Outbreak report: investigation into a UK wide outbreak of Shiga toxin-producing E. coli O157 September to October 2022
Published 24 April 2025
Executive summary
In late August and early September 2022, very early signals of a potential emerging outbreak of an undefined serogroup of Shiga toxin-producing E. coli (STEC) were identified by the Gastrointestinal Infections, Food Safety and One Health Division (GIFSOH) and the Gastrointestinal Bacteria Reference Unit (GBRU) at UKHSA. The observed increase in STEC activity was also observed by public health agencies in Scotland, Wales and Northern Ireland, constituting a significant nationwide surge in cases. On 7 September an enhanced national level incident response was initiated, and a multi-disciplinary cross government Incident Management Team was convened to investigate.
Whole genome sequencing (WGS) results became available in the second week of September and it was subsequently established that the substantial increase in activity was driven by the emergence of a single large outbreak caused by closely genetically related cases of STEC O157:H7 ST11 (5- SNP address 24.223.1102.2049.4926.5294) belonging to the domestic sublineage IIb. The outbreak strain possessed Shiga toxin genes stx1a, stx2c and eae+ indicating enhanced pathogenic potential (more likely to cause bloody diarrhoea and associated with an increased risk of hospitalisation but less likely to cause Haemolytic Uraemic Syndrome or HUS).
In total there were 259 confirmed cases reported in the UK, including 7 secondary cases, making this one of the largest outbreaks of STEC O157 on record in the UK. A further 25 confirmed cases were reported in Ireland, but no other country reported confirmed or possible related cases. In the UK, the first reported illness onset date was 5 August, however most cases reported illness onset between the 25 August and 3 September. Sample dates ranged from 26 August to 29 October 2022, with the majority (88%) of cases with sample dates between 29 August and 16 September. There was a higher proportion of female cases (55% of all cases) and the age groups most affected were aged 20 to 29 years (31%) and 30 to 39 years (accounting for 50% of all reported cases). 29% of cases reported hospitalisation. No cases were diagnosed with HUS and no deaths were reported to be associated with this outbreak.
The temporal distribution of confirmed outbreak cases suggested a point source or short-lived source of infection. Initial investigations indicated a signal for consumption of foods from national fast-food chains and consumption of salad products and chicken products. Descriptive epidemiological analyses and hypothesis generation questionnaires followed by analytical epidemiological studies (UK level and Wales specific) were carried out. The epidemiological studies did provide some evidence for an association between chicken consumption and illness and consumption of salad leaves and illness. Though consumption of iceberg lettuce was noted for the majority of cases, none of the studies could find convincing evidence of association with individual food products or ingredients implicating a specific vehicle of infection in this outbreak.
The FSA’s analysis of food exposure information and traceability investigations indicated limited commonalty between types of chicken products and supply chains but did identify linked supply chains of UK grown fresh produce. Subsequently a single salad grower was directly or indirectly linked to all the other identified growers or processors in the supply chain and consequently linked to the food service establishments and retailers of interest. The supply chain information highlighted that the suspected salad products were distributed to the UK and Republic of Ireland only, consistent with the international communications which had not demonstrated cases outside UK and Ireland and ruled out imported fresh produce as the vehicle for infection in this UK outbreak.
In summary, the source or cause of the outbreak could not be conclusively established through the epidemiological and food chain investigations and the outbreak was essentially over by the time putative links to the specific salad supply chains had been established. As a result of the pace of movement of fresh produce through a food chain from harvest to sale and consumption, there were no foods left from the hypothesised contaminated supplier, so there were no food items to sample to confirm the findings microbiologically. Additionally, at this point, supply had switched from domestic to imported products so no on-going risk was identified. However, the IMT concluded that the evidence gathered by the time the investigation was completed strongly suggested nationally distributed UK grown salad leaves, sourced from a single grower was the vehicle of infection in this outbreak. Cascading risks identified from analysis of weather data showing concurrent extreme weather events that could have amplified contamination at the growing and processing stage provided further supporting evidence for this conclusion, together with the timing of the outbreak in relation to salad product supply chains, the outcomes of the international communications that the suspected salad products were distributed to the UK and Republic of Ireland only and the phylogenetic analyses carried out.
The findings of the outbreak investigation were shared with the public in a peer-reviewed publication in the Eurosurveillance Journal (15) in September 2024.
Based on the outcomes and lessons identified in this outbreak investigation, recommendations for future consideration included:
Recommendation 1: UKHSA should continue to work with partner agencies (PHS, PHW, PHA, FSA, Local Authorities, APHA etc) to continue to progress full investigations into incidents to gather the best possible evidence for future preventative strategies.
Recommendation 2: Public health agencies, including UKHSA, and the Food Standards agencies in the UK should continue share information and findings with the food industry, including trade associations, and competent authorities.
Recommendation 3: Multidisciplinary research to gather the best possible evidence for refining of future preventative strategies at industry level is required.
Contextual analysis of WGS data and international communications including sharing of sequence data, as well as the timing of the outbreak in relation to salad product supply chains indicated a UK grown nationally distributed food item with a short shelf life as the cause of this outbreak. The analysis of genomic data supported the epidemiological and food chain investigation findings as well as informing hypothesis generation, risk assessment and targeting the investigation.
Recommendation 4: UKHSA along with partners such as the Animal Plant Health Agency (APHA) should perform pathogen characterisation and phylogenetic analyses to achieve best possible understanding of the STEC O157 population structure in the UK, likely sources of contamination and risk analysis in future.
Due to the nature and potential severity of STEC infection, especially within vulnerable groups and risks of progression to HUS, early detection and investigation of potential outbreak events is important for safeguarding public health. The close integration of the epidemiology, bioinformatics and reference microbiology laboratory teams, utilisation of multiple data sources for routine surveillance purposes and close engagement between all UK public health agencies in sharing of information resulted in early identification of an emerging outbreak and facilitated the rapid escalation of the outbreak response. However, there is known under-ascertainment of HUS cases which can result in underestimation of the severity of outcomes associated with a specific STEC strain or outbreak.
Recommendation 5: UKHSA should review national STEC surveillance systems and data linkage opportunities and implement enhancements where gaps and/or opportunities are identified to enhance further the detection and risk assessment of emerging outbreak clusters.
The novel analysis done on weather data supported the evidence generation during this outbreak investigation, highlighting the importance of work like this in understanding the current and future impacts of extreme weather events resulting from climate change. Therefore, the utility of this type of analysis, where warranted, as well as the incorporation of other relevant data analyses to generate supporting evidence on a routine basis during national level outbreaks of infectious gastrointestinal disease is being explored.
Recommendation 6: UKHSA should work with partners to consider how to optimise and study the potential impact of weather events, the efficacy of risk assessments in place to ensure safe food, as well as other influencing and risk cascading factors on foodborne pathogen transmission, contamination and amplification in food production environments.
Background
Shiga toxin-producing Escherichia coli (STEC) are a group of bacteria associated with human disease and are defined by the presence in the organisms of one or both phage-encoded Shiga toxin genes, stx1 and stx2. In the UK, STEC O157 is the most commonly reported serogroup (1).
STEC infections are of significant public health concern due to the potential severity of disease. Symptoms can range from mild diarrhoea to severe bloody diarrhoea and include abdominal cramps and vomiting. STEC infection usually results in relatively high hospitalisation rates of up to 50% depending on the serogroup – with STEC O157 usually resulting in on average 34% hospitalisation rate (2). In 5-15% of cases, infection can lead to the development of haemolytic uraemic syndrome (HUS), a severe multisystem condition that predominantly affects the kidneys (3). The clinical severity of STEC infections therefore potentially lead to consequent pressures on frontline health services, especially for paediatric and renal units.
STEC are zoonotic pathogens and ruminants are considered the main reservoir of infection. STEC has a very low infectious dose and transmission to humans occurs through consumption of contaminated food or water, direct or indirect contact with infected animals or their environment and through person to person spread. Most STEC infections are sporadic and are not part of a recognized outbreak(1)1, but outbreaks are regularly reported in the UK. Foodborne outbreaks of STEC O157:H7 in the UK are often attributed to contaminated meat and dairy products, but many recent outbreaks have been linked to ready-to-eat products, especially salad vegetables.
Faecal specimens from community and hospitalised cases with symptoms of infectious gastrointestinal disease are tested at local hospital microbiology laboratories to identify causative gastrointestinal pathogens and the results of this testing are reported to national surveillance systems as per the requirements of national legislation(4). HUS is a notifiable clinical diagnosis under the same legislation. Enhanced monitoring of STEC infections in the UK is undertaken by UK Public Health Agencies. All STEC O157 cases are requested to complete a routine enhanced surveillance questionnaire (ESQ) which captures clinical symptoms and environmental and food exposures(5). These ESQs are submitted for entry into the National Enhanced STEC Surveillance System (NESSS)(6) in England and similar in the other UK countries. In addition, isolates of STEC identified at local diagnostic laboratories are referred to the National Reference Laboratories for confirmatory testing. Whole genome sequencing (WGS) is employed on all STEC isolates referred to the Reference Laboratories, providing highly discriminatory typing for public health surveillance and facilitating outbreak detection and investigation.
Incident identification and coordination
In late August and early September 2022, the UKHSA National Reference Laboratory, the Gastrointestinal Bacteria Reference Unit (GBRU) noted a substantial increase in the submission of Containment Level three (CL3) faeces samples and isolates that were presumptive for STEC. A substantial increase in the number of ESQs submitted for collation in NESSS and reports by some UKHSA Health Protection Teams and from public health agencies in Scotland. Wales and Northern Ireland of an observed increase in STEC activity indicated a recent significant nationwide surge in cases. National exceedance reporting in England using data from the UKHSA Second Generation Surveillance System (SGSS) demonstrated a statistically significant increase in cases of STEC O157 in week 35 of 2022, reported on the 5 September. Investigations were initiated in the first week of September 2022
A higher-than-expected proportion of the confirmed STEC O157 isolates reported were phage type (PT)14 and possessed Shiga toxin genes stx1a, stx2c and eae+. Early investigations focussed on cases with disease caused by isolates with this specific confirmed phenotypic and gene virulence profile. Once WGS results became available on 9 September, identifying 2 cases belonging to one specific 5- single nucleotide polymorphism (5-SNP) cluster, with a further 19 cases belonging to the same 5-SNP cluster reported by 11 September, the investigation focussed on this specific genomic variant of STEC O157.
On 7 September 2022 an enhanced incident response was initiated, and the first Incident Management Team (IMT) meeting was held on 8 September. A Strategic Response Group (SRG) was convened to oversee the strategic aspects of incident management. The incident was managed as set out by UKHSA’s generic emergency preparedness, resilience and response (EPRR) arrangements detailed in its Incident Response Plan (IRP) and the investigation was carried out according to national level guidelines on communicable disease outbreak management. The overall aim of the investigation was to identify the vehicle(s) and source of contamination and to gather evidence to inform implementation of risk management measures to protect the public and, additionally, prevent future similar incidents.
The IMT included representatives from all relevant government departments/ agencies responsible for the protection of public health and food safety (Appendix 3) and met at regular agreed intervals to collate and review the epidemiological, microbiological and food chain evidence obtained during the investigation.
Epidemiological investigations were led by UKHSA, Public Health Scotland (PHS), Public Health Wales (PHW), Public Health Agency Northern Ireland (PHA NI) and the Republic of Ireland Health Protection Surveillance Centre (HPSC). Microbiology and phylogeny investigations were led by GBRU in collaboration with the Scottish Escherichia coli Reference Laboratory (SERL) and the Public Health Laboratory VTEC National Reference Laboratory in the Republic of Ireland. Food chain investigations were led by the food safety authorities, the Food Standards Agency (FSA) and Food Standards Scotland (FSS) in collaboration with Food Standards Agency Ireland (FSAI), working with relevant local authorities and industry partners.
Four operational cells were convened:
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an Epidemiology Cell (EpiCell) to progress the epidemiological investigations, led by UKHSA Field Services (FS)
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a Food Chain Cell to progress food tracing investigations led by the FSA
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a Regional Operational Cell to support the IMT and EpiCell with operational aspects of the investigation and to assess other STEC clusters of concern, led by the UKHSA Regional Lead for gastrointestinal infections
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a Communications Cell to coordinate the communications strategy, led by the UKHSA National Communications Team
All incident related documents and communications were securely managed and stored according to GDPR requirements. A dedicated email account was used to manage all incident related communications.
The incident was initially managed as a national enhanced response, then de-escalated to a standard response on 27 September and finally to routine response on 8 December 2022. The public health agencies incident response was closed on 30 December however further investigations led by the food safety authorities, including root cause analysis and other intelligence gathering initiatives to inform both the investigative outcomes for this specific outbreak and future management of such outbreaks, extended into 2023.
A briefing note was published on 14 September 2022 to alert UKHSA HPTs, clinical laboratories and Local Authority (LA) Environmental Health Teams to the outbreak. A notification via the European Centre for Disease Control (ECDC) EpiPulse platform was posted by the UK on 11 September to alert other countries to the outbreak in the UK and to determine if there were any potential cases associated with an outbreak outside the UK, indicating a cross-border threat.
Investigation methods
Epidemiological
The objectives of the epidemiological investigation were to identify and describe cases associated with the outbreak and to identify the likely vehicle of infection. Key strands of the epidemiological investigation included agreeing the outbreak case definition, outbreak case ascertainment and collection and analysis of epidemiological data for hypothesis generation and testing to identify the vehicle(s) of infection.
Microbiological typing results were used for case finding with classification according to the agreed case definitions. All cases in England, Wales and Northern Ireland were identified as meeting the confirmed case definition using the validated results reported in the UKHSA Gastrodata Warehouse (GDW2) database. Cases in Scotland were identified by SERL and cases in the Republic of Ireland were identified by the Public Health Laboratory (VTEC national reference laboratory, VTEC NRL).
Descriptive epidemiological analyses were performed in MS Excel and R version 4.2.1 using the case line list data. These analyses included a summary of available food exposure information, epidemiological curves, and age, sex and geographical distribution of the cases, travel reported and the clinical severity of illness.
Hypothesis generation interviews were undertaken between 13 to 16 September in the UK with 19 cases (or the parents or guardians in the case of children) with illness onsets between 10 August 2022 and 29 August 2022. A targeted questionnaire proforma was used in telephone interviews. The trawling questionnaire covered case demographics, details of illness onset and duration, hospitalisation, clinical management of the illness, detailed description of any eating out and extensive questions around consumption of different foods including meat and meat products, dairy products, eggs and egg products, salad, fruit and vegetables during the incubation period which was defined as 7 days prior to onset of illness. Non-food exposures (including national and international travel, unwell contacts, animal contact, pet foods and wildlife exposures), as well as food purchase locations were covered across this period as well.
The most commonly reported food exposures derived from case interviews were collated and submitted to the FSA for coordination of the food chain investigations and food chain analysis across competent authorities and industry partners. Data derived from the National Diet and Nutrition Survey (NDNS) (7) on typical consumption of food items most commonly reported by cases at the population level was also analysed for comparative purposes.
A frequency-matched case-control study was undertaken across all 4 UK nations. Cases for the study were selected using stratified random sampling and interviewed by telephone between 28 September and 14 October using a bespoke questionnaire focusing on frequently reported exposures derived from trawling interviews. These included eating out, chicken, beef and salad product exposures. Controls were recruited via a market research panel and were frequency matched to cases on country of residence, age and sex and who did not have a history of diarrhoea and/or vomiting in the 7 days prior to completion of the control questionnaire. Control questionnaires were completed online.
Univariable logistic regression analysis of each exposure variable was undertaken and odds ratios (OR), p-values and 95% confidence intervals (CI) were reported. Exposures with raised odds of illness and likelihood ratio test (LRT) p-value less than 0.2 from the univariable analysis were considered for inclusion in multivariable analysis (MVA) using Firth logistic regression and a forward stepwise approach. Two MVA models were constructed, one containing the largest number of observations and a second smaller model with more granular data on food item type. MVA was also undertaken in parallel by the UKHSA Statistics Unit for quality assurance purposes. Data were analysed using R version 4.2.1, RStudio 2022.07.0+548 and STATA version 17.0.
An additional case-case (control) study was undertaken by PHW with cases resident in Wales, which used the same questionnaire as the multi-nation analytical study. Controls were selected from cases of non-O157 STEC as reported in Tarian (Wales’ Case Management tool), between 1 August 2022 and 27 September 2022 and were frequency matched for age band (10/20 year). Univariable analysis was undertaken, followed by a series of stratified analyses using Firth logistic regression. Multivariable analysis was not undertaken because of the small sample size.
Microbiology and phylogeny investigations
On receipt at the reference laboratory, isolates were tested by PCR to determine the presence of the genes encoding Shiga toxin (stx1 and/or stx2), phage typed and sequenced on the Illumina HiSeq 2500 and Nextseq 1000 sequencing platforms. Genome-derived serotyping detection was performed using the GeneFinder tool. Illumina reads were mapped to the STEC O157:H7 reference genome Sakai (Genbank accession: BA000007). High-quality variants (SNPs) were identified using GATK v2.6.5 in unified genotyper mode. Core genome positions that have a high-quality SNP (>90% consensus, minimum depth 10×, GQ >=30) in at least one isolate were extracted from SnapperDB v0.2.8 and IQtree v2.0.4 was used to derive the maximum likelihood phylogeny of the isolates after first removing regions of the genome predicted to have undergone horizontal exchange using Gubbins v3.2.0 (8).
Hierarchical single linkage clustering was performed on the pairwise SNP difference between all strains within the same clonal complex at various distance thresholds (250, 100, 50, 25, 10, 5, 0) (9). For isolates from Scotland, variant calling was performed locally and then integrated with GBRU sequences to generate equivalent SNP addresses. Antibiotic resistance determinants were analysed using the UKHSA gene finder database (10).
Sequencing data from NCBI(11) and Enterobase (12)were downloaded and analysed to identify closely related international isolates. The Enterobase core-genome Multilocus Sequence Typing (cgMLST) hierarchical cluster designation for the outbreak isolates (HC5-115711) and 2 accession numbers (SRR21488028 and SRR10228115) were communicated internationally via the EpiPulse platform for comparison.
Food chain investigations
The FSA analysed the food exposure information derived from case interviews to inform supply chain analysis and investigation strategies into the main exposures of interest. The FSA also used case loyalty card data provided during the case interviews to request data on food purchase information from retailers for the relevant period. The FSA commissioned a series of information requests from Competent Authorities, Primary Authorities, INFOSAN ECPs, relevant Food Industry Trade Associations (TA) and key food business operators, (FBOs). The results were analysed and communicated by the FSA to the IMT and the Food Chain Cell.
The FSA liaised with key Industry TAs including the Fresh Produce Consortium, Chilled Food Association and the British Retail Consortium to establish possible emerging industry trends, processes, and procedures at each stage of the supply chain and the nature and detail of the risk assessments carried out pre- and post- harvest to ensure compliance and production of safe food. To further understand operational procedures and practises at the fresh produce grower level, processing and packing stages, FSA representatives also undertook 2 site visits: to a fresh produce grower and a fresh produce grower and processor.
The FSA provided microbiological food safety expertise, supply chain expertise to address any essential missing information, or that required further clarification from the business, which informed FSA risk management advice on appropriate and proportionate food safety actions required in response to the outbreak.
The FSA notified food safety officials in 2 European Union countries of the UK outbreak in September 2022 via the INFOSAN ECPs, with the aim of gathering relevant international food chain information based on assessment of international supply chain analysis and to establish food safety controls to ensure supply of safe food import to the UK. To compliment the understanding, a meeting was held via Teams on 28 September 2022 with an EI INFOSAN ECP.
Weather data analysis
The UKHSA Environmental Epidemiology team within the UKHSA Chemicals and Environmental Effects Department analysed land surface weather observation data from 2 sources: the Met Office Integrated Data Archive System (MIDAS) via the Environmental Public Health Surveillance System (EPHSS) and the Environment Agency (EA) rainfall data available via the Hydrology Data Explorer (13). Following the identification of produce supply chains of interest with potential links to the outbreak obtained during the FSA’s food chain investigations, rainfall data recorded by nine meteorological stations in the region of interest in the UK were analysed in further detail.
Epidemiology investigation results
In the early stage of the investigation into the exceedance in reports of STEC, the increase in reported STEC cases across the UK was determined to be initially primarily due to an increase in non-O157/unknown serogroup STEC, followed by a marked increase in STEC O157 cases. Initial bi-lateral enquiries with international partner public health agencies did not indicate similar signals in other European countries.
Analysis of the available enhanced epidemiological surveillance data for all reported STEC cases resident in England reported in the previous 3 months did not identify any specific epidemiological links between the cases. The case age/sex demographic was consistent with previous years (mean age: 35.9 years, 44% male) and there were no reported fatal cases where STEC infection was reported as causal or contributory to death. Analysis of available WGS data for non-O157 and O157 STEC showed that the majority of isolates were sporadic or belonged to a number of small clusters comprising 2 to 3 cases, with the exception of a single national outbreak of a STEC O157 consisting of nine cases that has been under investigation in England between mid-August 2022 and November 2022 with beef products being the suspected vehicle of infection.
Between 5 September and 7 September, the number of confirmed STEC O157 cases was 73, compared to an average of 16 cases of STEC O157 reported each week in the previous 4 weeks. Following identification of cases sharing the same 5-SNP address 24.223.1102.2049.4926.5294. (designated t5:5294) in the second week of September, the outbreak case definition was developed as follows:
Confirmed case: a case of STEC O157:H7 CC11 reported since 01 January 2022, resident in the UK, with a UKHSA 5-SNP address: 24.223.1102.2049.4926.5294. (t5:5294) or falling within t5.5294 after accounting for mobile genetic elements
Probable case: a case of STEC O157:H7 reported since 01 January 2022, resident in the UK and belonging to the same cgMLST HC5_115711 (Enterobase scheme) or clustering within 5 core genome allelic differences (AD) from the representative outbreak strain, accessible through the SRA code SRR21504806 using a national cgMLST pipeline.
Possible case: a case of STEC O157:H7 (stx1 and stx2) reported since 1 August 2022, awaiting SNP typing, and resident in the UK.
International case: defined according to the above national case definitions but resident outside the UK.
Co-primary cases were defined as cases with a disease onset within 4 days of another individual resident in the same household. Secondary cases were defined as cases with a date of onset more than 4 days after close contact with a primary case or where transmission was believed to be through exposure to a primary case.
Descriptive epidemiology
There were 259 confirmed cases of the outbreak strain STEC O157:H7, stx1a+, stx2c+, eae+ t5:5294 identified with sample dates ranging from 26 August to 29 October 2022, including seven secondary cases. Additionally, seven cases with this specific genetic strain of STEC O157 were previously reported in 2019 (3 cases), 2020 (2 cases) and 2021 (2 cases) (not included in the outbreak investigation or in the figures below).
The temporal distribution of the 2022 outbreak cases by sample date is presented in Figure 1 and by disease onset date in Figure 2. The major peak in case numbers, based on case sample date, was observed between 29 August and 2 September. A second smaller peak of reported cases was identified with sample dates between 5 and 6 September. 88% of all cases had sample dates between 29 August and 16 September. The first reported illness onset date was 5 August, however most cases reported illness onset between the 25 August and 3 September.
There was a higher proportion of female cases (55% of all cases) (Figure 3). The age groups most affected were aged 20 to 29 years (31%) and 30 to 39 years (19%) (Figure 3). Cases were dispersed throughout the UK, in all UKHSA regions in England and across all 4 countries of the UK (Table 1). Cases were also nationally distributed in the Republic of Ireland (data not shown).
Details on clinical symptoms and hospitalisation were available for 255 cases from enhanced surveillance databases in England, Wales, NI and Scotland. The most commonly reported symptoms were diarrhoea (n=234, 92%) and abdominal pain (n=222, 87%), followed by blood in stools (n=166, 65%), nausea (n=134, 53%), vomiting (n=82, 32%) and fever (n=76, 30%). In total 77 confirmed cases (30%) reported attending accident and emergency for their symptoms and 75 (29%) reported hospitalisation. No cases were diagnosed with HUS and no deaths were reported associated with this outbreak.
The median time between date of reported illness onset and date a sample was taken for clinical diagnosis was 4 days (range 0 – 25). The last 3 reported cases were siblings of a 6-child household where 2 other family members had reportedly been ill with symptoms consistent with STEC infection prior to the 3 children, therefore, it is considered likely these final 3 cases were secondary cases (Figure 2).
Initial analysis of exposure information derived from the hypothesis generation interviews indicated that the most frequently reported exposures were having eaten out (19 cases; 100%), eating chicken (18; 95%), any salad leaves or prepacked salad exposure (18; 95%) and beef (12; 63%). (Appendix 2). Data derived from the National Diet and Nutrition Survey (NDNS) indicated an estimated typical consumption of these food types in the population over a 4-day period as chicken (59% of the general population), salad leaves (65%) and beef (47%). Comparative data for eating out is not available in the NDNS survey data, but 100% of cases interviewed for this outbreak investigation reporting eating out was considered notable.
Travel information, derived from case interview data or laboratory sample submission forms, was available for 255 cases. Of these, 12 cases (5%) reported travel abroad to Egypt (1), France (1), Netherlands (1), Norway (1), Republic of Ireland (3), Spain (4) and Turkey (1) but not all reported travel was verified to be within the seven days prior to onset of symptoms nor did all cases reporting travel spend their entire incubation period in the destination country so it could not be verified if any confirmed cases had acquired their infection abroad.
Figure 1. Temporal distribution of confirmed STEC O157 t5.5294 cases in the UK based on specimen date [note 1] (n=247) or specimen receipt date (n=12) and country [note 1]
Note 1: The specimen date was not provided for twelve cases, the date of specimen receipt at the reference laboratory has been used instead.
Figure 2. Temporal distribution of confirmed STEC O157 t5.5294 cases in the UK based on onset date and epidemiology definition (n=231 [note 1])
Note 1: Information on case onset date or epidemiology definition not available for 28 cases
Figure 3. Age/sex distribution of confirmed STEC O157 t5.5294 cases in the UK (n=259 [note 1])
Note 1: 7 cases were considered to be secondary cases: median age 6 years, age range 1 to 51 years.
Table 1. Distribution of cases by UKHSA region or devolved administration of residence (n=259)
Region/country | Number of cases |
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East Midlands | 12 |
East of England | 13 |
London | 4 |
North East | 15 |
North West | 22 |
South East | 38 |
South West | 44 |
West Midlands | 17 |
Yorkshire and Humber | 30 |
England | 195 |
Northern Ireland | 18 |
Scotland | 33 |
Wales | 13 |
Total | 259 |
Analytical epidemiology: case-control study
For the frequency-matched case-control study across the 4 UK nations, a sample size calculation was performed with a ratio of 4 controls per case and no more than 30% of controls exposed, yielding a sample size of 38 cases and 152 unmatched controls, which would provide at least 80% power to detect the difference if 50% of cases were exposed and no more than 30% of controls were exposed. To allow for attrition and missing data, 190 controls (5 controls per case) were planned to be recruited to ensure power was maintained in the event of poor-quality data in the completed questionnaires. Overall, the study recruited 206 controls.
Case exposure data collected for the study revealed that 98% of cases ate chicken, with the most frequent individual chicken item being chicken pieces, which was eaten by 33% of cases. Salad leaves (including lettuce) were eaten by 83% of cases, with iceberg lettuce being consumed by 67% (22/33) of cases that recalled which type of lettuce they consumed. 65% of cases that ate chicken away from home also consumed lettuce away from home. 71% of cases reported eating beef, with beef burger (n=12; 29%) the most frequently reported beef item.
The univariable analysis showed a positive association between exposure to chicken and illness, with cases having an increased odds of exposure to eating chicken prepared away from the home. Consumption of any salad leaves, lettuce, and iceberg lettuce were all positively associated with illness; however, for any lettuce and iceberg, an increased odds was only seen in those that ate these items prepared away from the home. Beef consumption was associated with illness, however only in those who ate this item prepared at home.
Multivariable analysis (model 1) analysed variables to composite level variables where data was more complete than for individual ingredient variables. Multivariable analysis (model 1) including all observations (n=247; 41 cases and 206 controls) indicated an association between consumption of chicken away from the home at least some of the time and illness (OR=12.7; 95% CI: 2.24-72.2).
Multivariable analysis (model 2) included both composite and individual ingredient variables, allowing exploration of possible associations with specific products or ingredients. This multivariable analysis used fewer observations as some cases and controls did not report specific types of food items, for example lettuce (model 2: n=214; 30 cases and 184 controls), and explored individual food items which indicated an association between consumption of chicken pieces if prepared away from home, or both at home and away, and illness (OR=5.1; 95% CI: 1.65-16.1). There was weak evidence that eating chicken goujons (OR=5.34; 95% CI: 0.91-30.8) was associated with illness. There was also evidence that consumption of iceberg lettuce, prepared in any setting (home/away/both), was also associated with illness (OR=3.38; 95% CI: 1.35-9.23) in model 2. Output tables are included in Appendix 2
The case-case (control) study undertaken by Public Health Wales concurrently, indicated that the most significant association in this analysis was chicken prepared away from home (OR=15.00; 95% CI: 1.35-719), sandwiches prepared away from home (OR=16.33; 95% CI: 1.41-787) and any salad leave prepared away from home (OR=8.40, 95% CI: 0.79-409). It was not feasible to conduct a multivariable analysis due to small sample size, however stratified analyses were conducted using Firth logistic regression. When chicken and salad leaves prepared away from home are stratified, the odds ratios drop substantially and neither remain significant at p<0.05. However, the drop is larger for salad leaves (OR=8.40 v OR=1.78).
Microbiology and phylogeny investigation results
Phage typing results indicated the strain was PT14. The outbreak strain possessed Shiga toxin profile stx1a and stx2c. Further analysis indicated that ancestral strains harboured stx2c only, and that the outbreak strain had recently acquired stx1a. Antibiotic resistance determinants were not detected, and the outbreak strain was inferred to be fully susceptible to the 10 classes of antibiotic in the UKHSA gene finder database.
SNP-typing of WGS data identified the 2022 outbreak strain as STEC O157:H7 ST11 5-SNP address 24.223.1102.2049.4926.5294. Phylogenetic analyses revealed the outbreak cluster had a minimum SNP distance of 0 and a maximum SNP distance of 11 with the average SNP distance less than 1 SNP. A phylogenetic tree is included in Appendix 1
The outbreak strain belonged to sublineage IIb, a domestic type. Strains of STEC O157 belonging to sublineage IIb are common in the UKHSA archive, although the outbreak strain belonged to clade that was relatively rare.
The Enterobase core-genome Multilocus Sequence Typing (cgMLST) hierarchical cluster designation for the outbreak isolates was HC5-115711. FASTQ reads from all sequences in this study can be found at the UKHSA Pathogens BioProject at the National Center for Biotechnology Information (Accession PRJNA315192).
Food chain and environmental investigation results
Food chain tracing investigations
The FSA analysed the case food exposure information provided by the IMT and salad products indicating tomatoes, cucumbers, and salad leaves consumed in the home and at catering establishments were commonly consumed amongst confirmed cases, and became the focus of the food chain investigation. Chicken products were also considered as possible vehicles of infection, with food chain investigations also undertaken, but limited commonalty between types of chicken products, purchase location, consumption settings as well as consideration of the introduction of a kill step during cooking indicated these products were a lesser priority for follow up tracing. Therefore, less enhanced supply chain analysis was undertaken.
Salad leaves such as lettuce, spinach, baby leaf spinach, cos romaine and other leaf types were linked to the majority of the cases interviewed. There was no strong link to one specific type of salad leaf. The salad leaves highlighted in the food exposure information were a mix of processed (sliced, chopped and bagged) as well as unprocessed, unwashed whole products. Analysis of data from 4 available loyalty cards indicated several lettuce leaf types including Iceberg, Cos Romaine, Spinach, Baby leaf spinach and Mixed Salad Leaf bags. Iceberg was the most commonly reported salad leaf (10 retailers, 7 processors, 25 suppliers, 3 food services, 4 manufacturers and 14 wholesalers).
Twenty-five primary producers (farms), were linked to four national growers supplying product into 3 national chain food service establishments and 10 retail chain supermarkets were determined to be linked to 82 confirmed cases, out of the total 96 cases for which detailed food exposure information was available. Multiple cases were linked to more than one supply chain, but no cases were found to be linked to retail outlets only. Of the supply chains linked to retail chains, there were no common links amongst salad items indicating food chain investigation of the retail supply chain was necessary. The further traceability investigations identified four UK suppliers linked to the associated supply chains of UK grown fresh produce. The supply chain information highlighted that the suspected UK grown salad products were distributed to the UK and Republic of Ireland only.
Subsequently, food chain tracing information obtained from the identified food chain service establishments and retailers narrowed the traceability investigation to 2 main salad processors, with strong food chain links to one particular salad processor - processor A. On the basis of this information, the investigation was predominantly focussed on four growers: grower 1, grower 2, grower 3 and grower 4 that all supplied processor A either directly, or indirectly. The salad leaf supply chain flow is complex and dependent on the leaf, stage of the UK seasons and factors such as extreme weather that affect supply and demand.
While there were some, apparent, unsatisfactory findings in the data provided by 2 of the growers, particularly grower 1, including positive E. coli results in irrigation water, and the product being exposed to standing water following flooding, these were later found to not be a concern as appropriate steps had been taken during the manufacture process to mitigate potential risks. These measures included additional de-leafing to remove contamination and preventing part of the crops entering the food chain.
Weather data analysis
Analysis of rainfall and temperature data for nine weather stations in the region where the four identified growers were located indicated that 2 of these weather stations had high hourly rainfall amounts (in mm) on 16 and 17 August 2022 (Figure 4). Typical annual rainfall amounts in this area are around 600mm, however the total precipitation noted at one particular station (weather station 1) totalled 115.4mm in just 3 hours between 02:00 and 05:00 on 17 August 2022. This is equivalent to around 2 month’s rainfall. This was not observed at other sites in the region and was confirmed to be a very localised event.
This high rainfall event was preceded by several weeks of very hot, dry weather conditions. It was established that temperatures in the salad leaf grower region of interest reached over 40°C in July 2022, exceeding the previous UK record by 1.6°C, and the hot period in July saw the Met Office issue its first ever red warning for extreme heat(14). Figure 5 shows the mean daily maximum temperature anomaly map (a) for August 2022 illustrating mean daily maximum temperature expressed as the temperature deviation from the 1991 – 2020 averages and rainfall anomaly map (b) for August 2022 illustrating rainfall amounts expressed as a percentage of 1991 – 2020 averages(15).
Observation of the land surrounding weather station 1 using Google Maps(1) revealed a flat area of agricultural land which may have resulted in the spread of flood waters over the surrounding area and standing water accumulation. The main salad grower (grower 1) implicated in the FSA food chain investigations was geographically closely located to weather station 1.
Figure 4. Daily precipitation at Weather Station 1 and Weather Station 2, July 2022 - August 2022.
Figure 5a. Mean daily maximum temperature anomaly map for August 2022
Figure 5b. Mean daily maximum rainfall anomaly map for August 2022
The occurrence of unusual weather patterns that had coincided with the crop harvest period, included initial prolonged periods of heat, posing additional dust hazards, followed by high rainfall, causing soil wash of crops. This unusual weather pattern, the harvest of the salad crop and the contamination event all overlapped with the estimated period of harvest to shelf cycle and the estimated exposure period based on case illness onset dates. This informed the FSA’s considerations on the evidence for the vehicle of infection causing the outbreak, the risk assessment, risk management approach and root cause analysis. Information on geographical location of the farm, crop rotation on the land parcels of interest and water supply, pre- and post-harvest protocols including routine microbiological sampling programmes and weather events informed industry level routine pre- and post-harvest risk assessments. From these risk assessments the following information was confirmed:
- all the food businesses operators reported being impacted by the extreme weather during the period of interest (5 August to 5 September 2022)
- high temperatures, averaging at 33 degrees Celsius was the most common incident reported, while high rainfall was reported by Grower 1 (Grower 1 reported approximately 150mm in one night, equivalent to a month’s rainfall)
- each business conducted a risk assessment and corrective measures were implemented on a case-by-case basis at each grower and processor, including preventing parts of the crop from entering the food chain as a result of contamination
International investigation results
Twelve responses were received to the EpiPulse Notification (2022-FWD-00068) which indicated that only one responding country, the Republic of Ireland, had cases reported with isolates matching the UK representative outbreak sequence and with a clinical and epidemiological profile consistent with the cluster cases in the UK. By the end of September, 25 cases had been reported in Ireland.
Ten other European Union/European Economic Area (EU/EEA) countries reported no genetically matching cases and one country in the EU reported that although an increase in STEC reporting had been observed in 2022 compared to previous years, only 3 cases were STEC O157 stx1a+, stx2c+ but whole genome sequencing results were not available.
Information received by the FSA following communications via INFOSAN with food safety officials in 2 EU countries enabled the ruling out of imported fresh produce as the vehicle for infection in this UK outbreak. This information confirmed the FSA’s food chain tracing investigation findings that the suspected salad products were distributed to the UK and Republic of Ireland only
Discussion
In this incident very early signals of a potential emerging outbreak were identified in the UK through monitoring of Reference Laboratory referrals of presumptive STEC O157 isolates, ESQ submission numbers to STEC national enhanced surveillance systems and local intelligence communicated by regional Health Protection Teams. Once the WGS results were available, it was confirmed that the substantial increase in STEC O157 reports was driven by a single, large outbreak.
Use of WGS enables the genetic profile (‘fingerprint’) of the STEC bacteria to be analysed down to the single nucleotide (DNA base) resolution. Genetically related isolates of STEC can be easily identified and the similarity in the DNA sequences quantified. Every DNA sequence is allocated a ‘SNP address’(17), which allows closely related isolates to be easily identified. In this instance, all outbreak cases shared the same 5-SNP address 24.223.1102.2049.4926.5294, indicating all the sequences were related to each other through single linkage clustering at 5 or less SNPs. This provides strong evidence that outbreak cases are linked to a common source of contamination.
Virulence gene (shiga toxin) determination for risk assessment of likely clinical impact of the outbreak strain is also possible using genomic data. Further analysis of the outbreak strain indicated that the progenitor strains had stx2c only, and that the outbreak strain had recently acquired stx1a. The acquisition of stx1a is likely to have enhanced the pathogenic potential - STEC with stx1a are significantly more likely to cause bloody diarrhoea and are associated with an increased risk of hospitalisation but are unlikely to cause HUS. The risk of hospitalisation and severe clinical presentations is highest in young children under the age of 5 and in the elderly(18). In this outbreak, predominantly younger adults between the ages of 20 and 39 were affected, whereas typically cases of STEC are generally seen most commonly in the under 10-year-old age group (on average 23% of all cases of STEC reported in England). This may have influenced the overall lower than expected reported hospitalisation rate (29%), with no HUS cases or fatalities reported to be associated with this outbreak.
Overall, there were 259 confirmed outbreak cases based on WGS characterisation, with reported illness onset dates between 5 August and 12 October 2022. The first primary case onset date was 5 August, and the last primary case had a reported onset date of 20 September. The temporal distribution of confirmed outbreak cases suggested a point source or short-lived source of infection. Initial descriptive epidemiological investigations and analysis of the information gathered in the hypothesis generation questionnaires indicated a signal for consumption of foods from national fast-food chains and consumption of salad products and chicken products.
The analytical epidemiological studies (UK level and Wales only) did provide some evidence for an association between chicken consumption and illness and consumption of salad leaves and illness. However, none of the studies could find convincing evidence of association with individual food products or ingredients implicating the vehicle of infection in this outbreak. Consumption of iceberg lettuce on its own could potentially explain the largest number of cases.
The epidemiological investigations were strengthened by having different analytical studies undertaken although each study had both strengths and limitations. The UK level case-control study had a large sample size (within the context of outbreak-related case-control studies) and the recruitment criteria was met, minimising biases associated with smaller sample sizes. Limitations included that recall may have been different for cases and controls. Given the time period between illness and being interviewed, cases may have been able to recall items that they believed caused their illness more easily than the rest of their food history. However, cases were interviewed by telephone so may have been prompted to recall their food history more than controls who filled in an online questionnaire independently. Cases were interviewed between 28 September 2022 and 17 October 2022 while controls were recruited between 17 October 2022 and 02 November 2022. Given questionnaires for cases and controls were filled in at different times, there may have been variation in items consumed perhaps due to weather or seasonality of produce. Both case and control questionnaires included many free text fields which had to be recoded into individual food items by the analysis team. Steps were taken to minimise differences in coding approaches between team members but an element of subjectivity in the coding remains. In the Welsh case-case (control) study, both groups were interviewed over the phone using the same questionnaire, making the data more directly comparable. The recruitment of a control group based on notified cases of STEC meant there was a defined period of illness which could be used to aid recall in the control groups. However, this study had a smaller sample size and so likely underpowered to detect significant differences.
Early on in the investigation, case exposure information was provided to the FSA so that food chain investigations, which are complex, resource intensive and take a considerable time, could be progressed in parallel with the ongoing epidemiological investigations. Food supply tracing to gather evidence for an implicated contaminated supply chain and implicated food vehicle is a key part of the outbreak investigation and response. In this outbreak investigation the FSA’s food chain investigations identified contaminated salad leaves as the most likely vehicle of infection.
Lettuce and salad leaves consumed in the UK come almost exclusively from the European Union during the autumn and winter months, while during the summer months most salad vegetables are domestically produced. FSA food chain investigations for the period of interest (early August to early September 2022) revealed that one specific grower was found to be either directly or indirectly linked to all the food service establishments or retailers of interest identified through case interviews by the public health agencies in the UK and in RoI.
The consideration of both national and international supply chains and the FSA’s communications via INFOSAN with trading partner countries ruled out a non-UK sourced product as the outbreak vehicle and provided further supporting evidence for the source being a domestic producer. Additionally, the early notification to the international public health community via EpiPulse and ability to share raw sequence data and to query international open access databases for matching sequences reported by other countries identified that the outbreak was not widely distributed beyond the UK and RoI. This provided further supporting evidence for a domestically sourced food being the vehicle of infection in this outbreak.
There is further phylogenetic evidence that supports the finding of a likely UK grown salad item as the vehicle of infection. The STEC O517 population structure is divided into 3 main lineages (I, II, I/II) and 7 sublineages (Ia, Ib, Ic, IIa, IIb, IIc and I/II), The outbreak strain belonged to sublineage IIb which has been endemic in the UK sheep population since the 1980s which would be consistent with a domestically produced food item being the likely vehicle of infection. Small clusters of cases infected with sublineage IIb have been previously linked to lamb meat products including lamb mince and sausages made from lamb mince, and pre-packed mixed salad leaves (19). In this outbreak, there had also been a small number of cases reported in previous years, the timing of which were roughly consistent with the UK fresh produce production season: 5/6 historical cases were reported with sample dates in September to October time previously. Contamination of fresh produce due to persistence of the organism in the environment has been linked to recurrent outbreaks of the same strain of STEC O157 in romaine lettuce previously (20).
The IMT identified that unusual weather patterns had coincided with the period of interest for a potential food product contamination event that overlapped with the estimated period of exposure based on case illness onset dates. Given these atypical weather events, the IMT considered that assessment of the potential impact of weather events on foodborne pathogen introduction, spread and amplification in food production environments was warranted.
The FSA investigations revealed that growers/suppliers noted a sequence of climate challenges in July and August 2022, including prolonged periods of extremely dry weather followed by excess rain, which in some instances caused flooding. Under these circumstances, soil is likely to have been very dry from a hot and prolonged dry period, making the ground less absorbent and increasing the risks of “run off”, “soil wash/splash” and surface flooding. A single atypical rainfall event was identified within a geographically restricted area in August, which likely caused localised flooding where the main growers of interest were located which could have amplified contamination of crops. Heavy rainfall washing pathogens from animal pastures into fields with crops causing direct contamination through surface flooding and contaminating water supply subsequently used to wash crops could all have played a role.
The outbreak was declared over in mid-October and no further cases have been reported in the UK since October 2022 with STEC infection caused by this specific outbreak strain t5:5294. Proactive communications regarding the outbreak investigation and advice regarding options for consumers to avoid infection were not published, nor were product recall or withdrawal measures undertaken as the outbreak was of very short duration and was over by the time the potential cause of infection was established, with all potentially contaminated product no longer on the market, due to a short shelf life for salad leaves and a likely single, time-limited contamination event established to be the cause of the outbreak.
Extensive direct engagement with industry was initiated by the FSA during the investigation and continued after the investigation was closed, to exchange data, information and best practise. FSA supported the UK Food Safety Research Network, (UKFSRN), an event which brought together wide industry stakeholders responsible for producing, processing, and selling fresh produce and to engage in dialogue on the contamination issues of UK fresh produce supply chain, and the FSA funded UKFSRN supported a project led by UK Fresh Produce Consortium to develop fresh produce sector specific food safety and hygiene training to improve capabilities going forward.
The findings of the outbreak investigation were shared with the public in a peer-reviewed publication in Eurosurveillance Journal in September 2024 (15).
Conclusions and recommendations
This was the largest outbreak of STEC O157 reported in the UK since the implementation of routine WGS and overall was one of the largest on record. The short outbreak duration is characteristic of outbreaks caused by a food item with a short shelf life, such as salad, fresh fruit and/or ready to eat/raw vegetables. Rapidly emerging and escalating but short duration outbreaks of infectious gastrointestinal disease associated with fresh produce items are challenging to investigate. Gathering detailed epidemiological data and undertaking robust epidemiological investigations takes time and food chain investigations to identify associated supply chains to implement control measures are also time and labour intense. The results of the descriptive epidemiological analyses supported the hypothesis that the vehicle was a salad product, potentially associated with catering settings, but subsequent analytical epidemiological studies did not derive convincing evidence of association with individual food products or ingredients as the vehicle(s) of infection in this outbreak.
During the period of peak case exposure in early to mid-September, in the absence of available evidence in relation to any specific product, process or associated risk, targeted risk management action could not be taken. However, the investigation was still progressed and the evidence gathered by the time the investigation was completed by the FSA strongly suggested UK grown salad leaves, sourced from a single grower (grower 1) was the vehicle of infection in this outbreak. There were no samples left from the hypothesised contaminated supply chain or batch so there were no food items to sample to confirm the findings microbiologically. At this point supply had switched from domestic to imported products so no on-going risk was identified. Although case numbers had reduced by the time the most likely implicated food supply chain had been identified, a re-emergence of the outbreak strain is possible in future years. Owing to the resumption of domestically produced salad in the next summer season, re-contamination of fresh produce due to persistence of the organism within the environment, which may explain the cases spanning multiple years in this cluster, is possible.
Recommendation 1: UKHSA should continue to work with partner agencies (PHS, PHW, PHA, FSA, Local Authorities, APHA etc) to progress full investigations into incidents to gather the best possible evidence for future preventative strategies.
Recommendation 2: Public health agencies, including UKHSA, and the Food Standards agencies in the UK should continue share information and findings with the food industry, including trade associations, and competent authorities
Recommendation 3: Multidisciplinary research to gather the best possible evidence for refining of future preventative strategies at industry level is required.
Contextual analysis of WGS data and international communications including sharing of sequence data, as well as the timing of the outbreak in relation to salad product supply chains indicated a UK grown nationally distributed food item with a short shelf life as the cause of this outbreak. The analysis of genomic data supported the epidemiological and food chain investigation findings as well as informing hypothesis generation, risk assessment and targeting the investigation.
Recommendation 4: UKHSA along with partners such as APHA should perform pathogen characterisation and phylogenetic analyses to achieve best possible understanding of the STEC O157 population structure in the UK, likely sources of contamination and risk analysis in future.
Due to the nature and potential severity of STEC infection, especially within vulnerable groups and risks of progression to HUS, early detection and investigation of potential outbreak events is important for safeguarding public health. The close integration of the epidemiology, bioinformatics and reference microbiology laboratory teams and utilisation of multiple data sources for routine surveillance purposes together with the close engagement between all partner public health agencies in sharing of information resulted in early identification of potential indicators for an emerging outbreak and facilitated the rapid escalation of the outbreak response in this instance. However, the variability in how frontline diagnostic laboratories report STEC O157 to SGSS reduces the capacity to detect signals of an emerging STEC outbreak through exceedance reporting compared with other gastrointestinal pathogens. Furthermore, there is known under-ascertainment of HUS cases (21) which can result in underestimation of the severity of outcomes associated with a specific STEC strain/outbreak.
Recommendation 5: UKHSA should review national STEC surveillance systems and data linkage opportunities and implement enhancements where gaps and/or opportunities are identified to enhance further the detection and risk assessment of emerging outbreak clusters.
The novel analysis done on weather data supported the evidence generation during this outbreak investigation. The utility of this type of analysis, where warranted, as well as the incorporation of other relevant data analyses to generate supporting evidence on a routine basis during national level outbreaks of infectious gastrointestinal disease is being explore.
Recommendation 6: UKHSA should work with partners to consider how to optimise and study the potential impact of weather events, the efficacy of risk assessments in place to ensure safe food, as well as other influencing and risk cascading factors on foodborne pathogen transmission, contamination and amplification in food production environments.
Appendices
Appendix 1. STEC O157 CC11, t25:2049 phylogenetic tree
Figure 6. Phylogenetic tree with outbreak strain (t5:5294) on red branch, annotated with country (black: England; blue: Scotland; green Wales; orange: Northern Ireland), receipt date, Stx subtype and SNP address
Appendix 2. Epidemiological study tables
Table 2. Multivariable model 1. (n=247 observations)
Variable | Category | Adjusted OR | 95% CI | Wald p-value | LRT p-value |
---|---|---|---|---|---|
Any chicken | No chicken eaten | Reference | <0.001 | ||
Eaten only prepared at home | 2.33 | 0.32 – 16.9 | 0.39 | ||
Eaten away from home [note 1] | 12.7 | 2.24 – 72.2 | <0.001 | ||
Any salad leaves | Eaten prepared at home or away | 1.76 | 0.72 – 4.31 | 0.20 | 0.20 |
Any beef | Eaten prepared at home or away | 1.53 | 0.69 – 3.38 | 0.29 | 0.29 |
Age group | 0 – 19 years | Reference | 0.28 | ||
20 – 39 years | 0.82 | 0.33 – 2.04 | 0.67 | ||
>40 years | 1.70 | 0.59 – 4.96 | 0.33 | ||
Gender | Female | Reference | 0.28 | ||
Male | 0.99 | 0.48 – 2.03 | 0.98 | ||
Other | 13.3 | 0.41 – 434 | 0.11 | ||
Country | England | Reference | 0.99 | ||
Northern Ireland | 0.90 | 0.23 – 3.51 | 0.88 | ||
Scotland | 0.85 | 0.27 – 2.73 | 0.79 | ||
Wales | 0.87 | 0.27 – 2.82 | 0.81 | ||
Proton pump inhibitor | Took medication | 1.55 | 0.53 – 4.50 | 0.43 | 0.43 |
Note 1: may also have eaten chicken prepared at home
Table 7. Multivariable model 2 (n=214 observations)
Variable | Category | Adjusted OR | 95% CI | p-value [note 1] | LRT p-value |
---|---|---|---|---|---|
Chicken pieces | Eaten prepared away from home [note 2] | 5.1 | 1.65 – 16.14 | 0.005 | 0.005 |
Chicken goujons | Eaten only prepared at home | 5.34 | 0.91 – 30.75 | 0.06 | 0.064 |
Chicken nuggets/ popcorn chicken | Eaten prepared at home or away | 1.57 | 0.53 – 4.48 | 0.41 | 0.41 |
Iceberg lettuce | Eaten prepared at home or away | 3.38 | 1.35 – 9.23 | 0.009 | 0.009 |
Any beef | Eaten prepared at home or away | 1.94 | 0.73 – 5.57 | 0.18 | 0.18 |
Age group | <20 years | Reference | 0.41 | ||
20-39 years | 1.11 | 0.36 – 3.73 | 0.86 | ||
40+ years | 2.31 | 0.56 – 11.03 | 0.25 | ||
Gender | Female | Reference | 0.05 | ||
Male | 2.00 | 0.82 – 5.1 | 0.13 | ||
Other | 32.07 | 1.15 – 5614.79 | 0.04 | ||
Country | England | Reference | 0.97 | ||
Northern Ireland | 0.73 | 0.08 – 4.2 | 0.75 | ||
Scotland | 0.76 | 0.16 – 2.77 | 0.69 | ||
Wales | 0.82 | 0.19 – 2.88 | 0.77 | ||
Proton pump inhibitor | Took medication | 1.73 | 0.41 – 6.15 | 0.43 | 0.43 |
Note 1: Profile penalised log-likelihood p-value
Note 2: May also have eaten chicken prepared at home
Appendix 3. Incident Management Team member organisations
The multidisciplinary Incident Management Team consisted of representatives from the following organisations:
- UK Health Security Agency (UKHSA, formerly Public Health England)
- Public Health Scotland
- Public Heath Wales
- Public Health Agency, Northern Ireland
- Food Standards Agency
- Food Standards Scotland
- Health Protection Surveillance Centre, Ireland
- Food Safety Authority of Ireland
- Local authorities
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