Survey of Salmonella Contamination of Raw Shell Eggs Used in Food Service Premises in the United Kingdom, 2005 through 2006

19 Journal of Food Protection, Vol. 71, No. 1, 2008, Pages 19 26 Copyright, International Association for Food Protection Survey of Salmonella Contamination of Raw Shell Eggs Used in Food Service Premises in the United Kingdom, 2005 through 2006 C. L. LITTLE, 1 * J. R. RHOADES, 1 L. HUCKLESBY, 1 M. GREENWOOD, 2 S. SURMAN-LEE, 3 F. J. BOLTON, 4 R. MELDRUM, 5 I. WILSON, 6 C. MCDONALD, 7 E. DE PINNA, 1 E. J. THRELFALL, 1 AND C.-H. CHAN 8 1 Department of Gastrointestinal Infections, Health Protection Agency Centre for Infections, 61 Colindale Avenue, London NW9 5EQ, UK; 2 Microtech Services (Wessex) Limited, 1 Kinson Road, Bournemouth BH10 4AQ, UK; 3 Health Protection Agency London Food, Water and Environmental Microbiology Services Laboratory, 61 Colindale Avenue, London NW9 5EQ, UK; 4 Health Protection Agency North West Manchester Laboratory, Manchester Royal Infirmary, Manchester M13 9WZ, UK; 5 Microbiology Laboratory NPHS for Wales, Llandough Hospital, Penlan Road, Penarth CF64 2XX, UK; 6 Bacteriology Department, Belfast City Hospital Trust, Lisburn Road, Belfast BT9 7AB, UK; 7 Public Analyst Laboratory, Glasgow Scientific Services, 64 Everard Drive, Glasgow G21 1XG, UK; and 8 Food Standards Agency, Microbiological Safety Division, Aviation House, 125 Kingsway, London WC2B 6NH, UK MS 07-386: Received 25 July 2007/Accepted 8 September 2007 ABSTRACT This survey was launched after an unusual number of Salmonella Enteritidis outbreaks associated with the use of eggs in food service premises in England and Wales. Between November 2005 and December 2006, 9,528 eggs (1,588 pooled samples of 6 eggs) were collected from 1,567 food service premises in the United Kingdom, most of which (89%) were produced in the United Kingdom. Salmonella was isolated from 6 (0.38%) pools of eggs. Of these, 5 (0.31%) were Salmonella Enteritidis, which were further characterized to phage types (PTs): PT 4 (0.19%), PT 8 (0.06%), and PT 12 (0.06%). Salmonella Mbandaka was also isolated (0.06%). Salmonella was detected from five and one of pooled eggs samples that were produced in the United Kingdom and Germany, respectively; these were from different producers. The study showed evidence of poor egg storage and handling practices in food service premises, in that 55% did not store eggs under refrigerated conditions; 20.7% of eggs had expired best before dates or were in use after 3 weeks of lay, indicating poor stock rotation; and 37.1% pooled eggs not intended for immediate service. Eggs are a commonly consumed food that may occasionally be contaminated with Salmonella at different rates, according to their country of origin. The food service sector needs to be aware of this continuing hazard, receive appropriate food safety and hygiene training on storage and usage of raw shell eggs, adopt appropriate control measures, and follow advice provided by national food agencies in order to reduce the risk of infection. Infection with Salmonella Enteritidis remains an important public health problem in Europe and some parts of the world (9, 16). Outbreaks caused by Salmonella have been associated with a variety of foods. However, outbreaks caused by Salmonella Enteritidis are closely associated with eggs and egg products (5, 8, 9, 22, 24, 36, 39). Concerns are such that the European Commission Scientific Committee on Veterinary Measures relating to Public Health has identified eggs and egg products containing raw eggs as a food group that poses a hazard to public health (12). In the United Kingdom, the predominant phage type (PT) responsible for eggborne Salmonella Enteritidis infection has been PT4 (22). However, since 2002, the emergence of egg-associated Salmonella Enteritidis infection caused by phage types other than PT4 has been noted. Three-quarters of these outbreaks occurred in commercial food service premises (25, 26). This resurgence is thought to be associated with major changes in market supply with the import of eggs from other egg producers in European Union member states, in which there was a lack of vacci- * Author for correspondence. Tel: 44(0)20 8327 7931; Fax: 44(0)20 8327 7112; E-mail: christine.little@hpa.org.u.k. nation of layer flocks against Salmonella or controlled assurance schemes in place (16, 37, 42). Raw shell eggs have continued to be implicated as a source or vehicle of Salmonella Enteritidis infection in outbreaks associated with commercial food service premises in the United Kingdom (25, 26) despite almost 20 years of national guidance on this issue (6, 7, 17). The risk of Salmonella Enteritidis transmission can be reduced greatly by the use of pasteurized eggs, particularly in lightly cooked dishes (17). Information on the incidence of high-risk egg preparation practices that allow growth or survival of Salmonella Enteritidis in eggs in food service premises is needed. Surveys and investigations of eggs for Salmonella contamination have played an important role in understanding the extent and pattern of contamination. Studies of eggs appear to indicate that those originating from some countries outside the United Kingdom have a higher rate of Salmonella contamination, compared with United Kingdom produced eggs. In 2005 to 2006, a survey of non United Kingdom eggs at retail sale found a 3.3% weighted prevalence estimate of Salmonella; 2.6% contained Salmonella Enteritidis (34). The Health Protection Agency (HPA) public health investigation of eggs during 2002 to 2004 showed

20 LITTLE ET AL. J. Food Prot., Vol. 71, No. 1 a higher rate (5.9%) of Salmonella contamination in non United Kingdom eggs used in food service premises (33). In contrast, rates of Salmonella contamination in United Kingdom produced eggs appear to have decreased significantly (1995 and 1996, 1%; 2003, 0.3%), clearly indicating an improved situation (1, 18). The United Kingdom Food Standards Agency (FSA) has commissioned a series of raw shell egg surveys, including this survey of eggs at the food service level, one of non United Kingdom eggs at the retail level, and one of United Kingdom retail eggs (18, 34). The results will contribute to the identification of where particular contamination problems are occurring and hence where interventions to reduce Salmonella contamination might best be focused. The aims of the food service survey were to examine the use of raw shell eggs and to provide an estimate of Salmonella contamination of eggs used in these premises across the United Kingdom. MATERIALS AND METHODS Sample collection. There was no market share data on the origin of eggs used in the United Kingdom food service sector, and therefore, there was no basis on which to construct a sampling frame. However, registered food service premises lists held by local authority environmental health departments were used to derive an approach to sampling. Food service premises were selected at random from the local authorities databases of food businesses via a random number generator or every 10th entry, and if suitable samples were collected. Any food service premises could be included in the study, provided they mainly obtained their eggs from wholesale suppliers and not retail premises. Samples of eggs were collected by staff from 238 environmental health departments in England, Wales, Scotland, and Northern Ireland, between November 2005 and December 2006, using a standardized protocol and questionnaire. Information collected on the premises included type, cuisine, and use of raw shell eggs, and that on eggs included size, visual appearance, production method, and egg-packing station and producer codes (11). Samples were transported to the laboratory in accordance with the Food Law Code of Practice and Practice Guidance (19). Sample examination and isolation of Salmonella. Samples of raw shell eggs were examined in 28 official food control laboratories. Upon receipt of the sample, the examining laboratory recorded the appearance of the eggs, i.e., whether they were clean, dirty, or visibly cracked. If any marks (e.g., fecal material, dust, mud, blood, and the contents of other eggs) other than natural markings or printed marks were present, then eggs were considered dirty. If one egg within a group of eggs had visible signs of contamination, then the whole group would be described as dirty. Through this classification process, the number of dirty eggs reported in this survey may be higher than what is actually supplied to the food service sector. There is a degree of tolerance allowed for table (Grade A) eggs and this is covered in European Commission legislation (15). At packing centers, United Kingdom eggmarketing inspectors may downgrade if quality faults exceed 5% of the sample checked from any single batch. At any other marketing stage (e.g. wholesale, retail, catering premises) an additional 2%, taking the tolerance up to 7% total, is permitted before egg-marketing inspectors may downgrade eggs. The shells and contents of eggs were tested separately to provide an estimate on shell and contents contamination. Pooled samples of six eggs were aseptically cracked against the rim of a sterile screw-top container, and the shells and egg contents were divided and placed into separate containers. The presence of Salmonella was sought in accordance with BS EN ISO 6579 (3) except that an equal volume of buffered peptone water (BPW) was added to egg contents, and sufficient BPW was added to shell samples to completely cover them. After mixing the BPW suspensions they were incubated at 37 C for 18 2h. Incubated BPW broths were subcultured into selective enrichment broths: 0.1 to 10 ml of Rappaport-Vassiliadis soy peptone broth and 1 to 10 ml of Muller-Kauffmann tetrathionatenovobiocin broth and incubated at 41.5 and 37 C, respectively, for 24 3 h. The broths were subcultured onto xylose lysine deoxycholate agar and modified brilliant green agar plates and incubated at 37 C for 24 3 h. All plate and broth media were supplied by Oxoid (Basingstoke, UK). Serological and biochemical confirmation were carried out on typical or suspect colonies of Salmonella from each agar plate. The method above included the following modifications. The Rappaport-Vassiliadis soy peptone broth and Muller-Kauffmann tetrathionate-novobiocin broths were reincubated for a further 24 to 26 h and subcultured to xylose lysine deoxycholate agar and brilliant green agar. On examining xylose lysine deoxycholate agar and brilliant green agar plates for the presence of Salmonella, plates with no Salmonella colonies were reincubated for a further 22 2 h and then reexamined. Isolates of Salmonella were sent to the Laboratory of Enteric Pathogens, HPA Centre for Infections for serotyping and phage typing for Salmonella Enteritidis (43), and antimicrobial susceptibility testing (21). Statistical analysis. Data analysis was performed using Microsoft Excel and Epi Info, version 6.04d. Proportions were compared using the chi-squared test and Fisher s exact test. A probability value of less than 5% was deemed to be significant. RESULTS A total of 9,528 eggs (1,588 pooled samples of 6 eggs) were collected from 1,567 food service premises, of which 6 (0.38%) samples were contaminated with Salmonella (Table 1). Of these, 5 (0.31%) were Salmonella Enteritidis, which were characterized to PT 4 (0.19%), PT 8 (0.06%), and PT 12 (0.06%). Of the 6 samples contaminated with Salmonella, 1 had both shell and contents positive for this organism, while the other 5 were positive only from shells (Table 1). None of the isolates exhibited antimicrobial resistance. During the survey, eggs found to be contaminated with Salmonella were reported by the FSA to the appropriate authorities in the countries of origin. Egg production details in relation to presence of Salmonella. Eggs collected were produced in eight different countries (Table 2), with most originating from the United Kingdom (89%). Salmonella was detected from 0.4% of samples from the United Kingdom and 2.6% from Germany. Most of the eggs sampled (83.5%) were labeled as cage (Table 2). Salmonella was detected in 0.4 and 0.6% of the cage and free range produced egg samples, respectively. The 5 samples contaminated with Salmonella Enteritidis were from caged hens, while the other sample with Salmonella Mbandaka was from free range hens. All Salmonella-contaminated samples originated from different egg producers (Table 1). Most eggs sampled (73.9%) were medium sized (Table

J. Food Prot., Vol. 71, No. 1 SALMONELLA CONTAMINATION OF FOOD SERVICE EGGS 21 TABLE 1. Information on Salmonella-contaminated egg samples from food service premises (n 6) Country of origin Assurance scheme Stamp mark a Packing station code Salmonellacontaminated part of egg Salmonella serotype/phage type United Kingdom Lion Quality b 3UK11063 Not known Shell Enteritidis/PT4 United Kingdom Not known 3UK11462 UK/4/021 Shell Enteritidis/PT4 United Kingdom Lion Quality 3UK11043 UK/1/998W Shell Enteritidis/PT12 United Kingdom Laid in Britain c 1UK15054 UK/6/548 Shell Mbandaka United Kingdom Lion Quality 3UK10641 Not known Shell and contents Enteritidis/PT4 Germany Not known 3DE0351631 Not known Shell Enteritidis/PT8 a Egg stamp mark codes are in the format X.YY.12345, where X is a digit representing the farming method, e.g., 0 organic, 1 free range, 2 barn, 3 cage; YY are letters representing the country of origin; and 12345 are digits representing the unique identification number of the farm. b The Lion Code of Practice accounts for 80% of United Kingdom egg production, applies to production from lay to pack, and includes vaccination of pullets against Salmonella Enteritidis, biosecurity measures, hazard analysis critical control point, and full traceability and feed controls. c The Laid in Britain Scheme accounts for 5% of United Kingdom egg production, includes use of competitive exclusion and biosecurity measures, but does not include an element of vaccination. 2). Salmonella-positive samples were from medium-sized (0.3%) and large-sized (0.6%) eggs. Over a fifth (21.1%) of the eggshells in the pooled samples were recorded as having a dirty appearance, i.e., visibly soiled and/or the presence of fecal matter (Table 2). Salmonella was detected from 1.5 and 0.1% of those with dirty and clean eggshells, respectively. None of the egg samples examined were visibly cracked. Egg assurance schemes apply from lay to pack. Of the egg samples where assurance scheme information was known, most eggs sampled were recorded to be from the Lion Quality (32.7%, laid by hens vaccinated against Salmonella Enteritidis) and Laid in Britain (4.3%, which includes use of competitive exclusion but not vaccination) assurance schemes (Table 2). Twenty-seven (1.7%) samples came from hens that had been vaccinated against Salmonella, but the information provided did not allude as to whether or not the eggs were produced according to any specific assurance schemes. All egg samples produced within an assurance scheme or from vaccinated flocks were of United Kingdom origin. There was no evidence of any difference between the Salmonella contamination rate in eggs produced in the United Kingdom under egg assurance schemes (0.7%, 4 of 608) and eggs produced in the United Kingdom, where this information was not known (0.3%, 2 of 804) (P 0.4118). However, it is possible that eggs where information on assurance schemes was not known could also have come from vaccinated flocks. Traceability of eggs. Most samples (94%) had a stamp mark on the eggshell. All six samples that had Salmonella present were from eggs that had stamp mark details on the eggshell (Table 1). Over half of the samples (54.6%) had a packing station number available. When the packing station details were unknown, this was because the original packaging was not available. Shelf life of egg samples in relation to presence of Salmonella. The best before date (BBD) of eggs must not exceed 28 days from the date of lay (15). The BBD was available for 67.3% (1,070) of eggs sampled. The number of days remaining until consumption (i.e., number of days between the date sampled and the BBD) was determined and is provided in Table 3. Additionally, eggs must reach the final consumer (user) within 21 days from the date of lay (13), which means that eggs purchased by caterers should not have less than 7 days left before the BBD and should be used by the BBD. Three percent of egg samples were in use after their BBD (Table 3); these were in breach of the BBD requirements (15), and 17.6% were beyond the 21-day limit, before which the eggs should reach the final consumer. Three of the six pools of eggs containing Salmonella had 7 days left of shelf life. Food service premises details and use of eggs in relation to presence of Salmonella. Fast-food facilities (18%), cafés (17.8%), restaurants (17.7%), hotels (13.2%), pubs (11.9%), and institutional food service facilities (10.8%) formed most (89.4%) of the 1,567 premises visited (Table 4). Salmonella was detected from six samples of eggs collected from institutional food service facilities (1), fast-food facilities (1), restaurants (1), pubs (1), and in-store restaurants (2) visited. Most food service premises sampled served a general or mixed cuisine, or traditional British or Irish meals (53.6%) (Table 4). Among the categories of food service premises visited, almost all carried out the practice of pooling eggs for use during the day, with half of institutional (50.9%), hotels (50%), and restaurants (47.3%) carrying out this practice (Table 4). This finding was highly significant when comparing institutional food service facilities, hotels and restaurants with all other food service premises visited (P 0.0001). The practice of pooling eggs for use during the day and also at ambient temperature was shown to be predominant in those premises serving Chinese cuisine (77.8% pooled eggs; 40.7% pooled eggs stored at ambient temperature) (Table 4). These findings were highly significant when comparing Chinese cuisine with general and

22 LITTLE ET AL. J. Food Prot., Vol. 71, No. 1 TABLE 2. Production details of egg samples and Salmonellapositive pools Egg details Egg pools examined (n 1,588) a Salmonellapositive pools (n 6) Country of origin United Kingdom 1,413 89 5 0.4 Spain 48 3 0 Germany 38 2.4 1 2.6 The Netherlands 33 2.1 0 France 27 1.7 0 Portugal 8 0.5 0 Republic of Ireland 1 0.1 0 Poland 1 0.1 0 Mixed origin: United Kingdom and Spain 2 0.1 0 Not known 17 1.1 0 Production type Cage 1,326 83.5 5 0.4 Free range 159 10 1 0.6 Barn 40 2.5 0 Organic 2 0.1 0 Mixed sample 3 0.2 0 Not known b 58 3.7 0 Egg size Small ( 53 g) 38 2.4 0 Medium (53 to 63 g) 1,174 73.9 4 0.3 Large (63 to 73 g) 315 19.9 2 0.6 Extra large ( 73 g) 9 0.6 0 Other or not known 52 3.3 0 Condition of eggs Clean 1,246 78.4 1 0.1 Dirty 335 21.2 5 c 1.5 Not stated 7 0.4 0 Assurance scheme Lion Quality d 519 32.7 3 0.6 Laid in Britain d 69 4.3 1 1.5 Vaccinated against Salmonella e 27 1.7 0 Mixed sample: Lion Quality and not known 3 0.2 0 Not known 970 61.1 2 0.2 a Each sample comprised 6 eggs. b Not known due to lack of producer stamp mark, or details being illegible, on shells. c Eggshells soiled with: hen feces (4), contents of other egg (1). d Key to Lion Quality and Laid in Britain: see Table 1. e Information provided did not allude as to whether or not the eggs were produced according to any specific assurance schemes. mixed, British and Irish, sandwich and fried, and grill and fried cuisines (P 0.0001). Over half (55%) of the food service premises visited stored raw shell eggs at ambient temperature (Table 5). Salmonella was recovered from eggs stored at ambient (0.5%) and chilled (0.3%) temperatures. Eggs were broken, mixed, and pooled prior to use in 37.1% of food service premises (Table 5). Of these, the number of eggs pooled were mostly TABLE 3. Remaining days until expiration of best before date of egg samples used by food service premises, and Salmonella-positive pools Remaining days until bestbefore date Pools of eggs examined (n 1,070) a Salmonella-positive pools (n 5) 22 28 74 6.9 0 15 21 312 29.1 1 0.3 8 14 463 43.3 1 0.2 0 7 188 17.6 3 1.6 0 (expired) b 33 3.1 0 a Each sample comprised 6 eggs. b Best before date of eggs exceeded 28 days; in breach of European Commission regulation no. 557/2007 (11). less than 12 (57.5%) or between 12 and 36 eggs (33.4%), and left for less than 2 h before use (81.6%) at ambient (47.3%) or chilled (47.2%) temperature (Table 5). DISCUSSION Eggs are a commonly consumed food that may occasionally be contaminated with Salmonella at different rates according to their country of origin. A previous United Kingdom survey carried out in 2003 on food service eggs, of which most were of United Kingdom origin, uncovered a rate of Salmonella contamination of 0.30% (10), similar to that found in the current survey (0.38%). An examination of the surveys carried out in the United Kingdom on domestically produced eggs from 1995 to 2003 illustrates the decline in Salmonella contamination of eggs (1, 18), which is most likely to be due to the control measures introduced toward the end of the 1990s. Over the course of these 8 years, the prevalence of Salmonella in eggs has declined threefold, from 0.98 to 0.30%. This decrease has been reflected by the fall in the overall incidence of Salmonella Enteritidis contamination in United Kingdom produced eggs (England in 1995 and 1996, 0.82%; 2003, 0.28%) and especially Salmonella Enteritidis PT 4 (England in 1995 and 1996, 0.58%; 2003, 0.14%) (1, 18). The trend in the decline in Salmonella contamination of eggs appears not to be reflected in retail non United Kingdom eggs during 2005 and 2006, during which a 3.3% weighted estimated prevalence of Salmonella was found (34). The current survey saw a large number of United Kingdom eggs sampled (89%). This approximately reflects the United Kingdom egg market, in which most of the eggs consumed are obtained from United Kingdom sources, and non United Kingdom eggs only obtained when the United Kingdom supply falls. The volume of eggs imported to the United Kingdom therefore fluctuates throughout the year and closely reflects supply and demand. Although only a small proportion of the eggs sampled were of non United Kingdom origin in this survey, the nature of the United Kingdom food service egg market may allow the sporadic introduction of highly contaminated eggs (33). In all six contaminated egg samples, Salmonella was found to be on the egg; one was also contents positive.

J. Food Prot., Vol. 71, No. 1 SALMONELLA CONTAMINATION OF FOOD SERVICE EGGS 23 TABLE 4. Food service premises (n 1,567) type and cuisine regarding the use of pooled eggs Premises details No. (%) of food service premises No. (%) of pooling eggs for use during the day No. (%) of storing pooled eggs at ambient temp Premises type Fast food 282 (18) 87 (30.9) 43 (15.3) Café 279 (17.8) 99 (35.5) 57 (20.4) Restaurant 277 (17.7) 131 (47.3) 71 (25.6) Hotel 208 (13.3) 104 (50) 30 (14.4) Pub 187 (11.9) 43 (23) 14 (7.5) Institutional 169 (10.8) 86 (50.9) 41 (24.3) In-store restaurant 84 (5.4) 23 (27.4) 12 (14.3) Roadside food service 67 (4.3) 11 (16.4) 8 (11.9) Event caterer 10 (0.6) 4 (40) 2 (20) Transportation 4 (0.2) 0 0 Type of cuisine General/mixed 458 (29.2) 175 (38.2) 68 (14.8) British/Irish 382 (24.4) 150 (39.3) 66 (17.3) Sandwich/fried 219 (14) 70 (32) 40 (18.3) Grill/fried 188 (12) 47 (25) 25 (13.3) Chinese 81 (5.2) 63 (77.8) 33 (40.7) Italian 25 (1.6) 7 (28) 4 (16) European 12 (0.8) 9 (75) 2 (16.7) Indian 10 (0.6) 3 (30) 0 Thai 7 (0.4) 3 (42.9) 1 (14.3) Vietnamese 5 (0.3) 2 (40) 1 (20) French 4 (0.3) 2 (50) 2 (50) American 3 (0.2) 2 (66.7) 0 Other (Greek, Mediterranean, Japanese, Spanish, Swedish, kosher, seafood, vegetarian) 10 (0.6) 4 (40) 2 (20) Not stated 163 (10.4) 51 (31.3) 34 (20.9) There is an obvious cross-contamination risk from this external contamination, in that the organism can be transferred to other surfaces (e.g., hands) or to the egg contents during breaking of the shells. The presence of Salmonella on the surface of the shells of eggs therefore represents a potential risk to public health, just as well as contamination of the contents of the egg. Surface contamination may be the result of either infection of the lower reproductive tract of hens or fecal contamination (27). Reduction of this risk requires measures to be implemented at farms and packing stations to further reduce the prevalence of contamination and precautions are required by retailers and caterers to minimize spread, including adequate cooking of eggs and prevention of cross-contamination. Thirty-nine percent of egg samples used in the food service premises were produced from laying hens vaccinated against Salmonella or under a controlled assurance scheme. The World Health Organization Food and Agriculture Organization of the United Nations risk assessment of Salmonella Enteritidis in eggs indicates that a reduction in the prevalence of Salmonella Enteritidis in poultry flocks is directly proportional to a lower risk to human health (44). Vaccination of layer flocks, or those certified as free from Salmonella Enteritidis and Salmonella Typhimurium under controlled assurance schemes, combined with improved flock hygiene, appears to have made a significant impact on the prevalence of Salmonella contamination of eggs and on human Salmonella infection (1, 23). Targets for the reduction of Salmonella in laying hens within each member state were introduced in the European Union during 2006, with the first target deadline set for 2008. There will also be mandatory vaccination of layer hens against Salmonella from 2008 onward for layer hen holdings in member states with a Salmonella prevalence of 10% or more (14). In addition, from 2010 on, eggs from Salmonella-infected flocks will need to be treated in a manner that guarantees the elimination of Salmonella (14), e.g., eggs from contaminated farms will be sent for heat processing and will not be allowed to enter the fresh table-egg market; this is currently under review by the European Commission. Food safety concerns identified in relation to use of eggs in food service premises included the failure to observe BBDs and/or the advice that eggs should be consumed within 3 weeks of lay (i.e., by the sell by date) (13), and inappropriate storage temperature. The food service sector should pay close attention to egg stock rotation and refrigeration, as combining these is an easily achieved control measure to prevent low levels of salmonellae from achieving harmful population sizes (17, 35). If present, Salmonella can grow rapidly in eggs stored at room temperature, and growth is strongly governed by the age of the egg (4, 27, 31). The advantages of low-temperature storage of shell eggs are that salmonellae are less able to multiply, and the yolk membrane remains essentially intact for long periods of storage. This is particularly important in the commercial kitchen environment, where temperature fluc-

24 LITTLE ET AL. J. Food Prot., Vol. 71, No. 1 TABLE 5. Storage and use of eggs by food service premises, and Salmonella-positive pools Food service premises (n 1,567) Salmonella-positive pools (n 6) a Temp at which eggs are stored Chilled ( 8 C) 618 39.4 2 0.3 Ambient ( 8 C; range, 9 to 30 C) 862 55 4 0.5 Not stated 87 5.6 0 Multiple eggs broken, mixed, and pooled together for use during the day Yes 581 37.1 1 0.2 No 908 57.9 5 0.6 Not known 78 5 0 Eggs pooled (n 581) 12 334 57.5 0 12 36 194 33.4 1 0.5 36 53 9.1 0 Time pooled eggs are left before use (n 581) 2 h 474 81.6 0 2to 4 h 48 8.3 1 2.1 4to 6 h 24 4.1 0 6 h 27 4.6 0 Not known 8 1.4 0 Storage temp of pooled eggs (n 581) Ambient 275 47.3 0 Chilled 274 47.2 0 Not known 32 5.5 1 3.1 a Each sample comprised 6 eggs. tuations can accelerate changes to yolk permeability, allowing invasion of yolk contents and multiplication of Salmonella Enteritidis. Food safety guidance for the food service sector should also include storing eggs at or below 8 C. Other high-risk practices such as mixing and pooling shelled eggs for use during the day also occurred in food service premises, with institutional facilities, hotels and restaurants, and especially those serving Chinese cuisine, which are significantly more likely to carry out this practice. The FSA s Safer Food Better Business scheme for Chinese cuisine advises that if eggs are pooled for later use, then the liquid egg mix should be stored in the refrigerator (20). Food poisoning risks are multiplied when eggs contaminated with Salmonella are bulked with other eggs in food service, as this makes contaminated raw material available to a large number of consumers, and also if kept in a warm kitchen environment increases the potential for multiplication of the organism. Cross-contamination can also occur during egg preparation (2, 30), particularly when egg mixes are aerosolized during whisking, and especially when using an electric whisk. Once on surfaces, salmonellae can survive well (more than 24 h) in dried batter or egg mixes (30). There is also evidence from outbreak investigations of survival of salmonellae on cooking vessels for prolonged periods, after having been hand washed (40). Sagoo et al. (38) highlighted deficiencies in cleaning standards in food premises in the United Kingdom, including deficiencies in use of cleaning products and the importance of establishing effective cleaning schedules. Evidence on poor egg storage and handling practices in food service premises from the present survey concurs with that previously reported in the United Kingdom (10) and the United States (32). Poor practice regarding use of eggs presents an unacceptable level of risk to the consumer. Taylor (41) has also reported there is little awareness of food safety risks associated with eggs within the United Kingdom food service sector, for example, using raw eggs in uncooked dishes and serving lightly cooked dishes containing egg to vulnerable groups; good practice is not widespread; government guidance is not adhered to; and traditional methods of communicating food safety information to the food service sector is not effective. The food service sector can reduce the risk of their customers becoming infected with Salmonella by ensuring that eggs are stored at or below 8 C, avoiding bulking or pooling of eggs not intended for immediate service, avoiding contamination of ready-to-eat foods from eggs, and ensuring that salmonellae are killed through proper cooking (28, 29). A Ministry of Agriculture, Fisheries and Food Code of Practice on the handling and storage of eggs recommends that food hygiene training for staff should include attention to the correct handling of eggs and foods containing eggs, and the avoidance of cross-contamination (35). Taylor (41), however, identified the lack of specific advice on safe egg use in the Basic Food Hygiene Certificate, which is the major

J. Food Prot., Vol. 71, No. 1 SALMONELLA CONTAMINATION OF FOOD SERVICE EGGS 25 format for food hygiene training of food handlers to basic (now foundation) level in the United Kingdom. To improve public health, i.e., by trying to reduce the number of infections from eggborne Salmonella, new approaches need to be considered. Further work could be initiated to reinforce advice about pasteurized egg use for raw egg dishes, together with further advice on refrigerated storage of eggs and measures to prevent cross-contamination. Increased awareness, through improved training of all food handlers and managers, may lead to an improvement in hygienic practices during handling of eggs and preparation of egg dishes in food service premises. These findings have important implications for the food hygiene training of staff in the food service sector. 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