INTRODUCTION
Lightly cooked foods were originally described by Sir Benjamin Thompson (Count Rumford) in the late 18th century, and this cooking method was redeveloped by American and French engineers in the mid-1960s as a more widespread commercial cooking method [Reference Mossel and Struijk1]. There are now different techniques for lightly cooking foods, which include either the modification of existing processes with reduced cooking times (e.g. undercooking or flash frying), mild heating such as the using a bain-marie, or the use of a completely different cooking method such as sous-vide. The sous-vide method involves the cooking of food for extended times in hermetically (vacuum) sealed containers at ‘low’ temperatures by immersion in a water bath, and in some instances, followed by storage under refrigeration prior to a further heat regeneration before consumption [Reference Mossel and Struijk1, Reference Baldwin2]. Overall, lightly cooking methods can be used alone or in combination with other cooking methods and their use became more common in commercial cooking (especially for sous-vide) from the 1970s, particularly since there can be better consistency and moisture retention in the final product [Reference Mossel and Struijk1]. Sous-vide is also now available for use in domestic settings [3].
Lightly cooked foods encompass a wide range of cooking times and temperatures, and these can vary from minutes to several hours for sous-vide, and may involve temperatures between 40 and 60 °C [3]. After cooking and at the point of serving, products may be near sterile, or more often, either at a point where vegetative bacterial cells are destroyed but bacterial spores remain, or when both vegetative cells and bacterial spores remain. Examples of food cooked in these ways where vegetative cells are likely to survive are burgers served rare, rare duck meat (pink duck), liver parfait and liver pâtés.
There is some information on the survival of specific bacterial foodborne hazards through challenge studies using various sous-vide and other light cooking processes [3–Reference Juneja8]. However, there are limited data to predict the effectiveness to kill and prevent the growth of bacterial foodborne pathogens at the lower cooking temperatures [9] or to verify how efficient these processes are in practice including in commercial settings.
The purpose of this observational study was to investigate the microbiological quality of commercially prepared lightly cooked foods as would be served to a consumer. Because of the types of foods associated with foodborne illness as well the increased likelihood of bacterial hazards occurring, this study focused on products with major components of animal origin.
METHODS
Sample collection
A total of 356 samples of ready-to-eat lightly cooked foods (as would be served to a consumer) were collected by sampling officers from 75 Environmental Health Departments in England during April to September 2011. Samples were collected from catering, retail or producers, and included a wide range of products (mostly with animal product-based ingredients) and different cooking methods. All samples were collected independent of any known incident of foodborne illness. Samples (of at least 100 g) were collected and transported in accordance with the Food Standards Agency Food Law Practice Guidance [10]. Information on premises and sample type was also collected by the sampling officer using a standardized study questionnaire.
Microbiological examination
Samples were transported at between 0 and 8 °C to Health Protection Agency (HPA) Food Water and Environmental Microbiology Laboratories in England based at Ashford, Birmingham, Bristol, London, Preston, Porton and York. Samples were microbiologically examined within 24 h of collection using standard methods, which comprised: the presence of both Salmonella spp. (ISO 6579:2002) and Campylobacter spp. (ISO 10272-1:2006); the presence and enumeration of Listeria spp., including Listeria monocytogenes (ISO 11290-1:1996 and ISO 11290-2:1998); and enumeration of Clostridium perfringens (ISO 7937:2004), coagulase-positive staphylococci, including Staphylococcus aureus using (ISO 6888-1:1999), Bacillus spp., including Bacillus cereus (ISO 7932:2004), Escherichia coli (BS ISO 16649-2:2001), Enterobacteriaceae using (ISO 21528-2:2004) and Aerobic Colony Count (BS EN ISO 4833:2003). All presence/absence tests were performed on 25 g samples and the identification of isolates of Campylobacter spp., C. perfringens, L. monocytogenes and Salmonella spp. was performed in each of the individual laboratories as outlined in the standard methods above.
Microbiological results were interpreted according to the HPA guidelines for assessing the microbiological safety of ready-to-eat foods placed on the market [11] (Table 1) and, where relevant, using the EC Commission Regulation No. 2073 on the microbiological criteria for foodstuffs [12].
Confirmation of identity and typing of Campylobacter spp., L. monocytogenes and Salmonella spp.
Cultures were sent to the Public Health England (PHE) Gastrointestinal Bacteria Reference Unit (GBRU), for confirmation of identity and further characterization. Speciation was performed as described previously for Campylobacter spp. [Reference Best13], C. perfringens [Reference Grant14], L. monocytogenes [Reference Nogva15, Reference Vitullo16] and Salmonella spp. [Reference Bale17, Reference Grimont and Wei18]. Cultures were further characterized as follows: C. perfringens enterotoxin gene detection by PCR [Reference Grant14]; L. monocytogenes by molecular serogrouping by PCR [Reference Doumith19] and fluorescent amplified fragment length polymorphism (fAFLP) [Reference Roussel20]; and Salmonella spp. by serotyping and phage-typing [Reference Chambers21].
Statistical analysis
Descriptive and statistical analyses of the data were undertaken using Microsoft Excel. Relative proportions were compared using the Fisher's exact test. A probability value of <5% was defined as significant.
RESULTS
Amongst the total of 356 samples, 328 (92%) were from catering outlets (including restaurants, hotels or public houses), 24 (7%) were from retail establishments (e.g. delicatessens, farm-shops) and four (1%) were from producers. Sampling Officers were instructed to collect samples as they would be sold or served and 25 (9·8%: three beef; two duck; 12 lamb; four pork; two rabbit; one guiney-fowl and one quail) were collected from refrigerated storage and further reheating before serving may have been intended. A wide variety of dishes were sampled including lightly cooked poultry meats (e.g. duck breasts), liver of various species, red meats (e.g. steaks) and fish, pâtés, liver parfaits, terrines and smoked products. The major components in the products were: poultry meat, offal and eggs in 232 (65%); beef, ox or venison in 39 (11%); lamb in 34 (10%); pork in 27 (8%); rabbit in four (1%); meat of more than one mammalian species in two samples; and fish in 18 (5%; Table 2). It was not possible to collect temperature data for flash frying or bain-marie use; however, amongst the 115 samples cooked using sous-vide, temperatures of between 44 and >100 °C were recorded. Amongst those cooked at ⩽50 °C, cooking times of between 10 and 50 min were applied.
Microbiological quality in relation to animal origin type in 356 ready-to-eat lightly cooked foods
a L. monocytogenes detected in one of these samples.
b Beef (26), Veal (2) and Venison (1).
c Mixed ham and chicken (1) and mixed rabbit and ham (1).
Using the HPA Guidelines on microbiological quality (Table 1) [11], 44 (12%) of samples were of unsatisfactory microbiological quality, 63 (18%) were borderline and 249 (70%) were classified as of satisfactory microbiological quality (Table 2). Of the 44 unsatisfactory samples, six (2%) were classified as of unsatisfactory quality and potentially injurious to health, which related to the presence of Campylobacter spp. or Salmonella spp., an elevated count of either L. monocytogenes [4·3 × 103 cfu (colony-forming units)/g] or C. perfringens (2·5 × 105 cfu/g) (Table 3). The samples where either Salmonella spp. was detected or L. monocytogenes was recovered at >100 cfu/g did also not comply with microbiological criteria for meat preparations intended to be eaten cooked and ready-to-eat food, respectively, in EC Regulation No. 2073 [12].
Microbiological quality in relation to microbiological parameters of 356 lightly cooked foods
NA, not applicable; ACC, total aerobic colony count.
a Campylobacter spp. isolates from two of the three samples were submitted for further characterization and both identified as C. jejuni.
b Potentially injurious to health.
c C. perfringens did not harbour enterotoxin gene.
d Two samples L. monocytogenes detected (by enrichment only)
e L. monocytogenes serotype1/2c fAFLP type IIVc.
f Three samples Listeria spp. detected at enrichment only (two L. innocua and one L. welshimeri).
g Salmonella spp. isolates were identified as S. Typhimurium DT8 (four isolates) and S. Typhimurium DT30 (one isolate).
A category of either borderline or unsatisfactory [11] was detected in 30% of the poultry (n = 232), 27% of the mammalian (n = 106) and 44% of the fish-based products (n = 18): the product groups where the highest proportion were borderline or unsatisfactory were either chicken liver (36%) or duck/goose liver (38%). The six samples that were of an unsatisfactory quality and potentially injurious to health were all derived from poultry, however, compared with samples derived from all other animal species, this was not significantly different (Fisher's exact test; P > 0·05). Other samples of unsatisfactory microbiological quality were associated with high counts of E. coli, Enterobacteriaceae or aerobic colony count (ACC) (Table 3).
The cooking methods were described as using sous-vide only for 34 (10%), bain-marie only for 55 (15%), short time (‘flash’) frying for 60 (17%), sous-vide plus additional heating such as searing for 81 (23%), short-time frying plus additional heating such as roasting for 47 (13%), oven cooking alone for 34 (10%), poaching or smoking for 9 (2%), and was not described for the remaining 36 (10%) of samples (Table 4). For the different cooking methods, the highest proportion of samples of an unsatisfactory microbiological quality were for those prepared using sous-vide only (29%) followed by bain-marie (27%) and flash frying (15%; Table 4). When sous-vide was combined with other cooking methods there was a significant improvement in microbiological quality compared with sous-vide cooking only (Fisher's exact test, P = 0·0002; Table 4). The majority of poultry products were subjected to sous-vide and bain-marie preparations only (Table 5).
Cooking method in relation to microbiological quality
Cooking method in relation to main food component
Campylobacter spp. isolates from two of the three samples were submitted for further characterization and isolates from both duck breast samples were identified as Campylobacter jejuni (Table 6 and Table 7). Five Salmonella isolates from the sous-vide cooked duck breast were further characterized and identified as S. Typhimurium definitive phage type (DT) 8 (four isolates) and S. Typhimurium DT30 (one isolate). Two L. monocytogenes isolates from the sous-vide cooked duck confit-foie gras ballotine were both identified as L. monocytogenes serotype1/2c fAFLP type IIVc 17a. None of five C. perfringens isolates from the chicken liver pate examined harboured the enterotoxin gene (Table 6 and Table 7).
Cooking method and food type for samples of unsatisfactory/potentially injurious to health microbiological quality
ACC, aerobic colony count; B, borderline; cfu, colony-forming units; DT, definitive phage type; fAFLP, fluorescent amplified fragment length polymorphism; U, unsatisfactory.
Unsatisfactory microbiological quality results in relation to food type
* samples deemed unsatisfactory and potentially injurious to health; ACC, total aerobic colony count.
DISCUSSION
The study has investigated the microbiological quality of lightly cooked foods as they would be served to the consumer and prepared using a range of different cooking practices. It is important to understand the ability of foodborne pathogens to survive such cooking processes and how these processes are actually used. This information has implications for the risk associated with consuming such foods. Despite the increasing use of lightly cooking practices, there are no comparative data from other similar studies at this stage of the food chain. Although microbiological testing of final product will not assure food safety, it is important to verify that adequate food safety management systems are in place.
In this study, a total of 356 lightly cooked food samples were tested, and this is part of a continuing programme of PHE national co-ordinated food studies [Reference Willis22–Reference McLauchlin26]. This programme involves two to three studies per year and relies on the close working relationship with Environmental Health Departments throughout England to carry out the sampling as part of their routine monitoring. This approach allows sampling officers some flexibility to investigate premises and sample the product types that occur in their local food businesses, rather than being prescriptive about the numbers of each sample type to collect. While the sampling strategies are not precisely defined, the study described here presents the results of over 350 samples collected from across all areas of England and throughout a 6-month time period.
Using the HPA Guidelines for ready-to-eat foods [11] a relatively high proportion, of foods tested in this study were either of borderline quality (18%) or unsatisfactory (12%) microbiological quality with 2% categorized as unsatisfactory and potentially injurious to health. Three of the six unsatisfactory and potentially injurious to health samples also had unsatisfactory results for indicator bacteria. The reasons for the potentially hazardous results in these products may relate to undercooking (e.g. for the flash-fried duck breasts) but post cooking cross-contamination could also be a factor. The high levels of C. perfringens may reflect the addition of herbs and spices which, in combination with inadequate cooling as well as poor temperature control, can lead to growth of the bacterium.
During this study no human illness investigations were linked to the Salmonella, Campylobacter or L. monocytogenes isolates detected; however, the results of this survey has shown that products prepared by light cooking methods can be contaminated with pathogens, which is unacceptable. Amongst all the food types, the risk identified in this study was the highest for poultry-derived products, although too few bovine, ovine offal or fish samples were tested to make meaningful comparison with these products.
The results from this study are in contrast to the microbiological quality reported in other recent studies of ready-to-eat foods tested in England where a much lower proportion of results were interpreted as of unsatisfactory/potentially injurious microbiological quality [Reference Willis22–Reference McLauchlin26]. This may reflect the types of foods sampled, e.g. studies, sampling herbs, fruits or bean-sprouts or, if meat containing, adequately cooked ready-to-eat foods, may be less likely to result in detection of hazardous bacteria. A recent study in 2012–2013 of 870 samples of pâté on retail sale and from catering in England found only 8% of samples as unsatisfactory and of these two samples (0·2%) were deemed of a potentially injurious to health microbiological quality [one with B. cereus (2·6 × 105 cfu/g) and one with L. monocytogenes (2·9 × 103 cfu/g)]. Amongst the unsatisfactory samples there were no Salmonella spp. or Campylobacter spp. detected, and no elevated levels of C. perfringens [Reference McLauchlin26].
The main ingredients in the majority of foods examined in this study were of animal origin, and those of poorest microbiological quality contained poultry liver. It is well recognized that raw poultry livers frequently contain pathogens. Over 70% of UK retail chickens are contaminated with campylobacters and levels can exceed 1 million cells per whole fresh chicken [Reference Jørgensen27, 28]. Chicken livers are often contaminated with campylobacters on the surface but campylobacters may also be present inside the tissues: raw poultry livers have been shown to contain up to 72 000 cfu of campylobacters per liver [Reference Whyte, Hudson and Graham29]. A review of recipes for pâté manufacturing identified procedures likely to eliminate, or at least reduce, the presence of Campylobacter, i.e. washing livers with organic acids, freeze thawing and flambé in alcohol [Reference Hutchison30] and the Food Standards Agency (FSA) has provided advice including a liver pâté recipe ‘for caterers that's free from the bacteria campylobacter’ [31]. At the time of writing (2016) efforts by the poultry industry have shown some reduction in the levels of Campylobacter contamination on the surface of chickens at retail [32]. However, a study in 2015 showed a tendency for both chefs and the general public to undercook liver [Reference Jones33]. Although the highest numbers of campylobacteriosis outbreaks in England were reported in 2010 (where there was good evidence for inadequate cooking at the point of production in catering settings [Reference Little34, Reference O'Leary35]), these have continued to be reported each year up to the time of writing in 2016 (PHE unpublished data) demonstrating a continuing public health risk.
This study highlights public health risks associated with the consumption of lightly cooked foods especially when derived from poultry and demonstrates that, in 2011, some Food Business Operators do not have an adequate Food Safety Management System in place. Nevertheless, if cooking processes are properly applied (together with adequate storage and prevention of cross-contamination), evidence from elsewhere shows that the microbiological risks, at least from sous-vide processed food, can be controlled to an acceptable level [Reference Nissen36].
The UK FSA has recently commenced discussions considering ‘risky’ foods which were defined as ‘foods where risks per serving are significant’ [37]. While such foods are normally understood to include oysters consumed raw, raw drinking milk and rare burgers, undercooked poultry livers could also be classified as belonging to this category. The standing advice from the UK Advisory Committee on the Microbiological Safety of Food for cooking burgers is that they should be cooked thoroughly, i.e. reach a core temperature of 70 °C for 2 min (or equivalent) and this delivers a significant pathogen reduction [38]. However, for rare burgers it was proposed that, ‘it is not so unacceptable as to justify removing the adult consumer's right to choose to eat it, provided a validated and verified food safety management system is applied, including in each case a set of controls’. The controls should include a combination of source controls, evidence that controls for microbiological hazards have been validated and their effective application has been validated, pathway management and consumer advice. On the basis of the observations here, some of the products examined during this study would be of a similar level of risk to that described above as ‘risky’ foods, and the application of similar mitigation steps would be applicable.
ACKNOWLEDGEMENTS
This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors. The authors would like to thank the staff in Environmental Health Departments in England and staff in the PHE Food Water and Environmental Microbiology Laboratories for their contributions to this study. Thanks are also extended to staff in the PHE Gastrointestinal Bacteria Reference Unit for typing of isolates.
DECLARATION OF INTERESTS
None.
