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.

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.

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.

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.

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.

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.

Characterization of Foodborne Outbreaks of Salmonella enterica Serovar Enteritidis with Whole-Genome Sequencing Single Nucleotide Polymorphism-Based Analysis for Surveillance and Outbreak Detection.

Salmonella enterica serovar Enteritidis is a significant cause of gastrointestinal illness in the United States; however, current molecular subtyping methods lack resolution for this highly clonal serovar. Advances in next-generation sequencing technologies have made it possible to examine whole-genome sequencing (WGS) as a potential molecular subtyping tool for outbreak detection and source trace back. Here, we conducted a retrospective analysis of S. Enteritidis isolates from seven epidemiologically confirmed foodborne outbreaks and sporadic isolates (not epidemiologically linked) to determine the utility of WGS to identify outbreaks. A collection of 55 epidemiologically characterized clinical and environmental S. Enteritidis isolates were sequenced. Single nucleotide polymorphism (SNP)-based cluster analysis of the S. Enteritidis genomes revealed well supported clades, with less than four-SNP pairwise diversity, that were concordant with epidemiologically defined outbreaks. Sporadic isolates were an average of 42.5 SNPs distant from the outbreak clusters. Isolates collected from the same patient over several weeks differed by only two SNPs. Our findings show that WGS provided greater resolution between outbreak, sporadic, and suspect isolates than the current gold standard subtyping method, pulsed-field gel electrophoresis (PFGE). Furthermore, results could be obtained in a time frame suitable for surveillance activities, supporting the use of WGS as an outbreak detection and characterization method for S. Enteritidis.

Bacterial enteric infections detected by culture-independent diagnostic tests--FoodNet, United States, 2012-2014.

The increased availability and rapid adoption of culture-independent diagnostic tests (CIDTs) is moving clinical detection of bacterial enteric infections away from culture-based methods. These new tests do not yield isolates that are currently needed for further tests to distinguish among strains or subtypes of Salmonella, Campylobacter, Shiga toxin-producing Escherichia coli, and other organisms. Public health surveillance relies on this detailed characterization of isolates to monitor trends and rapidly detect outbreaks; consequently, the increased use of CIDTs makes prevention and control of these infections more difficult. During 2012-2013, the Foodborne Diseases Active Surveillance Network (FoodNet*) identified a total of 38,666 culture-confirmed cases and positive CIDT reports of Campylobacter, Salmonella, Shigella, Shiga toxin-producing E. coli, Vibrio, and Yersinia. Among the 5,614 positive CIDT reports, 2,595 (46%) were not confirmed by culture. In addition, a 2014 survey of clinical laboratories serving the FoodNet surveillance area indicated that use of CIDTs by the laboratories varied by pathogen; only CIDT methods were used most often for detection of Campylobacter (10%) and STEC (19%). Maintaining surveillance of bacterial enteric infections in this period of transition will require enhanced surveillance methods and strategies for obtaining bacterial isolates.

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.

Notes from the field: multistate outbreak of listeriosis linked to soft-ripened cheese--United States, 2013.

On June 27, 2013, the Minnesota Department of Health notified CDC of two patients with invasive Listeria monocytogenes infections (listeriosis) whose clinical isolates had indistinguishable pulsed-field gel electrophoresis (PFGE) patterns. A query of PulseNet, the national molecular subtyping network for foodborne disease surveillance, identified clinical and environmental isolates from other states. On June 28, CDC learned from the Food and Drug Administration's Coordinated Outbreak Response and Evaluation Network that environmental isolates indistinguishable from those of the two patients had been collected from Crave Brothers Farmstead Cheese during 2010-2011. An outbreak-related case was defined as isolation of L. monocytogenes with the outbreak PFGE pattern from an anatomic site that is normally sterile (e.g., blood or cerebrospinal fluid), or from a product of conception, with an isolate upload date during May 20-June 28, 2013. As of June 28, five cases were identified in four states (Minnesota, two cases; Illinois, Indiana, and Ohio, one each). Median age of the five patients was 58 years (range: 31-67 years). Four patients were female, including one who was pregnant at the time of infection. All five were hospitalized. One death and one miscarriage were reported.

An outbreak of foodborne illness among attendees of a wedding reception in Wisconsin likely caused by Arcobacter butzleri.

BACKGROUND: Arcobacter species, primarily Arcobacter butzleri, are widely distributed among animals, infrequently isolated from humans, and previously not associated with outbreaks of foodborne illness. We report results of an investigation of a foodborne outbreak that occurred among attendees of a wedding reception in Wisconsin, United States, and was likely caused by A. butzleri. METHODS: We conducted a case-control study among reception attendees and a laboratory investigation to determine the extent, source, and cause of the outbreak. A clinical case was defined as diarrhea in an attendee with illness onset ≤7 days following the wedding reception. RESULTS: The case-control study included 47 of 51 case patients and 43 non-ill attendees. Results demonstrated that consuming broasted chicken was the only factor significantly associated with illness (odds ratio 10.51; 95% confidence interval 1.28, 476.4). Five patients provided stool specimens. Comprehensive culture and polymerase chain reaction (PCR) testing did not detect common bacterial or viral pathogens. Subsequent testing with PCRs targeting 16S/23S rDNA of the three most clinically relevant Arcobacter spp. and the rpoB/C gene of A. butzleri provided products confirmed as A. butzleri (four patients) and A. cryaerophilus (one patient) by sequence analysis. CONCLUSIONS: The results of this investigation suggest that A. butzleri should be considered an agent that can cause outbreaks of foodborne illness. Rigorous investigation of outbreaks of undetermined etiology is valuable for incrementally increasing our understanding of emerging agents causing foodborne illnesses.

Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000-2010: epidemiologic features and comparison with E. coli O157 infections.

BACKGROUND: Shiga toxin-producing Escherichia coli (STEC) are an important cause of diarrhea and the major cause of postdiarrheal hemolytic uremic syndrome. Non-O157 STEC infections are being recognized with greater frequency because of changing laboratory practices. METHODS: Foodborne Diseases Active Surveillance Network (FoodNet) site staff conducted active, population-based surveillance for laboratory-confirmed STEC infections. We assessed frequency and incidence of STEC infections by serogroup and examined and compared demographic factors, clinical characteristics, and frequency of international travel among patients. RESULTS: During 2000-2010, FoodNet sites reported 2006 cases of non-O157 STEC infection and 5688 cases of O157 STEC infections. The number of reported non-O157 STEC infections increased from an incidence of 0.12 per 100,000 population in 2000 to 0.95 per 100,000 in 2010; while the rate of O157 STEC infections decreased from 2.17 to 0.95 per 100,000. Among non-O157 STEC, six serogroups were most commonly reported: O26 (26%), O103 (22%), O111 (19%), O121 (6%), O45 (5%), and O145 (4%). Non-O157 STEC infections were more common among Hispanics, and infections were less severe than those caused by O157 STEC, but this varied by serogroup. Fewer non-O157 STEC infections were associated with outbreaks (7% versus 20% for O157), while more were associated with international travel (14% versus 3% for O157). CONCLUSIONS: Improved understanding of the epidemiologic features of non-O157 STEC infections can inform food safety and other prevention efforts. To detect both O157 and non-O157 STEC infections, clinical laboratories should routinely and simultaneously test all stool specimens submitted for diagnosis of acute community-acquired diarrhea for O157 STEC and for Shiga toxin and ensure that isolates are sent to a public health laboratory for serotyping and subtyping.

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.

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.

A novel vehicle for transmission of Escherichia coli O157:H7 to humans: multistate outbreak of E. coli O157:H7 infections associated with consumption of ready-to-bake commercial prepackaged cookie dough--United States, 2009.

BACKGROUND: Escherichia coli O157:H7 is a Shiga toxin-producing E. coli (STEC) associated with numerous foodborne outbreaks in the United States and is an important cause of bacterial gastrointestinal illness. In May 2009, we investigated a multistate outbreak of E. coli O157:H7 infections. METHODS: Outbreak-associated cases were identified using serotyping and molecular subtyping procedures. Traceback investigation and product testing were performed. A matched case-control study was conducted to identify exposures associated with illness using age-, sex-, and state-matched controls. RESULTS: Seventy-seven patients with illnesses during the period 16 March-8 July 2009 were identified from 30 states; 35 were hospitalized, 10 developed hemolytic-uremic syndrome, and none died. Sixty-six percent of patients were <19 years; 71% were female. In the case-control study, 33 of 35 case patients (94%) consumed ready-to-bake commercial prepackaged cookie dough, compared with 4 of 36 controls (11%) (matched odds ratio = 41.3; P < .001); no other reported exposures were significantly associated with illness. Among case patients consuming cookie dough, 94% reported brand A. Three nonoutbreak STEC strains were isolated from brand A cookie dough. The investigation led to a recall of 3.6 million packages of brand A cookie dough and a product reformulation. CONCLUSIONS: This is the first reported STEC outbreak associated with consuming ready-to-bake commercial prepackaged cookie dough. Despite instructions to bake brand A cookie dough before eating, case patients consumed the product uncooked. Manufacturers should consider formulating ready-to-bake commercial prepackaged cookie dough to be as safe as a ready-to-eat product. More effective consumer education about the risks of eating unbaked cookie dough is needed.