Salmonella Serotypes: A Novel Measure of Association with Foodborne Transmission.

Most nontyphoidal Salmonella (NTS) illnesses in the United States are thought to be foodborne. However, transmission routes likely vary among the different serotypes. We developed a relative ranking of NTS serotypes according to the strength of their association with foodborne transmission. We used Laboratory-based Enteric Disease Surveillance data to estimate the proportion of infections for each Salmonella serotype reported from 1998 to 2015 and Foodborne Disease Outbreak Surveillance System data to calculate the proportion of foodborne outbreak-associated Salmonella illnesses caused by each serotype. We calculated the ratios of these proportions to create a foodborne relatedness (FBR) measure for each serotype. Of the top 20 serotypes, Saintpaul (2.14), Heidelberg (1.61), and Berta (1.48) had the highest FBR measures; Mississippi (0.01), Bareilly (0.13), and Paratyphi B variant L(+) tartrate(+) (0.20) had the lowest. The FBRs for the three most prevalent serotypes were 1.22 for Enteritidis, 0.77 for Typhimurium, and 1.16 for Newport. This method provides a quantitative approach to estimating the relative differences in the likelihood that an illness caused by a particular serotype was transmitted by food, which may aid in tailoring strategies to prevent Salmonella illnesses and guide future research into serotype-specific source attribution.

A Farm Transmission Model for Salmonella in Pigs, Applicable to E.U. Member States.

The burden of Salmonella entering pig slaughterhouses across the European Union is considered a primary food safety concern. To assist E.U. member states with the development of national control plans, we have developed a farm transmission model applicable to all member states. It is an individual-based stochastic susceptible-infected model that takes into account four different sources of infection of pigs (sows, feed, external contaminants such as rodents, and new stock) and various management practices linked to Salmonella transmission/protection (housing, flooring, feed, all-in-all-out production). A novel development within the model is the assessment of dynamic shedding rates. The results of the model, parameterized for two case study member states (one high and one low prevalence) suggest that breeding herd prevalence is a strong indicator of slaughter pig prevalence. Until a member state's' breeding herd prevalence is brought below 10%, the sow will be the dominant source of infection to pigs raised for meat production; below this level of breeding herd prevalence, feed becomes the dominant force of infection.

An Approach to Cluster EU Member States into Groups According to Pathways of Salmonella in the Farm-to-Consumption Chain for Pork Products.

The aim of the project as the cluster analysis was to in part to develop a generic structured quantitative microbiological risk assessment (QMRA) model of human salmonellosis due to pork consumption in EU member states (MSs), and the objective of the cluster analysis was to group the EU MSs according to the relative contribution of different pathways of Salmonella in the farm-to-consumption chain of pork products. In the development of the model, by selecting a case study MS from each cluster the model was developed to represent different aspects of pig production, pork production, and consumption of pork products across EU states. The objective of the cluster analysis was to aggregate MSs into groups of countries with similar importance of different pathways of Salmonella in the farm-to-consumption chain using available, and where possible, universal register data related to the pork production and consumption in each country. Based on MS-specific information about distribution of (i) small and large farms, (ii) small and large slaughterhouses, (iii) amount of pork meat consumed, and (iv) amount of sausages consumed we used nonhierarchical and hierarchical cluster analysis to group the MSs. The cluster solutions were validated internally using statistic measures and externally by comparing the clustered MSs with an estimated human incidence of salmonellosis due to pork products in the MSs. Finally, each cluster was characterized qualitatively using the centroids of the clusters.

A Transport and Lairage Model for Salmonella Transmission Between Pigs Applicable to EU Member States.

A model for the transmission of Salmonella between finisher pigs during transport to the abattoir and subsequent lairage has been developed, including novel factors such as environmental contamination and the effect of stress, and is designed to be adaptable for any EU Member State (MS). The model forms part of a generic farm-to-consumption model for Salmonella in pigs, designed to model potentially important risk factors and assess the effectiveness of interventions. In this article, we discuss the parameterization of the model for two case study MSs. For both MSs, the model predicted an increase in the average MS-level prevalence of Salmonella-positive pigs during both transport and lairage, accounting for a large amount of the variation between reported on-farm prevalence and reported lymph-node prevalence at the slaughterhouse. Sensitivity analysis suggested that stress is the most important factor during transport, while a number of factors, including environmental contamination and the dose-response parameters, are important during lairage. There was wide variation in the model-predicted change in prevalence in individual batches; while the majority of batches (80-90%) had no increase, in some batches the increase in prevalence was over 70% and in some cases infection was introduced into previously uninfected batches of pigs. Thus, the model suggests that while the transport and lairage stages of the farm-to-consumption exposure pathway are unlikely to be responsible for a large increase in average prevalence at the MS level, they can have a large effect on prevalence at an individual-batch level.

Turtles as a Possible Reservoir of Nontyphoidal Salmonella in Shanghai, China.

Terrapins and turtles are known to transmit Salmonella to humans. However, little was known about the occurrence of this pathogen in soft-shelled terrapin that is a popular delicacy in Chinese and other East Asian cuisines. We isolated and characterized 82 (24.4%) isolates of Salmonella from 336 fecal samples of soft-shelled terrapins (51 of 172; 29.7%) and pet turtles (31 of 164; 18.9%) in Shanghai. Salmonella Thompson was the most common serotype (17.1%) among others. Many isolates (84.1%) were resistant to multiple antimicrobials (≥3). Molecular analysis of Salmonella Thompson and Salmonella Typhimurium using pulsed-field gel electrophoresis unveiled a close genetic relationship between several human and terrapin isolates. Our results highlight the risk associated with the handling and consumption of turtles and their role in the spread of Salmonella in the human salmonellosis.

Understanding the Relationships Between Inspection Results and Risk of Foodborne Illness in Restaurants.

Restaurants are important settings for foodborne disease outbreaks and consumers are increasingly using restaurant inspection results to guide decisions about where to eat. Although public posting of inspection results may lead to improved sanitary practices in the restaurant, the relationship between inspection results and risk of foodborne illness appears to be pathogen specific. To further examine the relationship between inspection results and the risk of foodborne disease outbreaks, we evaluated results of routine inspections conducted in multiple restaurants in a chain (Chain A) that was associated with a large Salmonella outbreak in Illinois. Inspection results were collected from 106 Chain A establishments in eight counties. Forty-six outbreak-associated cases were linked to 23 of these Chain A restaurants. There were no significant differences between the outbreak and nonoutbreak restaurants for overall demerit points or for the number of demerit points attributed to hand washing or cross-contamination. Our analyses strongly suggest that the outbreak resulted from consumption of a contaminated fresh produce item without further amplification within individual restaurants. Inspections at these facilities would be unlikely to detect or predict the foodborne illness outbreak because there are no Food Code items in place to stop the introduction of contaminated food from an otherwise approved commercial food source. The results of our study suggest that the agent and food item pairing and route of transmission must be taken into consideration to improve our understanding of the relationship between inspection results and the risk of foodborne illness in restaurants.

Attributing foodborne salmonellosis in humans to animal reservoirs in the European Union using a multi-country stochastic model.

A Bayesian modelling approach comparing the occurrence of Salmonella serovars in animals and humans was used to attribute salmonellosis cases to broilers, turkeys, pigs, laying hens, travel and outbreaks in 24 European Union countries. Salmonella data for animals and humans, covering the period from 2007 to 2009, were mainly obtained from studies and reports published by the European Food Safety Authority. Availability of food sources for consumption was derived from trade and production data from the European Statistical Office. Results showed layers as the most important reservoir of human salmonellosis in Europe, with 42·4% (7 903 000 cases, 95% credibility interval 4 181 000-14 510 000) of cases, 95·9% of which was caused by S. Enteritidis. In Finland and Sweden, most cases were travel-related, while in most other countries the main sources were related to the laying hen or pig reservoir, highlighting differences in the epidemiology of Salmonella, surveillance focus and eating habits across the European Union.

Event-based surveillance of food- and waterborne diseases in Europe: urgent inquiries (outbreak alerts) during 2008 to 2013.

During 2008 to 2013, 215 outbreak alerts, also known as 'urgent inquiries' (UI), for food- and waterborne diseases were launched in Europe, the majority of them (135; 63%) being related to salmonellosis. For 110 (51%) UI, a potential food vehicle of infection was identified, with vegetables being the most reported category (34;31%). A total of 28% (n = 60) of the outbreaks reported had an international dimension, involving at least two countries (mean: 4; standard deviation: 2; range:2­14). Participating countries posted 2,343 messages(initial posts and replies, excluding updates), with a median of 11 messages per urgent inquiry (range:1­28). Of 60 multicountry UI, 50 involved between two and four countries. The UI allowed early detection of multicountry outbreaks, facilitated the identification of the suspected vehicles and consequently contributed to the timely implementation of control measures. The introduction of an epidemic intelligence information system platform in 2010 has strengthened the role of the Food- and Waterborne Diseases and Zoonoses network in facilitating timely exchange of information between public health authorities of the participating countries.

Human outbreak of Salmonella Typhimurium associated with exposure to locally made chicken jerky pet treats, New Hampshire, 2013.

Pet treats and pet food can be contaminated with Salmonella and other pathogens, though they are infrequently implicated as the source of human outbreaks. In 2013, the New Hampshire Department of Health and Human Services investigated a cluster of Salmonella Typhimurium infections associated with contaminated locally made pet treats. Case-patients were interviewed with standardized questionnaires to assess food, animal, and social histories. Laboratory and environmental investigations were conducted, including testing of clinical specimens, implicated product, and environmental swabs. Between June and October 2013, a total of 43 ill persons were identified. Sixteen patients (37%) were hospitalized. Among 43 case-patients interviewed, the proportion exposed to dogs (95%) and pet treats (69%) in the 7 days prior to illness was statistically higher than among participants in a U.S. population-based telephone survey (61%, p<0.0001 and 16%, p<0.0001, respectively). On further interview, 38 (88%) reported exposure to Brand X Chicken Jerky, the maker of Brand X chicken jerky, or the facility in which it was made. Product testing isolated the outbreak strain from four of four Brand X Chicken Jerky samples, including an unopened package purchased at retail, opened packages collected from patient households, and unpackaged jerky obtained from the jerky maker. A site visit revealed inadequate processing of the chicken jerky, bare-hand contact with the finished product prior to packaging, and use of vacuum-sealed packaging, which may have enabled facultative anaerobic bacteria to proliferate. Seven (78%) of nine environmental swabs taken during the site visit also yielded the outbreak strain. Brand X Chicken Jerky was voluntarily recalled on September 9, 2013. Consumers should be made aware of the potential for locally made products to be exempt from regulation and for animals and animal food to carry pathogens that cause human illness, and be educated to perform hand hygiene after handling pet food or treats.

Multidrug-Resistant Salmonella Heidelberg Associated with Mechanically Separated Chicken at a Correctional Facility.

We describe multidrug-resistant (MDR) Salmonella Heidelberg infections associated with mechanically separated chicken (MSC) served at a county correctional facility. Twenty-three inmates met the case definition. All reported diarrhea, 19 (83%) reported fever, 16 (70%) reported vomiting, 4 (17%) had fever ≥103°F, and 3 (13%) were hospitalized. A case-control study found no single food item significantly associated with illness. Salmonella Heidelberg with an indistinguishable pulsed-field gel electrophoresis pattern was isolated from nine stool specimens; two isolates displayed resistance to a total of five drug classes, including the third-generation cephalosporin, ceftriaxone. MDR Salmonella Heidelberg might have contributed to the severity of illness. Salmonella Heidelberg indistinguishable from the outbreak subtype was isolated from unopened MSC. The environmental health assessment identified cross-contamination through poor food-handling practices as a possible contributing factor. Proper hand-washing techniques and safe food-handling practices were reviewed with the kitchen supervisor.

Salmonella Prevalence and Antimicrobial Susceptibility from the National Animal Health Monitoring System Sheep 2011 Study.

Salmonella is a major cause of foodborne illness and can cause clinical disease in animals. Understanding the on-farm ecology of Salmonella will be helpful in decreasing the risk of foodborne transmission. An objective of this study was to determine the prevalence of Salmonella among fecal samples collected on sheep operations in the United States. Another objective was to compare the use of composite fecal samples with fecal samples collected from individual sheep as a tool for screening sheep flocks for Salmonella. Sheep fecal samples (individual and composite) were collected on operations in 22 states. Salmonella isolates were characterized with regard to species, serotype, and antimicrobial susceptibility profile. Most operations (72.1%) had at least one positive sample and overall 26.9% of samples were positive. The percentage of positive samples varied by animal age class. Composite and individual samples gave similar results. The majority of the isolates (94%) were Salmonella enterica subspecies diarizonae serotype 61:-:1,5,7. Nearly all of the isolates (91.2%) tested for antimicrobial susceptibility were susceptible to all antimicrobials in the panel. The findings suggest that salmonellae typically associated with foodborne disease transmission are infrequently found on sheep operations in the United States.

Multiple-serotype salmonella outbreaks in two state prisons--Arkansas, August 2012.

In August 2012, the Arkansas Department of Health (ADH) was notified of gastrointestinal illness outbreaks in two Arkansas state prisons. ADH investigated the outbreaks and conducted case-control studies to identify the source of the illnesses. This report describes the results of these investigations, which identified 528 persons with onset of diarrhea during August 2-18, 2012. Results from the prison A investigation identified chicken salad as the most likely vehicle. At prison B, person-to-person transmission and contamination of multiple foods likely contributed to illness. Analysis of stool specimens from inmates identified eight serotypes and 15 pulsed-field gel electrophoresis (PFGE) patterns of Salmonella. Isolates of Salmonella from eggs produced at prison B matched two outbreak patterns. An additional 69 inmates were positive by culture but were not interviewed or did not report diarrhea, making the total case count 597. Sanitarians identified problems with food preparation, hand washing, and food safety training. ADH tested inmate kitchen workers, excluded infected inmates from work, and provided food safety training. Prison kitchen staff should follow guidelines consistent with state regulations for safe food preparation and pass sanitarian inspection.

Source attribution of human salmonellosis: an overview of methods and estimates.

Reducing the burden of foodborne salmonellosis is challenging. It requires identification of the most important food sources causing disease and prioritization of effective intervention strategies. For this purpose, a variety of methods to estimate the relative contribution of different sources of Salmonella infections have been applied worldwide. Each has strengths and limitations, and the usefulness of each depends on the public health questions being addressed. In this study, we reviewed the source attribution methods and outcomes of several studies developed in different countries and settings, comparing approaches and regional differences in attribution estimates. Reviewed results suggest that illnesses and outbreaks are most commonly attributed to exposure to contaminated food, and that eggs, broiler chickens, and pigs are among the top sources. Although most source attribution studies do not attribute salmonellosis to produce, outbreak data in several countries suggest that exposure to raw vegetables is also an important source. International travel was also a consistently important exposure in several studies. Still, the relative contribution of specific sources to human salmonellosis varied substantially between studies. Although differences in data inputs, methods, and the point in the food system where attribution was estimated contribute to variability between studies, observed differences also suggest regional differences in the epidemiology of salmonellosis.

A community outbreak of Salmonella enterica serotype Typhimurium associated with an asymptomatic food handler in two local restaurants.

Between January and April 2012, the city of Long Beach Department of Health and Human Services investigated an outbreak involving 19 case patients who had tested positive for Salmonella enterica serotype Typhimurium with indistinguishable pulsed-field gel electrophoresis patterns. All cases were residents of or traveled to the city of Long Beach, California, during their incubation period, and the majority of patients reported eating at one of two restaurants in Long Beach. This article describes the outbreak investigation that traced the source to an asymptomatic food handler working at both restaurants and highlights the importance of maintaining a high index of suspicion for food handlers when faced with local outbreaks of diarrheal illness.

Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States.

Implemented in 2009, the National Outbreak Reporting System provides surveillance for acute gastroenteritis outbreaks in the United States resulting from any transmission mode. Data from the first 2 years of surveillance highlight the predominant role of norovirus. The pathogen-specific transmission pathways and exposure settings identified can help inform prevention efforts.

Investigation and management of an outbreak of Salmonella Typhimurium DT8 associated with duck eggs, Ireland 2009 to 2011.

Salmonella Typhimurium DT8 was a very rare cause of human illness in Ireland between 2000 and 2008, with only four human isolates from three patients being identified. Over a 19-month period between August 2009 and February 2011, 34 confirmed cases and one probable case of Salmonella Typhimurium DT8 were detected, all of which had an MLVA pattern 2-10-NA-12-212 or a closely related pattern. The epidemiological investigations strongly supported a linkbetween illness and exposure to duck eggs. Moreover, S. Typhimurium with an MLVA pattern indistinguishable (or closely related) to the isolates from human cases, was identified in 22 commercial and backyard duck flocks, twelve of which were linked with known human cases. A range of control measures were taken at farm level, and advice was provided to consumers on the hygienic handling and cooking of duck eggs. Although no definitive link was established with a concurrent duck egg-related outbreak of S. Typhimurium DT8 in the United Kingdom, it seems likely that the two events were related. It may be appropriate for other countries with a tradition of consuming duck eggs to consider the need for measures to reduce the risk of similar outbreaks.

A review of nosocomial Salmonella outbreaks: infection control interventions found effective.

OBJECTIVE: To review nosocomial salmonellosis outbreaks to identify: mode of transmission; morbidity and mortality patterns; and recommendations for control and prevention. DESIGN: Documented nosocomial salmonellosis outbreaks in hospitals published from January 1995 to November 2011, written in the English language, were systematically reviewed. METHODS: The study methodology incorporated steps from the PRISMA statement for a high quality review process. Computer-aided searches of Scopus, CAB Global Health and CINAHL(®), the Cumulative Index to Nursing and Allied Health Literature were completed to identify relevant outbreak reports written in English. To validate the electronic search methodology, bibliographies and reference lists of relevant review articles were hand-searched. Public health and government websites were searched for nosocomial salmonellosis. RESULTS: Fifty-two relevant reports were identified. The most frequently reported routes of transmission were food 31/52 (59.6%) and person-to-person transmission 7/52 (13.5%). Actions taken during the outbreak to control transmission included improvements to: 1) infection control practices (41.8% of actions); isolation or cohorting patients, hand hygiene practices, and enhancing cleaning and disinfection in patient care areas; and 2) food handling practices (24.4% of actions); reviewing food preparation practices, enhancing cleaning and sanitation of the kitchen, and controlling food temperatures. Investigators made recommendations retrospectively in outbreak reports to provide direction to health centees but these recommendations were not statistically evaluated for effectiveness. CONCLUSIONS: More emphasis should be placed on improving food handling practices, such as training food workers, monitoring food temperatures, and not using raw foods of animal origin, to prevent nosocomial salmonellosis outbreaks in hospitals because almost 60% of the outbreaks were foodborne.

Nationwide outbreak of Salmonella enterica serotype 4,[5],12:i:- infection associated with consumption of dried pork sausage, France, November to December 2011.

An outbreak of the monophasic variant of Salmonella enterica serotype 4,[5],12:i:- occurred in November and December 2011 in France. Epidemiological investigation and food investigation with the help of supermarket loyalty cards suggested dried pork sausage from one producer as the most likely source of the outbreak. Despite the absence of positive food samples, control measures including withdrawal and recall were implemented.

[Microbiological evaluation of chicken meal "shaverma" as a factor for Salmonella transmission].

It has been established that the dish shawarma may be a factor for Salmonella transmission, by involving in sporadic and outbreak cases of Salmonella infection. Chicken fillet grilling when cooking the dish shawarma has been found to ensure its guaranteed freedom from Salmonella only in a piece less than 2 cm thick. Deeper layers of chicken and its juice that accumulates in the grill tray may remain be Salmonella-contaminated throughout the heat treatment. Obviously, for the epidemiological safety of the dish shawarma, it is necessary to cut a not more than 2-cm piece of fillet every time the latter is ready-made, i.e. a white color and a clear juice are produced. At the time one should not use the chicken juice as sauce to the ready-made fillet and to gather and crumble the latter in a separate container rather than in the tray.

A national outbreak of Salmonella serotype Tennessee infections from contaminated peanut butter: a new food vehicle for salmonellosis in the United States.

BACKGROUND: Salmonella serotype Tennessee is a rare cause of the estimated 1 million cases of salmonellosis occurring annually in the United States. In January 2007, we began investigating a nationwide increase in Salmonella Tennessee infections. METHODS: We defined a case as Salmonella Tennessee infection in a patient whose isolate demonstrated 1 of 3 closely related pulsed-field gel electrophoresis patterns and whose illness began during the period 1 August 2006 through 31 July 2007. We conducted a case-control study in 22 states and performed laboratory testing of foods and environmental samples. RESULTS: We identified 715 cases in 48 states; 37% of isolates were from urine specimens. Illness was associated with consuming peanut butter more than once a week (matched odds ratio [mOR], 3.5 [95% confidence interval {95% CI}, 1.4-9.9]), consuming Brand X peanut butter (mOR, 12.1 [95% CI, 3.6-66.3]), and consuming Brand Y peanut butter (mOR, 9.1 [95% CI, 1.0-433]). Brands X and Y were produced in 1 plant, which ceased production and recalled products on 14 February 2007. Laboratories isolated outbreak strains of Salmonella Tennessee from 34 Brands X and Y peanut butter jars and 2 plant environmental samples. CONCLUSIONS: This large, widespread outbreak of salmonellosis is the first linked to peanut butter in the United States; a nationwide recall resulted in outbreak control. Environmental contamination in the peanut butter plant likely caused this outbreak. This outbreak highlights the risk of salmonellosis from heat-processed foods of nonanimal origin previously felt to be low risk for Salmonella contamination.