Chicago Salmonella Outbreak sickens 109

An outbreak of Salmonella was investigated by the Illinois Department of Public Health (IDPH) and the Chicago Department of Public Health (CDPH) in the summer of 2023. This outbreak was assigned the outbreak code IL2023-1678. An increase in the number of Salmonella cases was identified in September 2023, and the only location found to be common to these early cases was Carniceria Guanajuato at 3140 N. California Ave. in Chicago, Illinois, a grocery store chain and taqueria. Only this location was linked to the outbreak.

On September 8, CDPH issued a health alert to all Chicago hospitals to notify them of the outbreak, request prompt reporting of Salmonella cases, and inform clinicians of the high hospitalization rate among cases. On September 14, 2023, CDPH shared a press release about the outbreak to encourage all persons who dined at Carniceria Guanajuato to report their exposure to CDPH and to seek testing with their provider if they were experiencing symptoms. IDPH issued a CD alert to local health departments to notify them of any Salmonella cases who reported eating food purchased from Carniceria Guanajuato to interview or contact CDPH.

Outbreak definitions were created. A confirmed case was considered an individual who tested positive for S. Newport that was highly related (within 10 alleles) to the outbreak strain by whole genome sequencing (WGS) from August to September 2023, or a patron who reported eating at Carniceria Guanajuato in the week prior to onset of symptoms and tested positive via a culture for Salmonella at a clinical laboratory. A probable case (with lab testing) was defined as a patron who reported eating at Carniceria Guanajuato in the week prior to onset of symptoms and tested positive via a non-culture test for Salmonella at a clinical laboratory. A probable case (ill meal companion) was defined as a patron who had diarrhea (>3 stools in a 24-hour period) and/or vomiting and reported eating at Carniceria Guanajuato in the week prior to onset of symptoms and was epi-linked to a confirmed case. A probable case (clinically compatible illness with known exposure) was defined as a patron who had diarrhea (>3 stools in a 24-hour period) that was at least three days in duration or was accompanied by fever and reported eating at Carniceria Guanajuato in the week prior to onset of symptoms and was not epi-linked to a confirmed case.

            A total of 109 (45 confirmed, 64 probable) cases who met the outbreak definition were reported in this outbreak. Seven confirmed cases denied or could not recall eating at Carniceria Guanajuato despite matching the outbreak WGS pattern, and thus were excluded from the statistical analysis. One case was a resident of Louisiana. Median age of all cases was 36 years (range, 6 to 70 years); 62 (61%) were male.  For whom information was collected, 25 (23%) were hospitalized. For whom information was collected, none died. Exposures were reported between August 27 and September 6, 2023. Onsets were reported between August 27 and September 13, 2023. Most cases experienced diarrhea (some bloody), fever, and vomiting.

A case-control study was conducted to determine a potential food vehicle for infection with Salmonella. To identify controls, CD Program staff asked confirmed cases about their meal companions and obtained a list of individuals who placed orders through the online delivery service Uber Eats and consumed food between August 27 to September 8, 2023. The case-control analysis included 38 confirmed cases and 30 controls. Based on case exposure information collected for a case-control study, environmental and food testing, and a facility inspection, the common location to cases was Carniceria Guanajuato at 3140 N. California Ave. in Chicago, Illinois. 

A statistically significant association was observed between multiple food items and illness, including consumption of lettuce (odds ratio [OR] 5.96, 95% CI: 2.07-17.19), tomato (OR 5.96, 95% CI: 2.07-17.19), beans (OR 7.12, 95% CI: 2.40-21.13), and steak torta (OR 5.85, 95% CI: 1.71-20.02). These items are standard toppings included on a torta, and thus were highly correlated with one another. Lettuce, tomato and beans were all consumed by 68% of confirmed cases. Consumption was variable, however, among probable cases with lettuce, tomato and beans being consumed by 77%, 58% and 56% of probable cases respectively. 

On September 8, 2023, the Food Protection Division (FPD) conducted an environmental inspection of Carniceria Guanajuato and collected the following: food samples, initial information about restaurant employees and food preparation, and copies of invoices for food items. Food items collected included steak (raw and cooked), lettuce, onion, cilantro, tomato, avocado, refried beans, chile relleno, guacamole, pico de gallo, chile de arbol, and red salsa. CD Program staff performed in-depth interviews with the owners of the restaurant and employees. Because employees functioned in multiple roles, 14 restaurant employees were considered food handlers for the purposes of this outbreak investigation. Food handlers were asked to submit stool specimens to screen for Salmonella. Among the 14 food handlers interviewed, none reported any history of gastrointestinal illness in the two weeks preceding or during the outbreak period.

Several violations were identified during the sanitarians’ inspection of Carniceria Guanajuato: raw beef steak was observed above ready to eat foods (e.g., sliced lettuce) inside prep cooler, two cutting boards with deep seams and stains in found in the prep/cooking area, sliced tomatoes were held at an improper temperature, and improper cleaning of large pots due to the inability to submerge the pots in the sinks. Carniceria Guanajuato voluntarily closed on September 8, 2023 and re-opened on September 22, 2023. No additional complaints were received in association with the restaurant in the month following the date of this incident.

The outbreak strain was identified as Salmonella Newport. Specimens from the 38 confirmed cases included in the analysis yielded Salmonella isolates. Thirty-seven of the isolates were S. Newport and were clustered within 0-2 single-nucleotide polymorphisms (SNP) differences, indicating a close link among the cases. A second serotype was identified among one of the confirmed cases as a Multi-Drug Resistant strain of S. Newport. Additionally, of the 14 food handlers were screened, four tested positive for the outbreak strain of S. Newport and one tested positive for a different serotype, S. Enteritidis. Red salsa collected on September 8 from the grocery store cooler was found to be positive for S. Johannesburg, which was different than the outbreak strain of S. Newport. None of the other tested foods were found to be positive for Salmonella.

Statistical analysis with only confirmed cases identified beans as being statistically significant. This, however, did not align with the results of the sensitivity analysis, which used both confirmed and probable cases and found lettuce to be statistically significant. This misalignment is likely due to both differences in consumption of food items by confirmed versus probable cases and methodological limitations (i.e., unmatched case-control, insufficient number of controls) of the study. CDPH hypothesized that lettuce was the likely source of this outbreak, as it is fresh produce and is consequently at higher risk of contamination. This outbreak may have been caused by contamination of lettuce by infected food handlers or through cross-contamination from another source. The presence of multiple serotypes identified among cases, food handlers, and prepared foods also suggests the possibility of multiple cross-contamination events. Closure of the restaurant during the early stage of the investigation prevented additional cases of illness from occurring. 

Republished with permission from Bill Marler and Marler Clark. Copyright (c) Marler Clark LLP, PS. All rights reserved.