Salmonella Outbreaks Associated with Not Ready-to-Eat Breaded, Stuffed Chicken Products - United States, 1998-2022.

Not ready-to-eat (NRTE) breaded, stuffed chicken products (e.g., chicken stuffed with broccoli and cheese) typically have a crispy, browned exterior that can make them appear cooked. These products have been repeatedly linked to U.S. salmonellosis outbreaks, despite changes to packaging initiated in 2006 to identify the products as raw and warn against preparing them in a microwave oven (microwave) (1-4). On April 28, 2023, the U.S. Department of Agriculture proposed to declare Salmonella an adulterant* at levels of one colony forming unit per gram or higher in these products (5). Salmonella outbreaks associated with NRTE breaded, stuffed chicken products during 1998-2022 were summarized using reports in CDC's Foodborne Disease Outbreak Surveillance System (FDOSS), outbreak questionnaires, web postings, and data from the Minnesota Department of Health (MDH)† and the U.S. Department of Agriculture's Food Safety and Inspection Service (FSIS). Eleven outbreaks were identified in FDOSS. Among cultured samples from products obtained from patients' homes and from retail stores during 10 outbreaks, a median of 57% of cultures per outbreak yielded Salmonella. The NRTE breaded, stuffed chicken products were produced in at least three establishments.§ In the seven most recent outbreaks, 0%-75% of ill respondents reported cooking the product in a microwave and reported that they thought the product was sold fully cooked or did not know whether it was sold raw or fully cooked. Outbreaks associated with these products have occurred despite changes to product labels that better inform consumers that the products are raw and provide instructions on safe preparation, indicating that consumer-targeted interventions are not sufficient. Additional Salmonella controls at the manufacturer level to reduce contamination in ingredients might reduce illnesses attributable to NRTE breaded, stuffed chicken products.

Risk Factors for Non-O157 Shiga Toxin-Producing Escherichia coli Infections, United States.

Shiga toxin-producing Escherichia coli (STEC) causes acute diarrheal illness. To determine risk factors for non-O157 STEC infection, we enrolled 939 patients and 2,464 healthy controls in a case-control study conducted in 10 US sites. The highest population-attributable fractions for domestically acquired infections were for eating lettuce (39%), tomatoes (21%), or at a fast-food restaurant (23%). Exposures with 10%-19% population attributable fractions included eating at a table service restaurant, eating watermelon, eating chicken, pork, beef, or iceberg lettuce prepared in a restaurant, eating exotic fruit, taking acid-reducing medication, and living or working on or visiting a farm. Significant exposures with high individual-level risk (odds ratio >10) among those >1 year of age who did not travel internationally were all from farm animal environments. To markedly decrease the number of STEC-related illnesses, prevention measures should focus on decreasing contamination of produce and improving the safety of foods prepared in restaurants.

Use of Online Consumer Complaint Forms to Enhance Complaint-Based Surveillance for Foodborne Illness Outbreaks in Minnesota.

Foodborne illness complaint systems that collect consumer reports of illness following exposure at a food establishment or event are a primary tool for detecting outbreaks of foodborne illness. Approximately, 75% of outbreaks reported to the national Foodborne Disease Outbreak Surveillance System are detected through foodborne illness complaints. The Minnesota Department of Health added an online complaint form to their existing statewide foodborne illness complaint system in 2017. During 2018-2021, online complainants tended to be younger than those who used traditional telephone hotlines (mean age 39 vs 46 years; p value < 0.0001), reported illnesses sooner following onset of symptoms (mean interval 2.9 vs 4.2 days; p value = 0.003), and were more likely to still be ill at the time of the complaint (69% vs 44%; p value < 0.0001). However, online complainants were less likely to have called the suspected establishment to report their illness than those who used traditional telephone hotlines (18% vs 48%; p value < 0.0001). Of the 99 outbreaks identified by the complaint system, 67 (68%) were identified through telephone complaints alone, 20 (20%) through online complaints alone, 11 (11%) using a combination of both, and 1 (1%) through email alone. Norovirus was the most common outbreak etiology identified by both complaint system methods, accounting for 66% of outbreaks identified only via telephone complaints and 80% of outbreaks identified only via online complaints. Due to the COVID-19 pandemic in 2020, there was a 59% reduction in telephone complaint volume compared to 2019. In contrast, online complaints experienced a 25% reduction in volume. In 2021, the online method became the most popular complaint method. Although most outbreaks detected by complaints were reported by telephone complaints alone, adding an online form for complaint reporting increased the number of outbreaks detected.

Cronobacter sakazakii Infections in Two Infants Linked to Powdered Infant Formula and Breast Pump Equipment - United States, 2021 and 2022.

Cronobacter sakazakii, a species of gram-negative bacteria belonging to the Enterobacteriaceae family, is known to cause severe and often fatal meningitis and sepsis in young infants. C. sakazakii is ubiquitous in the environment, and most reported infant cases have been attributed to contaminated powdered infant formula (powdered formula) or breast milk that was expressed using contaminated breast pump equipment (1-3). Previous investigations of cases and outbreaks have identified C. sakazakii in opened powdered formula, breast pump parts, environmental surfaces in the home, and, rarely, in unopened powdered formula and formula manufacturing facilities (2,4-6). This report describes two infants with C. sakazakii meningitis reported to CDC in September 2021 and February 2022. CDC used whole genome sequencing (WGS) analysis to link one case to contaminated opened powdered formula from the patient's home and the other to contaminated breast pump equipment. These cases highlight the importance of expanding awareness about C. sakazakii infections in infants, safe preparation and storage of powdered formula, proper cleaning and sanitizing of breast pump equipment, and using WGS as a tool for C. sakazakii investigations.

Differences in risk factors for transmission among Shiga toxin-producing Escherichia coli serogroups and stx profiles.

OBJECTIVES: Trends in the incidence of O157 and non-O157 serogroups of Shiga toxin-producing Escherichia coli (STEC) infections have markedly diverged. Here, we estimate the extent to which STEC serogroups share the same transmission routes and risk factors, potentially explaining these trends. METHODS: With 3048 STEC cases reported in Minnesota from 2010 to 2019, we used lasso penalized regression to estimate pooled odds ratios (pOR) for the association between STEC risk factors and specific STEC serogroups and Shiga toxin gene profiles. We used random forests as a confirmatory analysis. RESULTS: Across an extended period of time, we found evidence for person-to-person transmission associated with the O26 serogroup, relative to other serogroups (pOR = 1.32 for contact with an individual with diarrhea). Rurality was less associated with non-O157 serogroups than O157 (pOR = 1.21 for each increasing level of rurality). We also found an association between unpasteurized juice and strains carrying only stx1 (pOR = 1.41). CONCLUSIONS: Collectively, these results show differences in risk factors across STEC types, which suggest differences in the most effective routes of transmission. Serogroup-specific disease control strategies should be explored. Specifically, preventative measures for non-O157 STEC need to extend beyond those we have employed for O157 STEC.

Transmission of and Infection With COVID-19 Among Vaccinated and Unvaccinated Attendees of an Indoor Wedding Reception in Minnesota.

Importance: Characterizing rates of SARS-CoV-2 infection among vaccinated and unvaccinated persons with the same exposure is critical to understanding the association of vaccination with the risk of infection with the Delta variant. Additionally, evidence of Delta variant transmission by children to vaccinated adults has important public health implications. Objective: To characterize transmission and infection of SARS-CoV-2 among vaccinated and unvaccinated attendees of an indoor wedding reception. Design, Setting, and Participants: This cohort study included attendees at an indoor wedding reception in Minnesota in July 2021. Data were collected from REDCap surveys and routine surveillance interviews. The full list of attendees and a partial list of emails were obtained. Fifty-seven attendees completed the emailed survey. Eighteen additional attendees were identified from the state health department COVID-19 surveillance database. Exposures: Attendance at an indoor event. Main Outcomes and Measures: Risk of SARS-CoV-2 infection among vaccinated and unvaccinated attendees, identification of an index case, whole genome sequencing (WGS) to identify the COVID-19 variant, understanding of transmission patterns, and assessment of secondary transmission. The primary case definition was an individual with a positive SARS-CoV-2 test who attended the wedding in the 14 days prior to their illness. Results: Data were gathered for 75 attendees (mean [SE] age, 37.5 [13.7] years; 57 [76%] female individuals), of whom 56 (75%) were fully vaccinated, 4 (5%) were partially vaccinated, and 15 (20%) were unvaccinated. Of 62 attendees who were tested, 29 (47%) tested positive, including 16 of 46 fully vaccinated attendees (35%), 2 of 4 partially vaccinated attendees (50%), and 11 of 12 unvaccinated attendees (92%). Being unvaccinated was associated with a higher risk of infection compared with being vaccinated (risk ratio, 2.64; 95% CI, 1.71-4.06; P = .001). One unvaccinated adult required hospitalization. An unvaccinated child who was symptomatic on the event date was identified as the index case. Eleven specimens were available for WGS. All sequenced specimens were closely related and were identified as the Delta variant. WGS supported secondary transmission from a vaccinated individual with SARS-CoV-2. Conclusions and Relevance: This cohort study identified a COVID-19 Delta variant outbreak at an indoor event despite a high proportion of vaccinated attendees. It found that vaccination was associated with a reduced risk of infection.

COVID-19 Outbreak Associated With a Fitness Center-Minnesota, September-November 2020.

The Minnesota Department of Health investigated a coronavirus disease 2019 (COVID-19) outbreak at a fitness center in Olmsted County, Minnesota. Twenty-three severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections (5 employees and 18 members) were identified. An epidemiological investigation supported by whole genome sequencing demonstrated that transmission of SARS-CoV-2 occurred at the fitness center despite following recommended prevention strategies.

Evidence of False Positivity for Vibrio Species Tested by Gastrointestinal Multiplex PCR Panels, Minnesota, 2016-2018.

BACKGROUND: Syndromic gastrointestinal multiplex polymerase chain reaction (PCR) panels (GMPPs) are used by an increasing number of clinical laboratories to identify enteric pathogens. Vibrio species are included on GMPPs, but because of the low prevalence of vibriosis, performance characteristics for these panels have been difficult to measure. METHODS: All Vibrio spp. cases identified by GMPPs in Minnesota during 2016-2018 (n = 100) were assessed to identify differences between culture-confirmed cases and those that were PCR-positive only. RESULTS: Overall, 47% of cases had Vibrio species recovered by culture. Two GMPPs were used in Minnesota, Verigene EPT and FilmArray GIP, and the recovery rate of Vibrio spp. was significantly different between these platforms (Verigene EPT 63%, compared with FilmArray GIP 28%). No distinct seasonality was identified among GMPP-positive, culture-negative cases, whereas culture-confirmed case incidence peaked during July and August. Among cases with no other pathogen detected by the GMPP, confirmed cases reported a lower rate of bloody diarrhea (odds ratio [OR], 0.7; P = .004) and were less likely to have a symptom duration >14 days (OR, 0.3; P = .04). Confirmed cases were also more likely to include reports of consuming food items typically associated with Vibrio spp. infection or to have another likely source of infection (eg, international travel or contact with an untreated body of fresh or salt water or marine life; OR, 9.6; P = .001). CONCLUSIONS: The combined findings indicate that cases identified by GMPP that did not have culture confirmation were less likely to include symptoms or exposures consistent with vibriosis. These findings emphasize the need for improvements to testing platform specificity and the importance of combining clinical and exposure information when diagnosing an infection. This study underscores the importance of maintaining the ability to culture Vibrio species to aid in accurate diagnoses.

Transmission Dynamics of Severe Acute Respiratory Syndrome Coronavirus 2 in High-Density Settings, Minnesota, USA, March-June 2020.

Coronavirus disease has disproportionately affected persons in congregate settings and high-density workplaces. To determine more about the transmission patterns of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in these settings, we performed whole-genome sequencing and phylogenetic analysis on 319 (14.4%) samples from 2,222 SARS-CoV-2-positive persons associated with 8 outbreaks in Minnesota, USA, during March-June 2020. Sequencing indicated that virus spread in 3 long-term care facilities and 2 correctional facilities was associated with a single genetic sequence and that in a fourth long-term care facility, outbreak cases were associated with 2 distinct sequences. In contrast, cases associated with outbreaks in 2 meat-processing plants were associated with multiple SARS-CoV-2 sequences. These results suggest that a single introduction of SARS-CoV-2 into a facility can result in a widespread outbreak. Early identification and cohorting (segregating) of virus-positive persons in these settings, along with continued vigilance with infection prevention and control measures, is imperative.

Hypothesis Generation During Foodborne-Illness Outbreak Investigations.

Hypothesis generation is a critical, but challenging, step in a foodborne outbreak investigation. The pathogens that contaminate food have many diverse reservoirs, resulting in seemingly limitless potential vehicles. Identifying a vehicle is particularly challenging for clusters detected through national pathogen-specific surveillance, because cases can be geographically dispersed and lack an obvious epidemiologic link. Moreover, state and local health departments could have limited resources to dedicate to cluster and outbreak investigations. These challenges underscore the importance of hypothesis generation during an outbreak investigation. In this review, we present a framework for hypothesis generation focusing on 3 primary sources of information, typically used in combination: 1) known sources of the pathogen causing illness; 2) person, place, and time characteristics of cases associated with the outbreak (descriptive data); and 3) case exposure assessment. Hypothesis generation can narrow the list of potential food vehicles and focus subsequent epidemiologic, laboratory, environmental, and traceback efforts, ensuring that time and resources are used more efficiently and increasing the likelihood of rapidly and conclusively implicating the contaminated food vehicle.

COVID-19 Outbreak Associated with a 10-Day Motorcycle Rally in a Neighboring State - Minnesota, August-September 2020.

During August 7-16, 2020, a motorcycle rally was held in western South Dakota that attracted approximately 460,000 persons from across the United States to numerous indoor and outdoor events over a 10-day period. During August-September 2020, the Minnesota Department of Health (MDH) investigated a coronavirus disease 2019 (COVID-19) outbreak associated with the rally in Minnesota residents. Fifty-one primary event-associated cases were identified, and 35 secondary or tertiary cases occurred among household, social, and workplace contacts, for a total of 86 cases; four patients were hospitalized, and one died. Approximately one third (34%) of 87 counties in Minnesota had at least one primary, secondary, or tertiary case associated with this rally. Genomic sequencing supported the associations with the motorcycle rally. These findings support current recommendations for mask use, physical distancing, reducing the number of attendees at gatherings, isolation for patients with COVID-19, and quarantine for close contacts to slow the spread of SARS-CoV-2 (1). Furthermore, although these findings did not capture the impact of the motorcycle rally on residents of other states, they demonstrate the rationale for consistent mitigation measures across states.

Can Aggregated Restaurant Inspection Data Help Us Understand Why Individual Foodborne Illness Outbreaks Occur?

ABSTRACT: Restaurant inspections seek to identify and correct risk factors for foodborne illness, but restaurant inspection data are not typically used more broadly as a food safety surveillance tool. In 2015, there was an outbreak of Salmonella serotype Newport infections associated with multiple restaurants in a chain (chain A), primarily in Minnesota. The outbreak was associated with tomatoes that were likely contaminated at the point of production. The objective of this study was to demonstrate the potential usefulness of aggregated restaurant inspection data in aiding individual outbreak investigations. Reports of the last inspection for all chain A restaurants that preceded the first reported case meal date in the outbreak were obtained from local health departments and the Minnesota Department of Health. Ordinal logistic regression was used to assess differences in risk factor and good retail practice violation categories and specific violations in restaurants with zero cases (nonoutbreak restaurants) (n = 25), one to two cases (n = 16), and at least three cases (n = 13). For restaurants with a "protection from contamination" violation in the routine inspection that preceded the outbreak, the proportional odds ratio for outbreak level was 4.92 (95% confidence interval: 1.57, 15.39; P = 0.01). These findings suggest that food handling practices in the outbreak restaurants may have increased contamination of foods through cross-contamination, which in turn increased transmission at outbreak restaurants. These data suggest that aggregated data from routine inspection reports can provide useful information to aid in outbreak investigations and other foodborne illness surveillance and prevention activities.

High Relative Frequency of Enteroaggregative Escherichia coli Among Patients With Reportable Enteric Pathogens, Minnesota, 2016-2017.

BACKGROUND: Enteroaggregative Escherichia coli (EAEC) is increasingly recognized as an enteric pathogen as clinical laboratories transition to culture-independent diagnostic tests that detect EAEC. To date, epidemiological studies have focused on children aged <5 years, and information on EAEC incidence, illness outcomes, and transmission avenues is limited. METHODS: Enteric disease surveillance data in Minnesota were used to describe EAEC illnesses reported to the Minnesota Department of Health from September 2016 through August 2017. We determined laboratory characteristics of EAEC using pulsed-field gel electrophoresis and next-generation sequencing. Frequency of EAEC illness, demographic profile of cases, clinical characteristics of illness, and plausible food or environmental exposures leading to EAEC transmission were assessed. RESULTS: During the study period, 329 EAEC cases were reported. Among a subset of health systems able to detect EAEC over the entire study, EAEC was the second most common reportable enteric pathogen detected after Campylobacter and the most detected diarrheagenic E. coli pathotype. No other reportable enteric pathogens were detected among 75.3% of EAEC cases, and 68% of cases reported no international travel before onset. Several virulence genes were associated with clinical characteristics. CONCLUSIONS: We provide evidence that EAEC is a likely causative agent of diarrheal illness in the United States. Our study contributes to criteria development for identification of pathogenic EAEC and proposes potential exposure avenues.

Outbreak of Salmonella Oslo Infections Linked to Persian Cucumbers - United States, 2016.

In April 2016, PulseNet, the national molecular subtyping network for foodborne disease surveillance, detected a multistate cluster of Salmonella enterica serotype Oslo infections with an indistinguishable pulsed-field gel electrophoresis (PFGE) pattern (XbaI PFGE pattern OSLX01.0090).* This PFGE pattern was new in the database; no previous infections or outbreaks have been identified. CDC, state and local health and agriculture departments and laboratories, and the Food and Drug Administration (FDA) conducted epidemiologic, traceback, and laboratory investigations to identify the source of this outbreak. A total of 14 patients in eight states were identified, with illness onsets occurring during March 21-April 9, 2016. Whole genome sequencing, a highly discriminating subtyping method, was used to further characterize PFGE pattern OSLX01.0090 isolates. Epidemiologic evidence indicates Persian cucumbers as the source of Salmonella Oslo infections in this outbreak. This is the fourth identified multistate outbreak of salmonellosis associated with cucumbers since 2013. Further research is needed to understand the mechanism and factors that contribute to contamination of cucumbers during growth, harvesting, and processing to prevent future outbreaks.

Long-Term Sentinel Surveillance for Enterotoxigenic Escherichia coli and Non-O157 Shiga Toxin-Producing E. coli in Minnesota.

Background. Enterotoxigenic Escherichia coli (ETEC) and non-O157 Shiga toxin-producing E. coli (STEC) are not detected by conventional culture methods. The prevalence of ETEC infections in the United States is unknown, and recognized cases are primarily associated with foreign travel. Gaps remain in our understanding of STEC epidemiology. Methods. Two sentinel surveillance sites were enrolled: an urban health maintenance organization laboratory (Laboratory A) and a rural hospital laboratory (Laboratory B). Residual sorbitol MacConkey (SMAC) plates from stool cultures performed at Laboratory A (1996-2006) and Laboratory B (2000-2008) were collected. Colony sweeps from SMAC plates were tested for genes encoding STEC toxins stx1 and stx2 (1996-2008) and ETEC heat-labile and heat-stable toxins eltB, estA 1, 2 and 3 (2000-2008) by polymerase chain reaction (PCR)-based assays. Results. In Laboratory A, a bacterial pathogen was identified in 7.0% of 21 970 specimens. During 1996-2006, Campylobacter was the most common bacterial pathogen (2.7% of cultures), followed by Salmonella (1.2%), Shigella (1.0%), and STEC (0.9%). Among STEC (n = 196), O157 was the most common serogroup (31%). During 2000-2006, ETEC (1.9%) was the second most common bacterial pathogen after Campylobacter (2.6%). In Laboratory B, of 19 293 specimens tested, a bacterial pathogen was identified for 5.5%, including Campylobacter (2.1%), STEC (1.3%), Salmonella (1.0%), and ETEC (0.8%). Among STEC (n = 253), O157 was the leading serogroup (35%). Among ETEC cases, 61% traveled internationally. Conclusions. Enterotoxigenic E. coli and STEC infections were as common as most other enteric bacterial pathogens, and ETEC may be detected more frequently by culture-independent multiplex PCR diagnostic methods. A high proportion of ETEC cases were domestically acquired.