Caroline Willis

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.

Partial Failure of Milk Pasteurization as a Risk for the Transmission of Campylobacter From Cattle to Humans

An outbreak investigation identified a plausible transmission route that may contribute to the large and poorly characterized human disease burden of Campylobacter jejuni from cattle and demonstrated an approach to testing this hypothesis through integration of genomic analysis in surveillance.

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.

Epidemiological and Microbiological Investigation of an Outbreak of Severe Disease from Shiga Toxin–Producing Escherichia coli O157 Infection Associated with Consumption of a Slaw Garnish

Investigating outbreaks of Shiga toxin-producing Escherichia coli (STEC) in England is a priority due to the potential severity of disease. However, there are often challenges in investigating outbreaks due to the small numbers of cases, poor patient recall, and low levels of bacteria that are challenging to detect in food samples using traditional laboratory culture techniques, and frequently a source is not identified. In September 2014, we investigated an STEC O157 outbreak associated with consuming a slaw garnish, and we report our findings here. Twenty confirmed cases were identified. Outbreak cases were interviewed, and menus reviewed to identify dishes consumed outside the home. Cases shared a history of eating meals at different chain restaurants. Analysis of menu items indicated shared consumption of slaw garnishes by 85.6% cases, although just 35.7% reported consuming them during interviews. Whole-genome sequencing linked cases where interpretation of the multilocus variable number tandem repeat analysis profile was obscured and indicated that the strain originated from a domestic (i.e., United Kingdom) source. Traceback identified that carrots and cabbages grown in the United Kingdom were the likely source of infection. Samples of products were examined, but STEC was not recovered. Epidemiological investigations linked the outbreak to consumption of a slaw garnish, which was poorly recalled by cases, and likely comprised of domestically produced raw vegetables. The causative organism was not isolated from food samples, and we conclude that future investigations should include sampling of animals and wildlife in the vicinity of farms where implicated produce is grown.

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.

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.

Recurrent seasonal outbreak of an emerging serotype of Shiga toxin-producing Escherichia coli (STEC O55:H7 Stx2a) in the south west of England, July 2014 to September 2015

The first documented British outbreak of Shiga toxin-producing Escherichia coli (STEC) O55:H7 began in the county of Dorset, England, in July 2014. Since then, there have been a total of 31 cases of which 13 presented with haemolytic uraemic syndrome (HUS). The outbreak strain had Shiga toxin (Stx) subtype 2a associated with an elevated risk of HUS. This strain had not previously been isolated from humans or animals in England. The only epidemiological link was living in or having close links to two areas in Dorset. Extensive investigations included testing of animals and household pets. Control measures included extended screening, iterative interviewing and exclusion of cases and high risk contacts. Whole genome sequencing (WGS) confirmed that all the cases were infected with similar strains. A specific source could not be identified. The combination of epidemiological investigation and WGS indicated, however, that this outbreak was possibly caused by recurrent introductions from a local endemic zoonotic source, that a highly similar endemic reservoir appears to exist in the Republic of Ireland but has not been identified elsewhere, and that a subset of cases was associated with human-to-human transmission in a nursery.

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.

National outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to mixed salad leaves, United Kingdom, 2016

We investigated a large outbreak of Escherichia coli O157 in the United Kingdom (UK) with 165 cases between 31 May and 29 July 2016. No linked cases were reported in other countries. Cases were predominately female (n = 128) and adult (n = 150), 66 attended hospital and nine had features of haemorrhagic uraemic syndrome. A series of epidemiological studies (case–control, case–case, ingredients-based and venue-based studies) and supply chain investigations implicated mixed salad leaves from Supplier A as the likely outbreak vehicle. Whole genome sequencing (WGS) indicated a link with strains from the Mediterranean and informed the outbreak control team to request that Supplier A cease distributing salad leaves imported from Italy. Microbiological tests of samples of salad leaves from Supplier A were negative. We were unable to confirm the source of contamination or the contaminated constituent leaf although our evidence pointed to red batavia received from Italy as the most likely vehicle. Variations in Shiga toxin-producing E. coli surveillance and diagnosis may have prevented detection of cases outside the UK and highlights a need for greater standardisation. WGS was useful in targeting investigations, but greater coverage across Europe is needed to maximise its potential.