Heather Aird

Public Health Investigation of Two Outbreaks of Shiga Toxin-Producing Escherichia coli O157 Associated with Consumption of Watercress

ABSTRACT An increase in the number of cases of Shiga toxin-producing Escherichia coli (STEC) O157 phage type 2 (PT2) in England in September 2013 was epidemiologically linked to watercress consumption. Whole-genome sequencing (WGS) identified a phylogenetically related cluster of 22 cases (outbreak 1). The isolates comprising this cluster were not closely related to any other United Kingdom strain in the Public Health England WGS database, suggesting a possible imported source. A second outbreak of STEC O157 PT2 (outbreak 2) was identified epidemiologically following the detection of outbreak 1. Isolates associated with outbreak 2 were phylogenetically distinct from those in outbreak 1. Epidemiologically unrelated isolates on the same branch as the outbreak 2 cluster included those from human cases in England with domestically acquired infection and United Kingdom domestic cattle. Environmental sampling using PCR resulted in the isolation of STEC O157 PT2 from irrigation water at one implicated watercress farm, and WGS showed this isolate belonged to the same phylogenetic cluster as outbreak 2 isolates. Cattle were in close proximity to the watercress bed and were potentially the source of the second outbreak. Transfer of STEC from the field to the watercress bed may have occurred through wildlife entering the watercress farm or via runoff water. During this complex outbreak investigation, epidemiological studies, comprehensive testing of environmental samples, and the use of novel molecular methods proved invaluable in demonstrating that two simultaneous outbreaks of STEC O157 PT2 were both linked to the consumption of watercress but were associated with different sources of contamination.

Assessment of the Microbiological Quality of Meat Pies from Retail Sale in England 2013

Outbreaks of foodborne illness caused by Bacillus cereus and Listeria monocytogenes in England associated with meat pie consumption were detected in 2012. To obtain baseline data for pies unrelated to outbreaks, 862 samples of ready-to-eat meat pies were collected at retail or from catering facilities in England in 2013 and examined to enumerate food-poisoning bacteria and indicator organisms using Organization for Standardization (ISO) methods for Listeria spp. including L. monocytogenes (ISO 11290), Clostridium perfringens (ISO 21528), coagulase-positive staphylococci including Staphylococcus aureus (ISO 6888), Bacillus spp. including B. cereus (ISO 1737), Escherichia coli (ISO 16649), Enterobacteriaceae (ISO 21528), and aerobic colony counts (ACCs; ISO 4833). Microbiological quality was satisfactory in 94% of samples, borderline in 5%, and unsatisfactory in 1%. The proportion of pies from markets that were borderline or unsatisfactory significantly increased, and the proportion of borderline or unsatisfactory pies from supermarkets significantly decreased. Among the refrigerated (0 to 15°C) pies, microbiological quality significantly decreased in pies stored at >8°C and further significantly decreased at in pies stored at ambient temperature (>15 to 25°C). Samples collected at 25 to 40°C had the highest proportion of borderline or unsatisfactory results, but results improved in pies stored at >40°C. The most common cause for borderline or unsatisfactory results was elevated ACCs (5% of all samples). Within the individual microbiological parameters, borderline or unsatisfactory results resulted from elevated Enterobacteriaceae or Bacillus levels (10 samples for each), C. perfringens levels (2 samples), and S. aureus or E. coli levels (1 sample each). L. monocytogenes was recovered from one pie at <10 CFU/g. A literature review revealed a range of microbiological hazards responsible for food poisoning and meat pie consumption, and surveillance data from 1992 to 2012 from England indicated that C. perfringens was the most commonly reported cause of outbreaks of foodborne illness.

Two Linked Enteroinvasive Escherichia coli Outbreaks, Nottingham, UK, June 2014.

These outbreaks highlight the necessity to consider this bacterium as a potential pathogen in foodborne outbreaks.

The occurrence of Salmonella in raw and ready-to-eat bean sprouts and sprouted seeds on retail sale in England and Northern Ireland.

A total of 554 samples of bean sprouts or other sprouted seeds were collected at retail sale and submitted to nine Official Control Laboratories in England and Northern Ireland during January to March 2011. Samples (100 g) were tested for the presence of Salmonella using the EN ISO 6579:2002 method. Products labelled as ready‐to‐eat comprised 23% of the samples and 61% were labelled as raw or to‐cook: the remaining 12% had no indication if the food was intended as ready‐to‐eat or ready‐to‐cook, and 4% were not recorded. Salmonella spp. were detected from four samples of mung‐bean sprouts (0·7% of all the 554 samples) and all four isolates were confirmed as Salmonella enterica serovar Abaetetuba (11 : k : 1,5). Two of the samples where Salmonella was detected were sold as ready‐to‐eat (labelled ‘rinse and serve’ only): The remaining two were from samples labelled as ready‐to‐cook.

An epidemiological review of gastrointestinal outbreaks associated with Clostridium perfringens, North East of England, 2012-2014.

An anecdotal increase in C. perfringens outbreaks was observed in the North East of England during 2012-2014. We describe findings of investigations in order to further understanding of the epidemiology of these outbreaks and inform control measures. All culture-positive (>105 c.f.u./g) outbreaks reported to the North East Health Protection Team from 1 January 2012 to 31 December 2014 were included. Epidemiological (attack rate, symptom profile and positive associations with a suspected vehicle of infection), environmental (deficiencies in food preparation or hygiene practices and suspected vehicle of infection) and microbiological investigations are described. Forty-six outbreaks were included (83% reported from care homes). Enterotoxin (cpe) gene-bearer C. perfringens were detected by PCR in 20/46 (43%) and enterotoxin (by ELISA) and/or enterotoxigenic faecal/food isolates with indistinguishable molecular profiles in 12/46 (26%) outbreaks. Concerns about temperature control of foods were documented in 20/46 (43%) outbreaks. A suspected vehicle of infection was documented in 21/46 (46%) of outbreaks (meat-containing vehicle in 20/21). In 15/21 (71%) identification of the suspected vehicle was based on descriptive evidence alone, in 5/21 (24%) with supporting evidence from an epidemiological study and in 2/21 (10%) with supporting microbiological evidence. C. perfringens-associated illness is preventable and although identification of foodborne outbreaks is challenging, a risk mitigation approach should be taken, particularly in vulnerable populations such as care homes for the elderly.

Assessment of the Microbiological Safety of Precut Fruit from Retail and Catering Premises in the United Kingdom.

Fresh fruit has been associated with a number of foodborne outbreaks in recent years. In particular, a large outbreak of listeriosis in the United States in 2011 was associated with consumption of cantaloupe melon, and an outbreak of Salmonella Newport in the United Kingdom and Europe (also in 2011) was linked to watermelon consumption. A study of precut fruit products from catering and retail premises in the United Kingdom was, therefore, carried out to assess their microbiological safety. Between January and March 2012, samples (1,188) of ready-to-eat precut fruit were collected from retail and catering premises in the United Kingdom, and 99% were of satisfactory microbiological quality. However, four samples (0.3%) were of an unsatisfactory quality (one with 800 CFU/g Listeria monocytogenes and three with >100 CFU/g Escherichia coli), and five samples (0.4%) were of a borderline quality owing to the presence of E. coli (two samples with a level of 20 CFU/g), Staphylococcus aureus (two samples with levels of >50 CFU/g), or L. monocytogenes (one sample with a level of 80 CFU/g). L. monocytogenes or other Listeria species were detected in a further 54 samples (4.5%) at levels below the threshold considered to be borderline or unsatisfactory. A significantly larger proportion of samples from one national supermarket chain was contaminated with L. monocytogenes than other supermarkets, and two types were, in this study, unique to this supermarket. This study shows that overall, the microbiological quality of ready-to-eat precut fruit was good. However, the presence of Listeria species in 5% of samples highlights the need for good hygiene during preparation and satisfactory temperature and time control during storage of these food products.

An assessment of the microbiological safety of fresh whole‐leaf herbs from retail premises in the United Kingdom with a focus on Salmonella spp.

Fresh herbs have been associated with a number of outbreaks in recent years, in the United Kingdom and elsewhere. A study of fresh herbs was carried out to assess their microbiological safety in relation to Salmonella contamination and levels of Escherichia coli.

An assessment of the microbiological quality and safety of raw drinking milk on retail sale in England

This study aimed to review the microbiological results for raw drinking milk (RDM) samples submitted to Public Health England laboratories between 2014 and 2016 in order to produce up‐to‐date data on the microbiological safety of RDM and inform future risk assessments on its sale.

An assessment of the microbiological quality of lightly cooked food (including sous-vide) at the point of consumption in England.

This observational study aims to investigate the microbiological quality of commercially prepared lightly cooked foods with a major component of food of animal origin and collected as would be served to a consumer. A total of 356 samples were collected from catering (92%), retail (7%) or producers (1%) and all were independent of known incidents of foodborne illness. Using standard methods, all samples were tested for: the presence of Campylobacter spp. and Salmonella spp. and enumerated for levels of, Bacillus spp. including B. cereus, Clostridium perfringens, Listeria spp. including L. monocytogenes, Staphylococcus aureus, Escherichia coli, Enterobacteriacea and aerobic colony count (ACC). Results were interpreted as unsatisfactory, borderline or satisfactory according to the Health Protection Agency guidelines for assessing the microbiological safety of ready-to-eat foods placed on the market. Amongst all samples, 70% were classified as satisfactory, 18% were borderline and 12% were of unsatisfactory microbiological quality. Amongst the unsatisfactory samples, six (2%) were potentially injurious to health due to the presence of: Salmonella spp. (one duck breast); Campylobacter spp. (two duck breast and one chicken liver pâté); L. monocytogenes at 4·3 × 103 cfu (colony-forming units)/g (one duck confit with foie gras ballotin) and C. perfringens at 2·5 × 105 cfu/g (one chicken liver pâté). The remaining unsatisfactory samples were due to high levels of indicator E. coli, Enterobacteriaceae or ACC.

An assessment of the microbiological quality of liver-based pâté in England 2012-13: comparison of samples collected at retail and from catering businesses.

The purpose of this study was to investigate the microbiological quality of liver pâté. During 2012-13, a total of 870 samples, unrelated to the investigation of food-poisoning outbreaks, were collected either at retail (46%), catering (53%) or the point of manufacture (1%) and were tested using standard methods to detect Salmonella spp. or Campylobacter spp., and to enumerate for Listeria spp., including Listeria monocytogenes, Clostridium perfringens, coagulase-positive staphylococci including Staphylococcus aureus, Bacillus spp., including Bacillus cereus, Escherichia coli, Enterobacteriaceae, and aerobic colony counts (ACCs). Seventy-three percent of samples were of satisfactory microbiological quality, 18% were borderline and 9% unsatisfactory. Salmonella spp. or Campylobacter spp. was not recovered from any sample. The most common causes of unsatisfactory results were elevated ACCs (6% of the samples) and high Enterobacteriaceae counts (4% of samples). The remaining unsatisfactory results were due to elevated counts of: E. coli (three samples); B. cereus (one sample at 2·6 × 105 cfu/g); or L. monocytogenes (one sample at 2·9 × 103 cfu/g). Pâté from retail was less likely to be contaminated with L. monocytogenes than samples collected from catering and samples from supermarkets were of significantly better microbiological quality than those from catering establishments.