Salmonella Saintpaul outbreak associated with cantaloupe consumption, the United Kingdom and Portugal, September to November 2023.

In September 2023, the UK Health Security Agency identified cases of Salmonella Saintpaul distributed across England, Scotland, and Wales, all with very low genetic diversity. Additional cases were identified in Portugal following an alert raised by the United Kingdom. Ninety-eight cases with a similar genetic sequence were identified, 93 in the United Kingdom and 5 in Portugal, of which 46% were aged under 10 years. Cases formed a phylogenetic cluster with a maximum distance of six single nucleotide polymorphisms (SNPs) and average of less than one SNP between isolates. An outbreak investigation was undertaken, including a case-control study. Among the 25 UK cases included in this study, 13 reported blood in stool and 5 were hospitalized. One hundred controls were recruited via a market research panel using frequency matching for age. Multivariable logistic regression analysis of food exposures in cases and controls identified a strong association with cantaloupe consumption (adjusted odds ratio: 14.22; 95% confidence interval: 2.83-71.43; p-value: 0.001). This outbreak, together with other recent national and international incidents, points to an increase in identifications of large outbreaks of Salmonella linked to melon consumption. We recommend detailed questioning and triangulation of information sources to delineate consumption of specific fruit varieties during Salmonella outbreaks.

Two Outbreaks of Foodborne Gastrointestinal Infection Linked to Consumption of Imported Melons, United Kingdom, March to August 2021.

The aim of this study was to describe two foodborne outbreaks caused by contaminated imported melon and make recommendations for future practice. Between March and July 2021, there was an outbreak of 113 cases of Salmonella Braenderup in the UK (62% female, median age 61 years, 33% hospitalized). Analytical epidemiological studies identified Galia melons as the vehicle of infection (OR 671.9, 95% CI 39.0-58,074.0, p < 0.001). Subsequently, the outbreak strain was isolated from two samples of Galia melon imported from Latin America. In July and August 2021, there was an outbreak of 17 cases of Shiga toxin-producing Escherichia coli (STEC) O157:H7 in the UK (53% female, median age 21 years, 35% were hospitalized). Review of the STEC surveillance questionnaire data, followed by the analysis of responses from a modified hypothesis-generating questionnaire, implicated eating precut watermelon from retailer B sourced from Europe as the vehicle of infection. Outbreaks of gastrointestinal pathogens caused by contaminated food of nonanimal origin are a global public health concern. Given the difficulty in removing pathogens from the flesh of ready-to-eat fruit and vegetables, public health interventions should target all steps of the food chain prior to consumption, from cultivation on the farm to processing/packing and distribution.

Impact of the COVID-19 pandemic on gastrointestinal infection trends in England, February-July 2020.

OBJECTIVE: To establish the impact of the first 6 months of the COVID-19 outbreak response on gastrointestinal (GI) infection trends in England. DESIGN: Retrospective ecological study using routinely collected national and regional surveillance data from seven UK Health Security Agency coordinated laboratory, outbreak and syndromic surveillance systems using key dates of UK governmental policy change to assign phases for comparison between 2020 and historic data. RESULTS: Decreases in GI illness activity were observed across all surveillance indicators as COVID-19 cases began to peak. Compared with the 5-year average (2015-2019), during the first 6 months of the COVID-19 response, there was a 52% decrease in GI outbreaks reported (1544 vs 3208 (95% CI 2938 to 3478)) and a 34% decrease in laboratory confirmed cases (27 859 vs 42 495 (95% CI 40 068 to 44 922)). GI indicators began to rise during the first lockdown and lockdown easing, although all remained substantially lower than historic figures. Reductions in laboratory confirmed cases were observed across all age groups and both sexes, with geographical heterogeneity observed in diagnosis trends. Health seeking behaviour changed substantially, with attendances decreasing prior to lockdown across all indicators. CONCLUSIONS: There has been a marked change in trends of GI infections in the context of the COVID-19 pandemic. The drivers of this change are likely to be multifactorial; while changes in health seeking behaviour, pressure on diagnostic services and surveillance system ascertainment have undoubtably played a role, there has likely been a true decrease in the incidence for some pathogens resulting from the control measures and restrictions implemented. This suggests that if some of these changes in behaviour such as improved hand hygiene were maintained, then we could potentially see sustained reductions in the burden of GI illness.

Levels and genotypes of Salmonella and levels of Escherichia coli in frozen ready-to-cook chicken and turkey products in England tested in 2020 in relation to an outbreak of S. Enteritidis.

Frozen reformulated (FR) breaded chicken products have previously been implicated in causing human salmonellosis. A multi-country Salmonella enterica serovar Enteritidis outbreak involving several strains with >400 reported human cases in the UK occurred in 2020. Initially S. Infantis was detected in one sample from a case home but S. Enteritidis was then also isolated using a S. Enteritidis specific PCR in combination with isolation via a Craigie-tube. This prompted a survey to examine the presence and levels of Salmonella and E. coli in ready-to-cook FR poultry products in England in 2020. From a total of 483 samples, including two from cases' homes, Salmonella was detected in 42 chicken samples, these originated from six out of 53 production plants recorded. Salmonella detection was associated with elevated levels of generic E. coli (OR = 6.63). S. Enteritidis was detected in 17 samples, S. Infantis in 25, S. Newport in four and S. Java, S. Livingstone and S. Senftenberg in one each. The highest levels of Salmonella were 54 MPN/g for S. Infantis and 28 MPN/g for S. Enteritidis; 60% of the Salmonella-positive samples had <1.0 MPN/g. S. Enteritidis was detected together with S. Infantis in five samples and with S. Livingstone in one. Where S. Enteritidis was detected with other Salmonella, the former was present at between 2 and 100-fold lower concentrations. The Salmonella contamination was homogeneously distributed amongst chicken pieces from a single pack and present in both the outer coating and inner content. The S. Enteritidis were all outbreak strains and detected in six products that were linked to four production plants which implicated a Polish origin of contamination. Despite S. Infantis being most prevalent in these products, S. Infantis from only two contemporaneous human cases in the UK fell into the same cluster as isolates detected in one product. Except for one human case falling into the same cluster as one of the S. Newport strains from the chicken, no further isolates from human cases fell into clusters with any of the other serovars detected in the chicken samples. This study found that higher E. coli levels indicated a higher probability of Salmonella contamination in FR chicken products. The results also highlight the importance of recognising co-contamination of foods with multiple Salmonella types and has provided essential information for detecting and understanding outbreaks where multiple strains are involved.

Development and evaluation of an outbreak surveillance system integrating whole genome sequencing data for non-typhoidal Salmonella in London and South East of England, 2016-17.

An outbreak surveillance system for Salmonella integrating whole genome sequencing (WGS) and epidemiological data was developed in South East and London in 2016-17 to assess local WGS clusters for triage and investigation. Cases genetically linked within a 5 single-nucleotide polymorphism (SNP) single linkage cluster were assessed using a set of locally agreed thresholds based on time, person and place, for reporting to local health protection teams (HPTs). Between September 2016 and September 2017, 230 unique 5-SNP clusters (442 weekly reports) of non-typhoidal Salmonella 5-SNP WGS clusters were identified, of which 208 unique 5-SNP clusters (316 weekly reports) were not reported to the HPTs. In the remaining 22 unique clusters (126 weekly clusters) reported to HPTs, nine were known active outbreak investigations, seven were below locally agreed thresholds and six exceeded local thresholds. A common source or vehicle was identified in four of six clusters that exceeded locally agreed thresholds. This work demonstrates that a threshold-based surveillance system, taking into account time, place and genetic relatedness, is feasible and effective in directing the use of local public health resources for risk assessment and investigation of non-typhoidal Salmonella clusters.

Genomic epidemiology of emerging ESBL-producing Salmonella Kentucky bla CTX-M-14b in Europe.

Global dissemination of ciprofloxacin-resistant Salmonella Kentucky has been observed over the past decades. In recent years, there have been reports of extended-spectrum ß-lactamase (ESBL) producing S. Kentucky. Routine surveillance at the European Centre for Disease Prevention and Control (ECDC) detected cases with a ciprofloxacin-resistant S. Kentucky with the ESBL-gene bla CTX-M-14b. Ensuing research identified 78 cases in 2013-2018 in eight European countries. Compared to other S. Kentucky and non-typhoidal Salmonella infections, reported to the European Surveillance System, these cases were more likely to be elderly and to present urinary-tract infections. Bayesian time-scaled phylogeny on whole genome sequences of isolates from these cases and supplementary isolates from public sequence databases was used to infer the origin and spread of this clone. We dated the origin of the bla CTX-M-14b clone to approximately 2005 in Northern Africa, most likely in Egypt. The geographic origin predicted by the phylogenetic analysis is consistent with the patients' travel history. Next to multiple introductions of the clone to Europe from Egypt, our analysis suggests that in some parts of Europe the clone might have formed a stable population, from which further spread has occurred. Comparative genomics indicated that the bla CTX-M-14b gene is present on the bacterial chromosome, within the type VI secretion system region. The bla CTX-M-14b gene is integrated downstream of the hcp1 gene, on a 2854 bp plasmid fragment containing also ISEcp1. This is the first report of a chromosomally integrated CTX-M gene in Salmonella spp. in Europe, previous studies having identified similar genes only on plasmids.

The Transformation of Reference Microbiology Methods and Surveillance for Salmonella With the Use of Whole Genome Sequencing in England and Wales.

The use of whole genome sequencing (WGS) as a method for supporting outbreak investigations, studying Salmonella microbial populations and improving understanding of pathogenicity has been well-described (1-3). However, performing WGS on a discrete dataset does not pose the same challenges as implementing WGS as a routine, reference microbiology service for public health surveillance. Challenges include translating WGS data into a useable format for laboratory reporting, clinical case management, Salmonella surveillance, and outbreak investigation as well as meeting the requirement to communicate that information in an understandable and universal language for clinical and public health action. Public Health England have been routinely sequencing all referred presumptive Salmonella isolates since 2014 which has transformed our approach to reference microbiology and surveillance. Here we describe an overview of the integrated methods for cross-disciplinary working, describe the challenges and provide a perspective on how WGS has impacted the laboratory and surveillance processes in England and Wales.

Salmonellosis outbreak with novel Salmonella enterica subspecies enterica serotype (11:z41:e,n,z15) attributable to sesame products in five European countries, 2016 to 2017.

In spring 2016, Greece reported an outbreak caused by a previously undescribed Salmonella enterica subsp. enterica serotype (antigenic formula 11:z41:e,n,z15) via the Epidemic Intelligence Information System for Food- and Waterborne Diseases and Zoonoses (EPIS-FWD), with epidemiological evidence for sesame products as presumptive vehicle. Subsequently, Germany, Czech Republic, Luxembourg and the United Kingdom (UK) reported infections with this novel serotype via EPIS-FWD. Concerned countries in collaboration with the European Centre for Disease Prevention and Control (ECDC) and European Food Safety Authority (EFSA) adopted a common outbreak case definition. An outbreak case was defined as a laboratory-confirmed notification of the novel Salmonella serotype. Between March 2016 and April 2017, 47 outbreak cases were notified (Greece: n = 22; Germany: n = 13; Czech Republic: n = 5; Luxembourg: n = 4; UK: n = 3). Whole genome sequencing revealed the very close genetic relatedness of isolates from all affected countries. Interviews focusing on sesame product consumption, suspicious food item testing and trace-back analysis following Salmonella spp. detection in food products identified a company in Greece where sesame seeds from different countries were processed. Through European collaboration, it was possible to identify and recall sesame spread as one contaminated food item serving as vehicle of infection and trace it back to its origin.

An investigation of Salmonella Fluntern illnesses linked to leopard geckos-United States, 2018.

Reptile contact can result in zoonotic non-typhoidal salmonellosis. In April 2018, Oregon Public Health Division contacted CDC about a cluster of four Salmonella serovar Fluntern (SF) illnesses in four states (OR, CA, IA, NY); patients reported contact with geckos, a popular reptile pet. PulseNet, the national molecular subtyping network of food-borne disease surveillance, subsequently identified additional SF clinical isolates. Twelve cases in 11 states were identified; median age was 5 years (range: <1-58 years). Three patients were hospitalized; no deaths were reported. Of those with exposure information (n = 10), all reported reptile exposure; 9 (90%) specified contact with leopard geckos. No common source of geckos was identified from reported purchase locations. Los Angeles County (LAC) health officials isolated SF from one patient's leopard gecko. Five reptile/gecko isolates were identified from the USDA National Veterinary Services Laboratories (NVSL) from 2015 to 2018. Five countries responded to an Epidemic Intelligence Information System post by PulseNet; reptile isolate sequence data were received from Czech Republic. A clinical case from England was identified through the National Center for Biotechnology Information pathogen detection pipeline; the patient did not report contact with leopard geckos. Whole genome sequencing analysis revealed substantial genetic diversity between clinical and animal isolates; however, gecko and clinical isolates from LAC were highly related (1 allele difference). This investigation linking SF illnesses to leopard geckos highlights an important public health risk from pets. A better understanding of how geckos are distributed by the pet industry in the United States could improve traceability to points of origin and mitigate Salmonella transmission at gecko breeders. Earlier NVSL reports of SF isolates from geckos suggest the risk of human SF infection from geckos is not new. This investigation demonstrates a need to educate gecko breeders, retailers and gecko owners about the continued Salmonella infection risk from pet geckos.

Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella Enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana.

BACKGROUND: Salmonella enterica serovar Enteritidis is a cause of both poultry- and egg-associated enterocolitis globally and bloodstream-invasive nontyphoidal Salmonella (iNTS) disease in sub-Saharan Africa (sSA). Distinct, multi-drug resistant genotypes associated with iNTS disease in sSA have recently been described, often requiring treatment with fluoroquinolone antibiotics. In industrialised countries, antimicrobial use in poultry production has led to frequent fluoroquinolone resistance amongst globally prevalent enterocolitis-associated lineages. METHODOLOGY/PRINCIPAL FINDINGS: Twenty seven S. Enteritidis isolates from patients with iNTS disease and two poultry isolates, collected between 2007 and 2015 in the Ashanti region of Ghana, were whole-genome sequenced. These isolates, notable for a high rate of diminished ciprofloxacin susceptibility (DCS), were placed in the phyletic context of 1,067 sequences from the Public Health England (PHE) S. Enteritidis genome database to understand whether DCS was associated with African or globally-circulating clades of S. Enteritidis. Analysis showed four of the major S. Enteritidis clades were represented, two global and two African. All thirteen DCS isolates, containing a single gyrA mutation at codon 87, belonged to a global PT4-like clade responsible for epidemics of poultry-associated enterocolitis. Apart from two DCS isolates, which clustered with PHE isolates associated with travel to Spain and Brazil, the remaining DCS isolates, including one poultry isolate, belonged to two monophyletic clusters in which gyrA 87 mutations appear to have developed within the region. CONCLUSIONS/SIGNIFICANCE: Extensive phylogenetic diversity is evident amongst iNTS disease-associated S. Enteritidis in Ghana. Antimicrobial resistance profiles differed by clade, highlighting the challenges of devising empirical sepsis guidelines. The detection of fluoroquinolone resistance in phyletically-related poultry and human isolates is of major concern and surveillance and control measures within the region's burgeoning poultry industry are required to protect a human population at high risk of iNTS disease.

An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study.

BACKGROUND: Salmonella spp are a major cause of food-borne outbreaks in Europe. We investigated a large multi-country outbreak of Salmonella enterica serotype Enteritidis in the EU and European Economic Area (EEA). METHODS: A confirmed case was defined as a laboratory-confirmed infection with the outbreak strains of S Enteritidis based on whole-genome sequencing (WGS), occurring between May 1, 2015, and Oct 31, 2018. A probable case was defined as laboratory-confirmed infection with S Enteritidis with the multiple-locus variable-number tandem repeat analysis outbreak profile. Multi-country epidemiological, trace-back, trace-forward, and environmental investigations were done. We did a case-control study including confirmed and probable cases and controls randomly sampled from the population registry (frequency matched by age, sex, and postal code). Odds ratios (ORs) for exposure rates between cases and controls were calculated with unmatched univariable and multivariable logistic regression. FINDINGS: 18 EU and EEA countries reported 838 confirmed and 371 probable cases. 509 (42%) cases were reported in 2016, after which the number of cases steadily increased. The case-control study results showed that cases more often ate in food establishments than did controls (OR 3·4 [95% CI 1·6-7·3]), but no specific food item was identified. Recipe-based food trace-back investigations among cases who ate in food establishments identified eggs from Poland as the vehicle of infection in October, 2016. Phylogenetic analysis identified two strains of S Enteritidis in human cases that were subsequently identified in salmonella-positive eggs and primary production premises in Poland, confirming the source of the outbreak. After control measures were implemented, the number of cases decreased, but increased again in March, 2017, and the increase continued into 2018. INTERPRETATION: This outbreak highlights the public health value of multi-country sharing of epidemiological, trace-back, and microbiological data. The re-emergence of cases suggests that outbreak strains have continued to enter the food chain, although changes in strain population dynamics and fewer cases indicate that control measures had some effect. Routine use of WGS in salmonella surveillance and outbreak response promises to identify and stop outbreaks in the future. FUNDING: European Centre for Disease Prevention and Control; Directorate General for Health and Food Safety, European Commission; and National Public Health and Food Safety Institutes of the authors' countries (see Acknowledgments for full list).

Operational burden of implementing Salmonella Enteritidis and Typhimurium cluster detection using whole genome sequencing surveillance data in England: a retrospective assessment.

Since April 2014 all presumptive Salmonella isolates received by Public Health England (PHE) have been characterised using whole genome sequencing (WGS) and the genomic data generated used to identify clusters of infection. To inform the implementation and development of a national gastrointestinal infection surveillance system based on WGS we have retrospectively identified genetically related clusters of Salmonella Enteritidis and Salmonella Typhimurium infection over a one year period and determined the distribution of these clusters by PHE operational levels. Using a constrained WGS cluster definition based on single nucleotide polymorphism distance, case frequency and temporal spread we demonstrate that the majority of clusters spread to multiple PHE operational levels. The greatest investigative burden is on national level staff investigating small, geographically dispersed clusters. We also demonstrate that WGS identifies long-running, slowly developing clusters that may previously have remained undetected. This analysis also indicates likely increased workload for local health protection teams and will require an operational strategy to balance limited human resources with the public health importance of investigating small, geographically contained clusters of highly related cases. While there are operational challenges to its implementation, integrated cluster detection based on WGS from local to international level will provide further improvements in the identification of, response to and control of clusters of Salmonella spp. with public health significance.

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.

ESBL-Producing and Macrolide-Resistant Shigella sonnei Infections among Men Who Have Sex with Men, England, 2015.

In England in 2015, Shigella sonnei isolates from men who have sex with men produced extended-spectrum ß-lactamases and exhibited macrolide resistance. Whole-genome sequencing showed a close relationship among the isolates, which harbored a plasmid that was previously identified in a shigellosis outbreak among this population but has acquired a mobile element.

Impact of socioeconomic deprivation on mortality in people with haemorrhagic stroke: a population-based cohort study.

PURPOSE: Socioeconomic deprivation (SED) has an effect on many health outcomes, including ischaemic stroke; however, its impact on mortality after haemorrhagic stroke remains unclear, particularly in the long run. We examined this association in a multiethnic population in the UK. DESIGN: We examined data from 782 patients with first-ever haemorrhagic stroke, collected by the South London Stroke Register from 1995 to 2011. SED was defined as the quartile with the highest Carstairs scores, and was analysed in relation to mortality after stroke in a multivariate-adjusted Cox regression model. RESULTS: In a follow-up of 17 years, 498 patients died. Compared with the first quartile of Carstairs score (the least deprived), the multivariate-adjusted HRs for 17-year mortality in patients in the second, third and fourth quartiles were 0.94 (95% CI 0.72 to 1.23), 1.17 (95% CI 0.90 to 1.52) and 1.36 (95% CI 1.04 to 1.78), overall p=0.04. The SED gradient association remained in patients with intracerebral haemorrhagic stroke, while in patients with subarachnoid haemorrhagic stroke the corresponding HRs were 2.62 (95% CI 1.22 to 5.64), 3.03 (95% CI 1.49 to 6.18) and 1.83 (95% CI 0.87 to 3.83), respectively. Results of 10-year mortality showed similar patterns, although the association of deprivation with 1-year mortality was not significant. CONCLUSIONS: There is a significant impact of SED on long-term mortality after haemorrhagic stroke. The reasons for this survival inequality must be explored to reduce mortality in patients with haemorrhagic stroke.