag (Sterilin Ltd., Aberbargoed, Wales, UK). With the use of a gravimetric diluter (AES Laboratoire, Combourg, France), a 10-fold dilution was made with maximum recovery diluent (Oxoid Ltd., Basingstoke, UK). The sample was then homogenized for 30 s in a stomacher machine (AES Laboratoire). Further serial dilutions (to 10 3 ) of this 10 1 dilution were then made with 9 ml of maximum recovery diluent. For the Salmonella test, a second 25-g ( 1 g) aliquot of sample was weighed out, diluted to 10 1, and homogenized with buffered peptone water (Oxoid Ltd.) instead of maximum recovery diluent. Aerobic colony count. For aerobic colony count (ACC), a spiral plater (Don Whitley, Shipley, UK) was used following the manufacturer s instructions. Plate Count Agar was used (Oxoid Ltd.). After inoculation, plates were incubated at 30 C ( 1 C) for 48 h ( 4 h). Counts were then made following the manufacturer s instructions. E. coli. The method was based on the Health Protection Agency (HPA) National Standard Method F20 (6). An aliquot of 0.5 ml of the 10 1 dilution was inoculated onto a tryptone bile X-glucuronide plate (Oxoid Ltd.) and spread with a sterile plastic spreader. The plate was incubated for 4hat30 C ( 1 C) and then for 18 h ( 2 h)at44 C in an automatic cycling incubator (Qualicool 260, LTE Scientific Ltd., Oldham, UK). The chromogenic substrate in the agar (5-bromo-4chloro-3indolyl- -D-glucoronic acid) detected the -glucoronidase reaction of E. coli, resulting in blue colonies. Listeria species, including L. monocytogenes. The method used was based on the HPA National Standard Method F19 (6). An aliquot of 0.5 ml of the 10 1 dilution was inoculated onto a Listeria selective agar (Oxford formulation) plate (Oxoid Ltd.) and spread with a sterile plastic spreader. The plate was incubated at 30 C ( 1 C) for 48 h ( 4 h). Typical colonies of Listeria were then subcultured onto blood agar plates (Oxoid Ltd.), and the identity was confirmed with the use of the API Listeria system following the manufacturer s instructions (biomérieux, Marcy l Etoile, France). Bacillus cereus. The method used was based on the HPA National Standard Method F15 (6). An aliquot of 0.1 ml of the 10 2 dilution was inoculated onto a B. cereus selective agar plate (Oxoid Ltd.) and spread with a sterile plastic spreader. The plate was incubated at 30 C ( 1 C) for 42 to 48 h. The plate was checked after 18 to 24 h of incubation, and typical Bacillus colonies were picked for confirmation that the plate had the potential to be overgrown after 48 h. Confirmation of B. cereus was made with the BBL Crystal GP system (Becton Dickinson Co., Shannon, Ireland), following the manufacturer s instructions. S. aureus. The method used was based on the HPA National Standard Method F12 (6). An aliquot of 0.5 ml of the 10 1 dilution was inoculated onto a Baird Parker agar plate (Oxoid Ltd.) and spread with a sterile plastic spreader. The plate was incubated at 37 C ( 1 C) for 44 to 48 h. After incubation, the plate was examined for typical colonies of S. aureus (black, shiny, convex colonies with a zone of opacity surrounded by a clear zone). The presence of S. aureus was confirmed by the DNase test with DNase agar (Oxoid Ltd.) and coagulase production with the Pro-Lab Prolex S. aureus latex kit (Pro-Lab Diagnostics UK, Neston, UK) following the manufacturer s instructions. Salmonella. The method used was based on the HPA National Standard Method F13 (6). As mentioned above, 25 g ( 1 g) of sample was homogenized in buffered peptone water. This homogenate was then poured into a sterile honey jar and incubated at 37 C ( 1 C) for 16 to 18 h. An aliquot of 0.1 ml of the buffered peptone water was inoculated into 10 ml of Rappaport-Vassiliadis broth and incubated at 41.5 C ( 1 C) for 24 h ( 3 h). An aliquot of 1.0 ml of the buffered peptone water was inoculated into Muller Kauffman tetrathionate broth and incubated at 37 C ( 1 C) for 18 to 24 h. The Rappaport-Vassiliadis and Muller Kauffman tetrathionate broths were subcultured onto xylose lysine desoxycholate agar and brilliant green agar and incubated at 37 C for 18 to 24 h. These plates were then examined for typical Salmonella colonies, and confirmation of presumptive Salmonella was carried out with the use of Poly O and Poly H serological agglutination reactions (Pro-Lab Diagnostics UK) and biochemical reactions with the API 20E kit (biomérieux), both following the manufacturers instructions. Clostridium perfringens. The method used was based on the HPA National Standard Method F14 (6). This test was not carried out on every food type sampled, only those deemed as potentially high risk for containing this organism. An aliquot of 1 ml of the 10 1 dilution was transferred into an empty sterile petri dish, and 15 ml of cooled, molten tryptose sulfite cycloserine agar (Oxoid Ltd.) to which 60 l of Oxoid Perfringens Selective supplement had been added was poured into the petri dish. The dish was then rotated gently to mix. After setting, the agar was overlaid with

3 J. Food Prot., Vol. 72, No. 1 MICROBIAL QUALITY OF SCHOOL FOOD 199 TABLE 1. Summary of current guideline limits for ready-to-eat foods (5) Parameter Food type a Category Guideline limit (CFU/g) ACC 1 Unsatisfactory Unsatisfactory Unsatisfactory Unsatisfactory Not applicable No limit E. coli 1 5 Unsatisfactory 100 Listeria spp. 1 5 Unsatisfactory 100 Salmonella 1 5 Unacceptable Detected in 25 g L. monocytogenes 1 5 Unacceptable 100 S. aureus 1 5 Unsatisfactory 10 2 to Unacceptable 10 4 C. perfringens 1 5 Unsatisfactory 10 2 to Unacceptable 10 4 B. cereus 1 5 Unsatisfactory 10 4 to Unacceptable 10 5 a Type 1, burgers, meat pies and pasties, and mousse; type 2, ready-to-eat meals, unsliced poultry, unfermented cooked sausages, cakes without dairy cream, cooked vegetables, and ice cream; type 3, sliced meats (excluding ham), seafood meals, and cakes with dairy cream; type 4, cooked ham, smoked fish, prepared mixed salads, and sandwiches without salad; type 5, fresh fruit and vegetables, yoghurt, fermented meats, and sandwiches with salad. another 15 ml of tryptose sulfite cycloserine and then set aside to set. The plate was then incubated anaerobically at 37 C ( 1 C) and read after 24 and 48 h. Any black colonies were then subcultured onto blood agar plates and then incubated both aerobically and anaerobically at 37 C ( 1 C) for 18 to 24 h. Any colony that failed to grow aerobically was then inoculated into motility nitrate medium and lactose gelatin medium for confirmation. RESULTS AND DISCUSSION The survey ran from September 2006 to July Overall, 20 of the 22 Local Authorities in Wales participated in the survey. Of 1,604 state schools within these participating Local Authority areas, 1,362 were primary schools, 202 secondary schools, and 40 special schools (15). Samples were taken from 448 schools (27.9%). In proportional terms, 23.4% of the primary schools, 61.4% of the secondary schools, and 10% of the special schools within the participating Local Authority areas were visited at least once during the survey. Of the 2,351 samples taken during the course of the survey, 1,383 (58.8%) were from primary schools, 955 (40.6%) from secondary schools, and 13 (0.6%) from other schools (mixed primary and secondary schools or special educational needs). All samples were tested for the full range of organisms, apart from C. perfringens, which was only tested for in samples deemed to be of potential high risk of containing this pathogen (n 1,032). Some schools were visited more than once. The range of foods taken reflected the range of food served to schoolchildren and were all ready to eat. Food types sampled included cooked burgers (n 91), cakes (with and without dairy cream) (n TABLE 2. Overall rates for all samples Parameter Satisfactory Acceptable Rate (%) Unsatisfactory Unacceptable ACC a N/A E. coli N/A Listeria N/A Salmonella N/A N/A 0.00 L. monocytogenes N/A 0.00 S. aureus C. perfringens B. cereus a Rates for ACC only refer to those for food types included in the Public Health Laboratory Service ready-to-eat guidelines (excluding fermented products and those containing fresh fruit, vegetables, or both). 144), all types of cheese (n 16), all types of cooked meats (n 141), coleslaw (n 74), desserts (including cheesecakes, fruit pies, fruit salads, ice cream, frozen yogurt, mousse, and trifle; n 111), raw and cooked fruit and vegetables (including cooked potatoes, cooked carrot, cooked sweet corn, uncooked apple, raw carrot, raw pepper, and raw cucumber; n 219), pies and pasties (n 63), gravy (n 169), green salads (n 130), sauces (sweet and savory; n 135), cooked poultry (n 63), quiche (n 12), rice (n 91), various ready-to-eat meals (n 553), sandwiches (n 185), and cooked sausages (n 111). The results from the microbiological examinations were compared with guidelines published by the Public Health Laboratory Service in 2000 (5). These guidelines provide guidance to public health bodies and Local Authorities regarding the relative quality of food sampled so that an informed judgment can be made. The guidelines have four categories: satisfactory, acceptable, unsatisfactory, and unacceptable. In these guidelines, the term acceptable is used as an index reflecting a borderline limit of microbiological quality, unsatisfactory is a result that would require further sampling or inspection of the premises concerned, and unacceptable is a result that suggests that urgent action is required and could be used as the basis for a prosecution under United Kingdom food safety law (5). The guidelines include limits for aerobic colony count, indicators, and pathogens. An overview of these guideline limits is presented in Table 1. An overview of the results found in this survey is presented in Table 2. The survey found that 48 samples (2.0%) fell into the unsatisfactory category when compared with the guidelines. However, 39 (1.7%) of these samples were unsatisfactory because of high ACC only and were satisfactory for all other measured parameters. Of the remaining unsatisfactory samples, four (0.17%) were unsatisfactory because of E. coli, four (0.17%) were unsatisfactory because of S. aureus, and one (0.04%) was unacceptable because of a high B. cereus count. The sample types with unsatisfactory counts of E. coli were three green salads (120, 640, and 1,140 CFU/g) and one sample of cooked rice (340 CFU/g). For

4 200 MELDRUM ET AL. J. Food Prot., Vol. 72, No. 1 TABLE 3. Comparison of unsatisfactory rates a Parameter Unsatisfactory rate in school food Unsatisfactory rate from all-wales sampling program b ACC E. coli Listeria Salmonella 0.0* 0.006* L. monocytogenes 0.0* 0.2* S. aureus C. perfringens B. cereus 0.04* 0.08* a Values with asterisks (*) indicate unacceptable ratings. b Rates are from Meldrum et al. (11). S. aureus, the sample types with unsatisfactory counts were two green salads (120 and 230 CFU/g), a chicken curry meal (400 CFU/g), and a ham sandwich (320 CFU/g) that did not contain salad (n 12). For B. cereus, the sample containing an unacceptable level ( CFU/g) of this potential pathogen was a cake containing dairy cream (n 12). No samples had detectable levels of Listeria, Salmonella, C. perfringens, or Salmonella. When these data were compared with other data collected from the microbiological examination of food sampled from retail and catering premises in Wales between 1995 and 2003 (11), it was found that the unsatisfactory rates were generally lower in the food sampled from schools (Table 3). It should be noted that the all-wales dataset used for comparison (11) did have a total of more than 15,000 samples and therefore would be more statistically reliable than a dataset of 2,351. It also should be noted that the all-wales sampling dataset did include food bought in shops and supermarkets rather than exclusively from catering establishments, but the dataset does serve as a useful comparison to gauge the relative quality of the food taken from schools. Tessi et al. (18) sampled 101 food samples in total from one centralized school kitchen in Argentina and reported unsatisfactory rates in 35 salads of 74.3% for ACC and 63% for Enterobacteriaceae. These authors found none of these salads had any unsatisfactory counts of B. cereus and none had detectable levels of Salmonella, S. aureus, E. coli, or C. perfringens (18). Cooked hot meals (n 66), sampled in the same study, had no detectable levels of any indicators or pathogens. A study of the microbiological quality of ready-to-eat salad vegetables found that 3% of samples were unsatisfactory for E. coli and one sample ( 1%) was unsatisfactory for L. monocytogenes (16). A survey of rice and chicken sandwiches found that rice samples were unsatisfactory for B. cereus (10%) and the sandwiches were unsatisfactory for E. coli (9%) and S. aureus (6%) (8). A study in New Zealand found the presence of L. monocytogenes in 1% of sliced, cooked ham samples (19). A similar United Kingdom based survey found that ready-to-eat cold sliced meats were unsatisfactory for the presence of L. monocytogenes in two samples ( 1%) (4). The presence of unsatisfactory and unacceptable levels of Campylobacter, Salmonella, and E. coli O157 was found in ready-to-eat burgers (9). A survey of fresh produce on sale in Norway examined precut salads, herbs, and fruit and found S. aureus in none of the samples of salad (7). S. aureus was found in samples of salad and ready-to-eat meals served in military cafeterias in Turkey (2). From the results of this survey of food available in schools across Wales, it would seem fair to conclude that, in relative terms, the food sampled from schools was generally of good microbiological quality. However, although the vast majority of samples taken were satisfactory, a number of food samples did contain pathogenic organisms at either unsatisfactory or unacceptable levels and therefore presented a potential hazard to the consumer. Because this survey was a snapshot of one academic year, it is recommended that periodic sampling and examination of food available in schools in Wales be undertaken to continue to monitor the general microbiological quality and identify any developing trends. REFERENCES 1. Abe, K., S. Yamamoto, and K. Shinagawa Economic impact of an Escherichia coli O157 outbreak in Japan. J. Food Prot. 65: Aycicek, H., S. Cakiroglu, and T. H. Stevenson Incidence of Staphylococcus aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control 16: BBC Action Network. 5 September The schools system in Wales. Available at: Accessed 1 June Elson, R., F. Burgess, C. L. Little, and R. T. Mitchell Microbiological examination of ready-to-eat cold sliced meats and pate from catering and retail premises in the UK. J. Appl. Microbiol. 96: Gilbert, R. J., J. de Louvois, T. Donovan, C. Little, K. Nye, C. D. Ribeiro, J. Richards, D. Roberts, and F. J. 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