Outbreak of Salmonella Typhimurium linked to Swedish pre-washed rocket salad, Sweden, September to November 2022.

In September 2022, the Public Health Agency of Sweden observed an increase in domestic Salmonella Typhimurium cases through the Swedish electronic notification system, and an outbreak strain was identified with whole genome sequencing. Overall, 109 cases with symptom onset between 17 September and 24 November 2022 were reported from 20 of 21 Swedish regions. The median age of cases was 52 years (range 4-87 years) and 62% were female. A case-control study found cases to be associated with consumption of rocket salad (adjusted odds ratio (aOR) = 4.9; 95% confidence interval (CI): 2.4-10, p value < 0.001) and bagged mixed salad (aOR = 4.0; 95% CI: 1.9-8.1, p value < 0.001). Trace-back, supported by Finnish authorities who identified the Swedish outbreak strain in a Finnish cluster during the same time period, identified rocket salad, cultivated, pre-washed and pre-packed in Sweden as the likely source of the outbreak. No microbiological analyses of rocket salad were performed. Our investigation indicates that bagged leafy greens such as rocket salad, regardless of pre-washing procedures in the production chain, may contain Salmonella and cause outbreaks, posing a health risk to consumers. We emphasise the need for primary producers of leafy greens to identify possible contamination points to prevent outbreaks.

Epidemiology and antimicrobial resistance of Salmonella serovars Typhimurium and 4,[5],12:i- recovered from hospitalized patients in China.

Global emergence of multidrug-resistant (MDR) Salmonella enterica serovar Typhimurium is a continuing challenge for modern healthcare. However, the knowledge, regarding the epidemiology of salmonellosis caused by the monophasic variant S. 4,[5],12:i:- in hospitalized patients, is limited in China. To bridge this gap, we carried out a retrospective study to determine the antimicrobial resistance, trends, and risk factors of S. Typhimurium and S. 4,[5],12:i:- (n = 329) recovered from patients in Zhejiang province between 2011 and 2019. The results showed that 90.57% (298/329) of the isolates were MDR; among them, 48.94% (161/329) and 12.46% (41/329) were phenotypically resistant to cephalosporins and fluoroquinolones, respectively, which are the drugs of choice used to treat salmonellosis in clinics. Additionally, we observed a higher incidence of infections among the young population (<5 years old). Notably, the higher prevalence of ST34 (sequence type 34) isolates, especially after 2014, with MDR (57.05%, 170/298) phenotype, and incidence of ST34 isolates co-harbouring mcr-1 (mobile colistin resistance gene) and blaCTX-M-14 (ß-lactamase gene) suggest an association between STs and drug resistance. Together, the increasing prevalence of MDR ST34 calls for enhanced monitoring strategies to mitigate the spread and dissemination of MDR clones of S. Typhimurium and S. 4,[5],12:i-. Our study provides improved knowledge about non-typhoid Salmonella (NTS) infections, which could help in the effective recommendation of antimicrobials in hospitalized patients.

Salmonellosis outbreak archive in China: data collection and assembly.

Infectious disease outbreaks transcend the medical and public health realms, triggering widespread panic and impeding socio-economic development. Considering that self-limiting diarrhoea of sporadic cases is usually underreported, the Salmonella outbreak (SO) study offers a unique opportunity for source tracing, spatiotemporal correlation, and outbreak prediction. To summarize the pattern of SO and estimate observational epidemiological indicators, 1,134 qualitative reports screened from 1949 to 2023 were included in the systematic review dataset, which contained a 506-study meta-analysis dataset. In addition to the dataset comprising over 50 columns with a total of 46,494 entries eligible for inclusion in systematic reviews or input into prediction models, we also provide initial literature collection datasets and datasets containing socio-economic and climate information for relevant regions. This study has a broad impact on advancing knowledge regarding epidemic trends and prevention priorities in diverse salmonellosis outbreaks and guiding rational policy-making or predictive modeling to mitigate the infringement upon the right to life imposed by significant epidemics.

Quantitative microbial risk assessment of Salmonella in fresh chicken patties.

Quantitative microbial risk assessment (QMRA) has witnessed rapid development within the context of food safety in recent years. As a means of contributing to these advancements, a QMRA for Salmonella spp. in fresh chicken patties for the general European Union (EU) population was developed. A two-dimensional (Second Order) Monte-Carlo simulation method was used for separating variability and uncertainty of model's parameters. The stages of industrial processing, retail storage, domestic storage, and cooking in the domestic environment were considered in the exposure assessment. For hazard characterization, a dose-response model was developed by combining 8 published dose-response models using a Pert distribution for describing uncertainty. The QMRA model predicted a mean probability of illness of 1.19*10-4 (5.28*10-5 - 3.57*10-4 95 % C.I.), and a mean annual number of illnesses per 100,000 people of 2.13 (0.96 - 6.59 95 % C.I.). Moreover, sensitivity analysis was performed, and variability in cooking preferences was found to be the most influential model parameter (r = -0.39), followed by dose-response related variability (r = 0.22), and variability in the concentration of Salmonella spp. at the time of introduction at the processing facility (r = 0.11). Various mitigation strategy scenarios were tested, from which, "increasing the internal temperature of cooking" and "decreasing shelf life" were estimated to be the most effective in reducing the predicted risk of illness. Salmonella-related illnesses exhibit particularly high severity, making them some of the most prominent zoonotic diseases in the EU. Regular monitoring of this hazard in order to further highlight its related parameters and causes is a necessary procedure. This study not only provides an updated assessment of Salmonella spp. risk associated with chicken patties, but also facilitates the identification of crucial targets for scientific investigation and implementation of real-world intervention strategies.

Multinational collaboration in solving a European Salmonella Braenderup outbreak linked to imported melons, 2021.

A genomic cluster of Salmonella Braenderup ST22, a serovar of Salmonella enterica subsp. enterica which causes symptoms of gastrointestinal illness, was notified by Danish authorities to the European Centre for Disease Prevention and Control (ECDC) on 3 May 2021. By 6 July 2021, S. Braenderup outbreak cases (n = 348) had been reported from 12 countries in the European Union/European Economic Area (EU/EEA) and the United Kingdom (UK), including 68 hospitalised cases. With support from affected EU/EEA countries, and in partnership with the European Food Safety Authority (EFSA), ECDC established an international outbreak investigation team to rapidly identify the source and prevent outbreak spread. Consumption information was shared with affected countries through a standard line list, revealing that 124 of 197 cases (63%) reported having eaten (any) melons within 7 days prior to disease onset. The speed and completeness of the investigation, which identified the outbreak vehicle as galia melons imported from Honduras in June 2021, was a direct result of extensive collaboration and information sharing between countries' national food safety and public health authorities. This article describes the outbreak and the benefits, successes, and challenges of multi-country collaboration for consideration in future large foodborne outbreaks across Europe.

Nontyphoidal Salmonella Outbreaks Associated With Chocolate Consumption: A Systematic Review.

BACKGROUND: A large, cross-border outbreak of nontyphoidal salmonellosis connected to chocolate product consumption was recently reported. This occurrence motivated us to conduct a comprehensive review of existing literature concerning outbreaks of nontyphoidal salmonellosis associated with chocolate consumption. METHODS: We performed a systematic review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (PROSPERO CRD42022369023) in 3 databases: U.S. National Library of Medicine, Web of Science and Excerpta Medica. Google Scholar and the bibliography of each identified report were also screened. Eligible were articles published after 1970, describing outbreaks of more than 10 patients with a nontyphoidal salmonellosis associated with chocolate consumption. RESULTS: Twenty-three articles were included, which described 12 outbreaks involving a total of 3266 patients. All outbreaks occurred in high-income countries: 1 was limited to 1 city, 6 involved 1 country and the remaining 5 involved 2 or more countries. Six outbreaks peaked in winter, 3 in autumn, 2 in spring and 1 in summer. Children were mainly affected. No predominant serotype was identified. CONCLUSIONS: Our data documents that chocolate is an optimal medium for the transmission of nontyphoidal salmonellosis. A connected worldwide reporting system including high-income, middle-income and low-income countries is crucial to detect infectious diseases outbreaks in an early phase and avoid their spread.

Assessment of environmental safety and protective efficacy of O-antigen deficient DIVA capable Salmonella Enteritidis against chicken salmonellosis.

In this study, we incorporated deletion of the O-antigen ligase gene to an attenuated Salmonella Enteritidis (SE) strain, JOL919 (SE PS; Δlon ΔcpxR), using the Lambda-Red recombination method and evaluated the safety and immunological aspects of the novel genotype, JOL2381 (SE VS: Δlon, ΔcpxR, ΔrfaL). Assessment of fecal shedding and organ persistence following administration via oral and IM routes revealed that the SE VS was safer than its parent strain, SE PS. Immunological assays confirmed that immunization via the oral route with SE PS was superior to the SE VS. However, chickens immunized with SE PS and SE VS strains via the IM route showed higher humoral and cell-mediated immune responses. Compared to PBS control, the IM route of immunization with SE VS resulted in a higher IgY antibody titer and expansion of CD4+ and CD8+ T-cell populations, which resulted in the clearance of Salmonella from the liver and splenic tissues. Furthermore, deletion of the O-antigen ligase gene caused lower production of LPS-specific antibodies in the host, promoting DIVA functionality and making it a plausible candidate for field utilization. Due to significant protection, high attenuation, and environmental safety concerns, the present SE VS strain is an ideal choice to prevent chicken salmonellosis and ensure public health.

An outbreak of Salmonella Typhimurium associated with the consumption of raw liver at an Eid al-Adha celebration in Wales (UK), July 2021.

In July 2021, Public Health Wales received two notifications of salmonella gastroenteritis. Both cases has attended the same barbecue to celebrate Eid al-Adha, two days earlier. Additional cases attending the same barbecue were found and an outbreak investigation was initiated. The barbecue was attended by a North African community's social network. On same day, smaller lunches were held in three homes in the social network. Many people attended both a lunch and the barbecue. Cases were defined as someone with an epidemiological link to the barbecue and/or lunches with diarrhoea and/or vomiting with date of onset following these events. We undertook a cohort study of 36 people attending the barbecue and/or lunch, and a nested case-control study using Firth logistic regression. A communication campaign, sensitive towards different cultural practices, was developed in collaboration with the affected community. Consumption of a traditional raw liver dish, 'marrara', at the barbecue was the likely vehicle for infection (Firth logistic regression, aOR: 49.99, 95%CI 1.71-1461.54, p = 0.02). Meat and offal came from two local butchers (same supplier) and samples yielded identical whole genome sequences as cases. Future outbreak investigations should be relevant to the community affected by considering dishes beyond those found in routine questionnaires.

Development of recombinant subunit vaccine targeting InvH protein of Salmonella Typhimurium and evaluation of its immunoprotective efficacy against salmonellosis.

Salmonella Typhimurium is the most prevalent non-host specific Salmonella serovars and a major concern for both human and animal health systems worldwide contributing to significant economic loss. Type 3 secretion system (T3SS) of Salmonella plays an important role in bacterial adherence and entry into the host epithelial cells. The product of invH gene of Salmonella is an important component of the needle complex of the type 3 secretion system. Hence, the present study was undertaken to clone and express the 15 kDa InvH surface protein of Salmonella Typhimurium in an E. coli host and to evaluate its immune potency in mice. The purified recombinant InvH (r-InvH) protein provoked a significant (p < 0.01) rise in IgG in the inoculated mice. The immunized mice were completely (100%) protected against the challenge dose of 107.5 LD50, while protection against challenge with the same dose of heterologous serovars was 90%. The bacterin-vaccinated group showed homologous protection of 60% against all three serovars. Findings in this study suggest the potential of the r-InvH protein of S. Typhimurium as an effective vaccine candidate against Salmonella infections.

Human Salmonellosis Outbreak Linked to Salmonella Typhimurium Epidemic in Wild Songbirds, United States, 2020-2021.

Salmonella infection causes epidemic death in wild songbirds, with potential to spread to humans. In February 2021, public health officials in Oregon and Washington, USA, isolated a strain of Salmonella enterica serovar Typhimurium from humans and a wild songbird. Investigation by public health partners ultimately identified 30 illnesses in 12 states linked to an epidemic of Salmonella Typhimurium in songbirds. We report a multistate outbreak of human salmonellosis associated with songbirds, resulting from direct handling of sick and dead birds or indirect contact with contaminated birdfeeders. Companion animals might have contributed to the spread of Salmonella between songbirds and patients; the outbreak strain was detected in 1 ill dog, and a cat became ill after contact with a wild bird. This outbreak highlights a One Health issue where actions like regular cleaning of birdfeeders might reduce the health risk to wildlife, companion animals, and humans.

Multistate outbreak of turtle-associated salmonellosis highlights ongoing challenges with the illegal sale and distribution of small turtles.

The sale and distribution of small turtles (shell length <4 inches) as pets has been banned in the United States since 1975 because of the risk of Salmonella transmission, especially to children. Despite this 48-year-old ban, salmonellosis outbreaks continue to be linked to contact with small turtles. During investigations of turtle-associated outbreaks, information regarding the turtle farm of origin is difficult to obtain because turtles are commonly sold by transient vendors. During 2020-2021, public health officials investigated a multistate illness outbreak caused by Salmonella enterica serotype Typhimurium linked to pet small turtles. Cases were defined as a laboratory-confirmed Salmonella Typhimurium infection highly related (within 0-6 allele differences) to the outbreak strain based on whole-genome sequencing analysis by core-genome multilocus sequence typing with illness onset occurring during 27 August 2020-14 May 2021. Forty-three patients were identified from 12 states; of these, 35% (15/43) were children <5 years old. Among patients with available information, 37% (14/38) were hospitalized, and one death was reported. Seventy-four percent (25/34) of patients reported turtle exposure in the week before illness onset, and 84% (16/19) specified exposure to small turtles. The outbreak strain was isolated from samples collected from a Pennsylvania patient's small turtle tank. Two patients reported purchasing their small turtles from pet stores. Salmonella Braenderup was isolated from samples collected from small turtles and their habitat at one of these stores; however, at that time, this strain was not associated with any human illnesses. This investigation was notable because of the documented sale of small turtles from several pet stores combined with the identification of a single small turtle supplier to these pet stores. The high proportion of children involved in this outbreak highlights the continued need to educate the pet industry as well as parents and caregivers about the risk of turtle-associated salmonellosis especially in children. Understanding and addressing the persisting challenges related to the illegal sale and distribution of small turtles could reduce the burden of turtle-associated salmonellosis.

Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis.

With poultry products as one of the leading reservoirs for the pathogen, in a typical year in the United States, it is estimated that over one million individuals contract non-typhoidal Salmonella infections. Foodborne outbreaks associated with Salmonella infections in poultry, thus, continue to remain a significant risk to public health. Moreover, the further emergence of antimicrobial resistance among various serovars of Salmonella is an additional public health concern. Feeding-based strategies (such as use of prebiotics, probiotics, and/or phytobiotics as well as essential oils), non-feeding-based strategies (such as use of bacteriophages, vaccinations, and in ovo strategies), omics tools and surveillance for identifying antibiotic-resistance genes, post-harvest application of antimicrobials, and biosecurity measures at poultry facilities are practical interventions that could reduce the public health burden of salmonellosis and antibiotic resistance associated with poultry products. With the escalating consumption of poultry products around the globe, the fate, prevalence, and transmission of Salmonella in agricultural settings and various poultry-processing facilities are major public health challenges demanding integrated control measures throughout the food chain. Implementation of practical preventive measures discussed in the current study could appreciably reduce the public health burden of foodborne salmonellosis associated with poultry products.

An Outbreak of Salmonella Typhimurium Infections Linked to Ready-To-Eat Tofu in Multiple Health Districts - Ontario, Canada, May-July 2021.

From May to mid-August 2021, the Ontario, Canada provincial public health agency, Public Health Ontario, in collaboration with local public health authorities and federal food safety partners, investigated a spatiotemporal cluster of 38 patients with Salmonella Typhimurium infections across multiple public health districts in Ontario. Five (13%) patients were hospitalized; no deaths were reported. The outbreak was linked to consumption of ready-to-eat seasoned tofu from one manufacturer that was distributed to multiple Ontario restaurants. Isolates from the seasoned tofu were within one or fewer allele differences to the outbreak strain by whole genome sequencing. Evidence from food safety investigations conducted by local public health authorities and the Canadian Food Inspection Agency (CFIA) revealed that unsanitary conditions could have led to cross-contamination of the tofu, and insufficient heating of the tofu at the production level likely resulted in failure to eliminate the pathogen. The CFIA issued a food recall for the tofu at hotel, restaurant, and institution levels. Tofu was identified as a novel outbreak-associated food vehicle for S. Typhimurium in this outbreak. Interventions that target the production level and all parts of the supply chain and include additional safeguarding steps that minimize microbial growth are important.

Salmonella assessment along the Spanish food chain: Likelihood of Salmonella occurrence in poultry and pig products is maintained across the food chain stages.

Salmonellosis is one of the most important foodborne diseases worldwide, including the European Union. Despite the One Health approach measures for risk assessment and risk management implemented by the European Union, the occurrence of disease and disease outbreaks remains high (e.g. 694 outbreaks were reported in 2020), highlighting the need of new assessment methods. Herein we applied machine learning using the random forests method to evaluate and identify key points regarding the occurrence of Salmonella sp. along the Spanish food chain during 2015-2020, using data provided by the Spanish Agency for Food Safety and Nutrition. We compared the role of the three categorical variables [product (20 categories), region (18 categories) and stage (11 categories)]. Salmonella presence was influenced by the three explanatory variables considered: first by product, followed by region and stage. The most determinant product for Salmonella probability was 'meat', while the most important stage was 'slaughterhouse'. Specifically, the highest values were found in pig and poultry meats. In these products, the Salmonella probability was high at the early and final stages of the food chain, although not at intermediate stages. The presence of Salmonella in the final stages (retail) of the food chain is of concern, as it can cause human cases of salmonellosis, including outbreaks. This study demonstrates the utility of the random forest method to identify key points and evaluate the control efforts. We recommend improving the surveillance and control measures, especially in the product and stages pointed out by our analysis, and enhancing the data collection harmonization among the different autonomous communities.

Implementation of routine genomic surveillance provided insights into a locally acquired outbreak caused by a rare clade of Salmonella enterica serovar Enteritidis in Queensland, Australia.

Salmonellosis is a significant public health problem globally. In Australia, Salmonella enterica serovar Enteritidis is one of the main causes of salmonellosis. This study reports how the implementation of routine genetic surveillance of isolates from human S. Enteritidis cases enabled identification of the likely source of an outbreak that occurred in a remote town in Far North Queensland, Australia. This study included patient, food and water samples collected during an outbreak investigation. S. Enteritidis of the novel sequence type 5438 was isolated from all seven patient samples and one bore water sample but not any of the food samples. Both whole-genome single nucleotide polymorphism (SNP) and core-genome multilocus sequence typing analysis revealed that S. Enteritidis isolated from outbreak-related patient samples and the bore water isolates clustered together with fewer than five SNP differences and ten allelic differences. This genetic relatedness informed the outbreak response team around public health interventions and no further cases were identified post-treatment of the bore water. This disease cluster was identified through the routine sequencing of S. Enteritidis performed by the state public health laboratory in an actionable time frame. Additionally, genomic surveillance captured a case with unknown epidemiological links to the affected community, ruled out a simultaneous outbreak in an adjacent state as the source and provided evidence for the likely source preventing further transmission. Therefore, this report provides compelling support for the implementation of whole-genome sequencing based genotyping methods in public health microbiology laboratories for better outbreak detection and management.

Dominant Salmonella Serovars in Australian Broiler Breeder Flocks and Hatcheries: a Longitudinal Study.

A longitudinal study was conducted to determine the dominance and prevalence of Salmonella enterica subsp in Australian broiler breeder flocks and hatcheries. Twenty-two flocks (n = 3339 samples) were sampled over 6 time points beginning at placement until week 40. Hatcheries (n = 274 samples) were sampled following removal of chicks hatched from eggs originating from the 22 donor parent flocks. The percent of positive flocks (36%) and frequency of positive samples (15.6%) were highest during rearing at week 7. The frequency of positive samples decreased over the 40 weeks; however, the number of positive flocks remained relatively consistent. Geographical location had a greater influence on Salmonella detection frequency than company sample origin, despite differing management and vaccination protocols within and between companies. Twelve serovars were detected in total. The predominant serovars during rearing were Salmonella Mbandaka (32%), S. Saintpaul (27%), and S. Liverpool (18%). The predominant serovars detected during production were S. Cubana (27%), S. Saintpaul (24%), and S. Havana (13%). Salmonella Typhimurium, S. Ohio, and S. Hessarek were detected in the hatcheries. Of the serovars detected, only S. Typhimurium and S. Ohio were found in both broiler breeder flocks and hatcheries. However, detection did not correspond to the status of the flock eggs feeding into the hatchery. This study provides an up-to-date capture of the current Salmonella serovars circulating in the broiler breeder industry. Continued surveillance within the Australian Chicken Meat industry is imperative to mitigate and reduce the risk of salmonellosis in the community related to chicken meat. IMPORTANCE This study identified prevalent and dominant Salmonella enterica subsp in Australian Broiler Breeder flocks, as well as in hatcheries post chick hatch and removal, from eggs originating from these donor parent flocks. The captured Salmonella data was further compared to the most common Salmonella serovars isolated from broilers, as well as human salmonellosis notification data, which is useful for consideration of the circulating serovars within the chicken meat industry and their significance in public health. As there are multiple entry points for Salmonella during the entire chicken meat production chain that can lead to carcass contamination, it is important to distinguish serovars present between the different stages of vertical integration to implement and enable Salmonella control strategies.

Investigation of a Salmonella Montevideo Outbreak Related to the Environmental Contamination of a Restaurant Kitchen Drainage System, Québec, Canada, 2020-2021.

In May 2020, the Direction de santé publique du CIUSSS de la Capitale-Nationale (DSPu) received a report from the Laboratoire de santé publique du Québec of a cluster of three cases of Salmonella enterica enterica, serogroup C1, serotype Montevideo. The epidemiological investigation identified a total of 67 cases between January 1, 2020, and August 13, 2021, 66% of which were directly linked to a restaurant in the area. The Salmonella strains from most of these cases were found to be identical by whole-genome sequencing (cluster code 2005MontWGS-1QC). The initial inspection of the restaurant by the competent authorities (Ministère de l'agriculture, des pêcheries et de l'alimentation du Québec) - including the evaluation of hygiene and food safety, the search for cases of illness among workers and food sampling - was unable to establish the source of the outbreak. Environmental samples showed that the restaurant's kitchen drains were contaminated with the same strain of Salmonella Montevideo as the cases in the outbreak. Several cleaning and disinfection methods were used repeatedly. When environmental sampling at the restaurant sites was repeatedly and consecutively negative, cases in the community stopped. The prior occurrence of a fire in the kitchen may have played a role in the contamination of the restaurant drains. In conclusion, public health professionals should consider drainage systems (plumbing) and possible aerosolization of bacteria as a potential source of a restaurant-related salmonellosis outbreak.

Local Salmonella Enteritidis restaurant outbreak investigation in England provides further evidence for eggs as source in widespread international cluster, March to April 2023.

We report a 5-single nucleotide polymorphism cluster of Salmonella Enteriditis in England, part of a global cluster of S. Enteritidis ST11. Forty-seven confirmed cases have been investigated of whom 25 were linked to a restaurant. In addition, there were 18 probable cases with restaurant exposure. Epidemiological investigations suggested eggs or chicken as the most likely cause of the outbreak but were unable to distinguish between those two food vehicles. Ongoing food chain investigations indicated links to imported eggs from Poland.