Public Health Response to Multistate Salmonella Typhimurium Outbreak Associated with Prepackaged Chicken Salad, United States, 2018.

Quantifying the effect of public health actions on population health is essential when justifying sustained public health investment. Using modeling, we conservatively estimated that rapid response to a multistate foodborne outbreak of Salmonella Typhimurium in the United States in 2018 potentially averted 94 reported cases and $633,181 in medical costs and productivity losses.

An outbreak of monophasic Salmonella Typhimurium associated with raw pork sausage and other pork products, Denmark 2018-19.

In Denmark, outbreaks of salmonella with more than 20 cases have become rare. In November 2018, an outbreak of monophasic Salmonella Typhimurium was detected and an investigation initiated with the aim of identifying the source and controlling the outbreak. Outbreak cases were defined based on core genome multilocus sequence types. We conducted hypothesis-generating interviews, a matched case-control study, food sampling and trace-back investigations. We identified 49 cases distributed across Denmark. In univariable analyses a traditional form of raw Danish pork sausage (medister sausage), pork chops and ground veal/pork showed matched odds ratio of 26 (95% CI 3-207), 4 (95% CI 1-13) and 4 (95% CI 1-10), respectively. In a multivariable analysis, only medister sausage remained significant. Several patients described tasting or eating the sausage raw or undercooked. Samples of medister sausage analysed were negative for salmonella and investigations at the production site did not reveal the mechanism of contamination. In conclusion, in spite of having eliminated salmonella in the egg and broiler industry, Denmark is still at risk of major salmonella outbreaks. We identified a raw pork sausage as a particular risk product that needs to be thoroughly cooked before consumption. Tasting raw meat or eating undercooked pork should be discouraged.

New product, old problem(s): multistate outbreak of Salmonella Paratyphi B variant L(+) tartrate(+) infections linked to raw sprouted nut butters, October 2015.

A cluster of Salmonella Paratyphi B variant L(+) tartrate(+) infections with indistinguishable pulsed-field gel electrophoresis patterns was detected in October 2015. Interviews initially identified nut butters, kale, kombucha, chia seeds and nutrition bars as common exposures. Epidemiologic, environmental and traceback investigations were conducted. Thirteen ill people infected with the outbreak strain were identified in 10 states with illness onset during 18 July-22 November 2015. Eight of 10 (80%) ill people reported eating Brand A raw sprouted nut butters. Brand A conducted a voluntary recall. Raw sprouted nut butters are a novel outbreak vehicle, though contaminated raw nuts, nut butters and sprouted seeds have all caused outbreaks previously. Firms producing raw sprouted products, including nut butters, should consider a kill step to reduce the risk of contamination. People at greater risk for foodborne illness may wish to consider avoiding raw products containing raw sprouted ingredients.

National outbreak of Salmonella Give linked to a local food manufacturer in Malta, October 2016.

Salmonella Give is a rare serotype across Europe. In October 2016, a national outbreak of S. Give occurred in Malta. We describe the epidemiological, environmental, microbiological and veterinary investigations. Whole-genome sequencing (WGS) was performed on human, food, environmental and veterinary isolates. Thirty-six human cases were reported between October and November 2016, 10 (28%) of whom required hospitalisation. Twenty-six (72%) cases were linked to four restaurants. S. Give was isolated from ready-to-eat antipasti served by three restaurants which were all supplied by the same local food manufacturer. Food-trace-back investigations identified S. Give in packaged bean dips, ham, pork and an asymptomatic food handler at the manufacturer; inspections found inadequate separation between raw and ready-to-eat food during processing. WGS indicated two genetically distinguishable strains of S. Give with two distinct clusters identified; one cluster linked to the local food manufacturer and a second linked to veterinary samples. Epidemiological, environmental and WGS evidence pointed towards cross-contamination of raw and ready-to-eat foods at the local manufacturer as the likely source of one cluster. Severity of illness indicates a high virulence of this specific serotype. To prevent future cases and outbreaks, adherence to food safety practices at manufacturing level need to be reinforced.

Risk Assessment of Salmonellosis from Consumption of Alfalfa Sprouts and Evaluation of the Public Health Impact of Sprout Seed Treatment and Spent Irrigation Water Testing.

We developed a risk assessment of human salmonellosis associated with consumption of alfalfa sprouts in the United States to evaluate the public health impact of applying treatments to seeds (0-5-log10 reduction in Salmonella) and testing spent irrigation water (SIW) during production. The risk model considered variability and uncertainty in Salmonella contamination in seeds, Salmonella growth and spread during sprout production, sprout consumption, and Salmonella dose response. Based on an estimated prevalence of 2.35% for 6.8 kg seed batches and without interventions, the model predicted 76,600 (95% confidence interval (CI) 15,400-248,000) cases/year. Risk reduction (by 5- to 7-fold) predicted from a 1-log10 seed treatment alone was comparable to SIW testing alone, and each additional 1-log10 seed treatment was predicted to provide a greater risk reduction than SIW testing. A 3-log10 or a 5-log10 seed treatment reduced the predicted cases/year to 139 (95% CI 33-448) or 1.4 (95% CI <1-4.5), respectively. Combined with SIW testing, a 3-log10 or 5-log10 seed treatment reduced the cases/year to 45 (95% CI 10-146) or <1 (95% CI <1-1.5), respectively. If the SIW coverage was less complete (i.e., less representative), a smaller risk reduction was predicted, e.g., a combined 3-log10 seed treatment and SIW testing with 20% coverage resulted in an estimated 92 (95% CI 22-298) cases/year. Analysis of alternative scenarios using different assumptions for key model inputs showed that the predicted relative risk reductions are robust. This risk assessment provides a comprehensive approach for evaluating the public health impact of various interventions in a sprout production system.

Highly suspected cases of salmonellosis in two cats fed with a commercial raw meat-based diet: health risks to animals and zoonotic implications.

BACKGROUND: Feeding raw meat-based diets (RMBD) to companion animals raises public health concerns for both animals and humans. While considerable attention has been paid to bacterial contamination of commercial pet food, few literature studies have investigated foodborne disease in companion animals. Salmonellosis is reported to be infrequent in cats but no known data or studies estimating feline salmonellosis are available or large-scale epidemiological studies assessing Salmonella risk factors. CASE PRESENTATION: Two highly suspected cases of salmonellosis in two cats fed with a commercial frozen poultry RMBD are presented, for the first time from the same household. The clinical presentation, diagnostics, treatment and follow-up are reported and the zoonotic implications are discussed. CONCLUSIONS: This case highlights the health risks posed to both animals and owners by feeding RMBD to pets, and suggests that these risks should be considered by veterinary practitioners.

Bayesian Source Attribution of Salmonellosis in South Australia.

Salmonellosis is a significant cause of foodborne gastroenteritis in Australia, and rates of illness have increased over recent years. We adopt a Bayesian source attribution model to estimate the contribution of different animal reservoirs to illness due to Salmonella spp. in South Australia between 2000 and 2010, together with 95% credible intervals (CrI). We excluded known travel associated cases and those of rare subtypes (fewer than 20 human cases or fewer than 10 isolates from included sources over the 11-year period), and the remaining 76% of cases were classified as sporadic or outbreak associated. Source-related parameters were included to allow for different handling and consumption practices. We attributed 35% (95% CrI: 20-49) of sporadic cases to chicken meat and 37% (95% CrI: 23-53) of sporadic cases to eggs. Of outbreak-related cases, 33% (95% CrI: 20-62) were attributed to chicken meat and 59% (95% CrI: 29-75) to eggs. A comparison of alternative model assumptions indicated that biases due to possible clustering of samples from sources had relatively minor effects on these estimates. Analysis of source-related parameters showed higher risk of illness from contaminated eggs than from contaminated chicken meat, suggesting that consumption and handling practices potentially play a bigger role in illness due to eggs, considering low Salmonella prevalence on eggs. Our results strengthen the evidence that eggs and chicken meat are important vehicles for salmonellosis in South Australia.

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.

Salmonella Infection in Middle-Aged and Older Adults: Incidence and Risk Factors from the 45 and Up Study.

BACKGROUND: Salmonella infection is one of the most common foodborne bacterial pathogens, and causes a significant health burden globally. We investigated the incidence and risk factors for notification and hospitalization due to Salmonella infection in older adults. MATERIALS AND METHODS: We used the 45 and Up Study, a large-scale Australian prospective study of adults aged ≥45 years, with record linkage to multiple databases for the years 2006-2012 to estimate the incidence of notification and hospitalization for Salmonella infection and estimate hazard ratios using Cox regression. RESULTS: Over a total follow-up of 1,120,242 person-years, 333 adults had laboratory-confirmed Salmonella infection and 101 were hospitalized; the notification and hospitalization incidence were 29.7 (95% confidence interval [CI]: 26.9-33.3) and 9.0 (95% CI: 7.4-10.9) per 100,000 person-years, respectively. The risk of Salmonella infection notification did not differ by age, but risk of hospitalization increased with age. Elderly males had the highest risk of infection-related hospitalization. The risk of notification was higher for those living in rural or remote areas (adjusted hazard ratio [aHR] 1.7, 95% CI 1.3-2.2), those taking proton pump inhibitors (aHR 1.9, 95% CI 1.4-2.4), and those reporting chicken/poultry intake at least seven times per week (aHR 3.2, 95% CI 1.3-7.9). CONCLUSIONS: Chicken consumption remains a significant risk factor for Salmonella infection, highlighting the importance of reducing contamination of poultry and improving food safety advice for older people.

Longitudinal Monitoring of Successive Commercial Layer Flocks for Salmonella enterica Serovar Enteritidis.

The Pennsylvania Egg Quality Assurance Program (EQAP) provided the framework for Salmonella Enteritidis (SE) control programs, including the Food and Drug Administration (FDA) mandated Final Egg Rule, for commercial layer facilities throughout the United States. Although flocks with ≥3000 birds must comply with the FDA Final Egg Rule, smaller flocks are exempted from the rule. As a result, eggs produced by small layer flocks may pose a greater public health risk than those from larger flocks. It is also unknown if the EQAPs developed with large flocks in mind are suitable for small- and medium-sized flocks. Therefore, a study was performed to evaluate the effectiveness of best management practices included in EQAPs in reducing SE contamination of small- and medium-sized flocks by longitudinal monitoring of their environment and eggs. A total of 59 medium-sized (3000 to 50,000 birds) and small-sized (<3000 birds) flocks from two major layer production states of the United States were enrolled and monitored for SE by culturing different types of environmental samples and shell eggs for two consecutive flock cycles. Isolated SE was characterized by phage typing, pulsed-field gel electrophoresis (PFGE), and clustered regularly interspaced short palindromic repeats-multi-virulence-locus sequence typing (CRISPR-MVLST). Fifty-four Salmonella isolates belonging to 17 serovars, 22 of which were SE, were isolated from multiple sample types. Typing revealed that SE isolates belonged to three phage types (PTs), three PFGE fingerprint patterns, and three CRISPR-MVLST SE Sequence Types (ESTs). The PT8 and JEGX01.0004 PFGE pattern, the most predominant SE types associated with foodborne illness in the United States, were represented by a majority (91%) of SE. Of the three ESTs observed, 85% SE were typed as EST4. The proportion of SE-positive hen house environment during flock cycle 2 was significantly less than the flock cycle 1, demonstrating that current EQAP practices were effective in reducing SE contamination of medium and small layer flocks.

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.

Risk factors associated with sporadic salmonellosis in children: a case-control study in Lower Saxony, Germany, 2008-2011.

We conducted a case-control study based on 884 laboratory-confirmed sporadic Salmonella cases reported to the German infectious disease notification system. For controls, we recruited 510 rotavirus cases via the same system. Univariable and multivariable logistic regression analyses were performed separately for children aged 0-3 years and 4-14 years. In both age groups, the highest odds ratios (OR) were found for raw ground pork consumption [0-3 years: OR 8·6, 95% confidence interval (CI) 2·4-30·8; 4-14 years: OR 4·5, 95% CI 1·1-19]. Further risk factors were exposure to animals (OR 1·6, 95% CI 1·1-2·1), consumption of poultry (OR 1·5, 95% CI 1·1-2·1), food items containing eggs (OR 1·5, 95% CI 1·1-2) and black pepper (OR 1·7, 95% CI 1·1-3·5) in children aged 0-3 years, and consumption of uncooked pork sausage (OR 3·6, 95% CI 1·4-9·3) in children aged 4-14 years. This study highlights the significance of raw pork products ('Mett' in German) as risk factors for sporadic salmonellosis in children in Germany.

Using surveillance and monitoring data of different origins in a Salmonella source attribution model: a European Union example with challenges and proposed solutions.

Microbial subtyping approaches are commonly used for source attribution of human salmonellosis. Such methods require data on Salmonella in animals and humans, outbreaks, infection abroad and amounts of food available for consumption. A source attribution model was applied to 24 European countries, requiring special data management to produce a standardized dataset. Salmonellosis data on animals and humans were obtained from datasets provided by the European Food Safety Authority. The amount of food available for consumption was calculated based on production and trade data. Limitations included different types of underreporting, non-participation in prevalence studies, and non-availability of trade data. Cases without travel information were assumed to be domestic; non-subtyped human or animal records were re-identified according to proportions observed in reference datasets; missing trade information was estimated based on previous years. The resulting dataset included data on 24 serovars in humans, broilers, laying hens, pigs and turkeys in 24 countries.

Salmonella typhimurium infections associated with peanut products.

BACKGROUND: Contaminated food ingredients can affect multiple products, each distributed through various channels and consumed in multiple settings. Beginning in November 2008, we investigated a nationwide outbreak of salmonella infections. METHODS: A case was defined as laboratory-confirmed infection with the outbreak strain of Salmonella Typhimurium occurring between September 1, 2008, and April 20, 2009. We conducted two case-control studies, product "trace-back," and environmental investigations. RESULTS: Among 714 case patients identified in 46 states, 166 (23%) were hospitalized and 9 (1%) died. In study 1, illness was associated with eating any peanut butter (matched odds ratio, 2.5; 95% confidence interval [CI], 1.3 to 5.3), peanut butter-containing products (matched odds ratio, 2.2; 95% CI, 1.1 to 4.7), and frozen chicken products (matched odds ratio, 4.6; 95% CI, 1.7 to 14.7). Investigations of focal clusters and single cases associated with nine institutions identified a single institutional brand of peanut butter (here called brand X) distributed to all facilities. In study 2, illness was associated with eating peanut butter outside the home (matched odds ratio, 3.9; 95% CI, 1.6 to 10.0) and two brands of peanut butter crackers (brand A: matched odds ratio, 17.2; 95% CI, 6.9 to 51.5; brand B: matched odds ratio, 3.6; 95% CI, 1.3 to 9.8). Both cracker brands were made from brand X peanut paste. The outbreak strain was isolated from brand X peanut butter, brand A crackers, and 15 other products. A total of 3918 peanut butter-containing products were recalled between January 10 and April 29, 2009. CONCLUSIONS: Contaminated peanut butter and peanut products caused a nationwide salmonellosis outbreak. Ingredient-driven outbreaks are challenging to detect and may lead to widespread contamination of numerous food products.

Outbreak of Salmonella infantis gastroenteritis among people who had eaten at a hash house in southern Italy.

OBJECTIVES: To describe an outbreak of acute gastroenteritis in people who had eaten at a hash house in southern Italy. STUDY DESIGN: Case-control study. METHODS: A clinical case of gastroenteritis was defined as a person who had eaten at the hash house from 29 August to 4 September 2011 and who experienced defined gastrointestinal symptoms within 72 hours, or a person with a laboratory-confirmed salmonella infection without symptoms. A convenience sample was enrolled as the control group. Environmental and human samples were collected, and Salmonella infantis was identified by polymerase chain reaction. Univariate analysis was performed for each food type, and multivariate analysis was performed for each food type and demographic variable (gender, age). RESULTS: Twenty-three cases of gastroenteritis were notified between 1 and 4 September 2011, two of which were admitted to the local hospital. Multivariate analysis showed that porchetta [odds ratio (OR) 22.0, 95% confidence interval (CI) 3.2-152.6, z = 3.13, P = 0.002] and roasted meat (OR 14.4, 95% CI 1.7-122.0, z = 2.45, P = 0.014) were associated with gastrointestinal symptoms. Environmental and human isolates exhibited the same sequence type (ST 32). CONCLUSIONS: This experience highlighted that, in the control of a foodborne outbreak, integrated epidemiological and laboratory surveillance enables rapid identification of the source of infection, thus reducing the risk of an epidemic.

Risk factors associated with sporadic salmonellosis in adults: a case-control study.

In order to identify and assess recent risk factors for sporadic human infections with Salmonella enterica, we conducted a case-control study in Lower Saxony, Germany. The data collection was based on standardized telephone interviews with 1017 cases and 346 controls aged >14 years. Odds ratios were calculated in single-factor and multi-factor analyses for Salmonella cases and two different control groups, i.e. population controls and controls with rotavirus infection. Multi-factor analysis revealed associations between sporadic Salmonella infections for two exposures by both sets of controls: consumption of raw ground pork [adjusted odds ratio (aOR) 2·38, 95% confidence interval (CI) 1·27-4·44] and foreign travel (aOR 2·12, 95% CI 1·00-4·52). Other exposures included consumption of food items containing eggs (aOR 1·43, 95% CI 0·80-2·54), consumption of chicken meat (aOR 1·77, 95% CI 1·26-2·50), outdoor meals/barbecues (aOR 3·96, 95% CI 1·41-11·12) and taking gastric acidity inhibitors (aOR 2·42, 95% CI 1·19-4·92), all were significantly associated with respect to one of the two control groups. The impact of consuming food items containing eggs or chicken meat was lower than expected from the literature. This might be a consequence of Salmonella control programmes as well as increased public awareness of eggs and chicken products being a risk factor for salmonellosis. Efforts to reduce Salmonella infections due to raw pork products should be intensified.

Nationwide outbreak of Salmonella Montevideo infections associated with contaminated imported black and red pepper: warehouse membership cards provide critical clues to identify the source.

In November 2009, we initiated a multistate investigation of Salmonella Montevideo infections with pulsed-field gel electrophoresis pattern JIXX01.0011. We identified 272 cases in 44 states with illness onset dates ranging from 1 July 2009 to 14 April 2010. To help generate hypotheses, warehouse store membership card information was collected to identify products consumed by cases. These records identified 19 ill persons who purchased company A salami products before onset of illness. A case-control study was conducted. Ready-to-eat salami consumption was significantly associated with illness (matched odds ratio 8·5, 95% confidence interval 2·1-75·9). The outbreak strain was isolated from company A salami products from an environmental sample from one manufacturing plant, and sealed containers of black and red pepper at the facility. This outbreak illustrates the importance of using membership card information to assist in identifying suspect vehicles, the potential for spices to contaminate ready-to-eat products, and preventing raw ingredient contamination of these products.

Cohort study of a dual-pathogen point source outbreak associated with the consumption of chicken liver pâté, UK, October 2009.

BACKGROUND: In October 2009, a dual-pathogen outbreak of Campylobacter and Salmonella occurred in which 59 cases were identified among guests attending a regional conference in the North of England. The mean symptomatic period was 5.4 days ( confidence intervals: 4.4-6.4), and over 84% of the cases had abdominal pain and diarrhoea. METHODS: A retrospective cohort study was used to investigate the outbreak, and active case-finding was performed through the conference organizers and environmental health officers. A focused questionnaire was distributed to all guests via the event organizers 10 days after the conference. RESULTS: Response rate among guests was 61% (107/175). A cohort study was undertaken, and a strong association was found between illness and consumption of chicken liver pâté, supporting the hypothesis that chicken liver pâté was the most likely cause of the outbreak. CONCLUSION: This is the first mixed pathogen outbreak documented associated with the consumption of chicken liver pâté and adds to the evidence of potential hazards associated with the undercooking of poultry livers. A rapid outbreak investigation with collaboration between several organizations and the venue led to identification of the most probable source.

Salmonella enterica serotype enteritidis outbreak at a long-term care facility, Connecticut, 2012.

In May of 2012, the Connecticut Department of Public Health (DPH) was notified of three hospitalized residents of a long-term care facility (LTCF) who had gastrointestinal illness, one of whom had a stool culture positive for Salmonella enterica. A multiagency outbreak investigation was initiated and identified a total of 21 possible salmonellosis cases; nine were culture-confirmed Salmonella serotype Enteritidis with an indistinguishable pulsed-field gel electrophoresis pattern (PFGE). This report describes the epidemiologic, environmental, and laboratory investigation conducted as part of DPH's response. Undercooked raw shell eggs were the likely source of infection. This investigation reemphasizes the vulnerabilityof certain populations to severe illness from Salmonella and further stresses previous recommendations in the literature to use only pasteurized egg products in long-term care and other health care facilities.

Multistate outbreak of Salmonella serotype Bovismorbificans infections associated with hummus and tahini--United States, 2011.

On September 27, 2011, three clinical isolates of Salmonella enterica serotype Bovismorbificans with indistinguishable pulsed-field gel electrophoresis (PFGE) patterns were identified by the District of Columbia Public Health Laboratory (PHL). Human infection with S. Bovismorbificans is rare in the United States. Through query of PulseNet, the national molecular subtyping network for foodborne disease surveillance, six additional cases with indistinguishable PFGE patterns were identified in three states (Maryland, Michigan, and Virginia) during the prior 60 days. All nine patients had eaten at restaurants in the District of Columbia (DC) or northern Virginia <2 weeks before illness onset. This report summarizes the investigation led by the DC Department of Health (DOH), in which 23 cases of S. Bovismorbificans infections were identified among persons from seven states and DC, with illness onset during August 19-November 21, 2011. On May 30, 2012, traceback indicated that contaminated tahini (sesame seed paste) used in hummus prepared at a Mediterranean-style restaurant in DC was a plausible source of Salmonella infections. DOH restricted the sale of hummus and prohibited the use of hummus ingredients in other food items at implicated restaurants to prevent further illness. This investigation also illustrates challenges associated with ingredient-driven outbreaks and the value of PulseNet for identifying clusters of cases that are geographically dispersed.