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.

Use of Whole Genome Sequencing by the Federal Interagency Collaboration for Genomics for Food and Feed Safety in the United States.

ABSTRACT: This multiagency report developed by the Interagency Collaboration for Genomics for Food and Feed Safety provides an overview of the use of and transition to whole genome sequencing (WGS) technology for detection and characterization of pathogens transmitted commonly by food and for identification of their sources. We describe foodborne pathogen analysis, investigation, and harmonization efforts among the following federal agencies: National Institutes of Health; Department of Health and Human Services, Centers for Disease Control and Prevention (CDC) and U.S. Food and Drug Administration (FDA); and the U.S. Department of Agriculture, Food Safety and Inspection Service, Agricultural Research Service, and Animal and Plant Health Inspection Service. We describe single nucleotide polymorphism, core-genome, and whole genome multilocus sequence typing data analysis methods as used in the PulseNet (CDC) and GenomeTrakr (FDA) networks, underscoring the complementary nature of the results for linking genetically related foodborne pathogens during outbreak investigations while allowing flexibility to meet the specific needs of Interagency Collaboration partners. We highlight how we apply WGS to pathogen characterization (virulence and antimicrobial resistance profiles) and source attribution efforts and increase transparency by making the sequences and other data publicly available through the National Center for Biotechnology Information. We also highlight the impact of current trends in the use of culture-independent diagnostic tests for human diagnostic testing on analytical approaches related to food safety and what is next for the use of WGS in the area of food safety.

Multidrug-Resistant Salmonella I 4,[5],12:i:- and Salmonella Infantis Infections Linked to Whole Roasted Pigs from a Single Slaughter and Processing Facility.

We describe two outbreaks of multidrug-resistant (MDR) Salmonella I 4,[5],12:i:- infection, occurring in 2015 to 2016, linked to pork products, including whole roaster pigs sold raw from a single Washington slaughter and processing facility (establishment A). Food histories from 80 ill persons were compared with food histories reported in the FoodNet 2006 to 2007 survey of healthy persons from all 10 U.S. FoodNet sites who reported these exposures in the week before interview. Antimicrobial susceptibility testing and whole genome sequencing were conducted on selected clinical, food, and environmental isolates. During 2015, a total of 192 ill persons were identified from five states; among ill persons with available information, 30 (17%) of 180 were hospitalized, and none died. More ill persons than healthy survey respondents consumed pork (74 versus 43%, P < 0.001). Seventeen (23%) of 73 ill persons for which a response was available reported attending an event where whole roaster pig was served in the 7 days before illness onset. All 25 clinical isolates tested from the 2015 outbreak and a subsequent 2016 smaller outbreak (n = 15) linked to establishment A demonstrated MDR. Whole genome sequencing of clinical, environmental, and food isolates (n = 69) collected in both investigations revealed one clade of highly related isolates, supporting epidemiologic and traceback data that establishment A as the source of both outbreaks. These investigations highlight that whole roaster pigs, an uncommon food vehicle for MDR Salmonella I 4,[5],12:i:- outbreaks, will need further attention from food safety researchers and educators for developing science-based consumer guidelines, specifically with a focus on the preparation process.

Protracted Outbreak of Salmonella Newport Infections Linked to Ground Beef: Possible Role of Dairy Cows - 21 States, 2016-2017.

In January 2017, CDC identified a cluster of Salmonella enterica serotype Newport infections with isolates sharing an indistinguishable pulsed-field gel electrophoresis (PFGE) pattern, JJPX01.0010 (pattern 10), through PulseNet, the national molecular subtyping network for foodborne disease surveillance. This report summarizes the investigation by CDC, state and local health and agriculture departments, and the U.S. Department of Agriculture's Food Safety and Inspection Service (USDA-FSIS) and discusses the possible role of dairy cows as a reservoir for strains of Salmonella that persistently cause human illness. This investigation combined epidemiologic and whole genome sequencing (WGS) data to link the outbreak to contaminated ground beef; dairy cows were hypothesized to be the ultimate source of Salmonella contamination.

Intensified Sampling in Response to a Salmonella Heidelberg Outbreak Associated with Multiple Establishments Within a Single Poultry Corporation.

On June 28, 2013, the Food Safety and Inspection Service (FSIS) was notified by the Centers for Disease Control and Prevention (CDC) of an investigation of a multistate cluster of illnesses of Salmonella enterica serovar Heidelberg. Since case-patients in the cluster reported consumption of a variety of chicken products, FSIS used a simple likelihood-based approach using traceback information to focus on intensified sampling efforts. This article describes the multiphased product sampling approach taken by FSIS when epidemiologic evidence implicated chicken products from multiple establishments operating under one corporation. The objectives of sampling were to (1) assess process control of chicken slaughter and further processing and (2) determine whether outbreak strains were present in products from these implicated establishments. As part of the sample collection process, data collected by FSIS personnel to characterize product included category (whole chicken and type of chicken parts), brand, organic or conventional product, injection with salt solutions or flavorings, and whether product was skinless or skin-on. From the period September 9, 2013, through October 31, 2014, 3164 samples were taken as part of this effort. Salmonella percent positive declined from 19.7% to 5.3% during this timeframe as a result of regulatory and company efforts. The results of intensified sampling for this outbreak investigation informed an FSIS regulatory response and corrective actions taken by the implicated establishments. The company noted that a multihurdle approach to reduce Salmonella in products was taken, including on-farm efforts such as environmental testing, depopulation of affected flocks, disinfection of affected houses, vaccination, and use of various interventions within the establishments over the course of several months.

National Outbreak of Multidrug Resistant Salmonella Heidelberg Infections Linked to a Single Poultry Company.

IMPORTANCE: This large outbreak of foodborne salmonellosis demonstrated the complexity of investigating outbreaks linked to poultry products. The outbreak also highlighted the importance of efforts to strengthen food safety policies related to Salmonella in chicken parts and has implications for future changes within the poultry industry. OBJECTIVE: To investigate a large multistate outbreak of multidrug resistant Salmonella Heidelberg infections. DESIGN: Epidemiologic and laboratory investigations of patients infected with the outbreak strains of Salmonella Heidelberg and traceback of possible food exposures. SETTING: United States. Outbreak period was March 1, 2013 through July 11, 2014. PATIENTS: A case was defined as illness in a person infected with a laboratory-confirmed Salmonella Heidelberg with 1 of 7 outbreak pulsed-field gel electrophoresis (PFGE) XbaI patterns with illness onset from March 1, 2013 through July 11, 2014. A total of 634 case-patients were identified through passive surveillance; 200/528 (38%) were hospitalized, none died. RESULTS: Interviews were conducted with 435 case-patients: 371 (85%) reported eating any chicken in the 7 days before becoming ill. Of 273 case-patients interviewed with a focused questionnaire, 201 (74%) reported eating chicken prepared at home. Among case-patients with available brand information, 152 (87%) of 175 patients reported consuming Company A brand chicken. Antimicrobial susceptibility testing was completed on 69 clinical isolates collected from case-patients; 67% were drug resistant, including 24 isolates (35%) that were multidrug resistant. The source of Company A brand chicken consumed by case-patients was traced back to 3 California production establishments from which 6 of 7 outbreak strains were isolated. CONCLUSIONS: Epidemiologic, laboratory, traceback, and environmental investigations conducted by local, state, and federal public health and regulatory officials indicated that consumption of Company A chicken was the cause of this outbreak. The outbreak involved multiple PFGE patterns, a variety of chicken products, and 3 production establishments, suggesting a reservoir for contamination upstream from the production establishments. Sources of bacteria and genes responsible for resistance, such as farms providing birds for slaughter or environmental reservoir on farms that raise chickens, might explain how multiple PFGE patterns were linked to chicken from 3 separate production establishments and many different poultry products.

Notes from the Field: Outbreak of Multidrug-Resistant Salmonella Infections Linked to Pork--Washington, 2015.

During June-July 2015, Public Health-Seattle & King County (PHSKC) and Washington State Department of Health (WADOH) investigated 22 clusters of Salmonella serotype I 4,[5], 12:i:- infections. Serotype I 4,[5], 12:i:- is the fifth most frequently reported Salmonella serotype in the United States, but is uncommon in Washington. On July 29, 2015, WADOH and PHSKC requested assistance from CDC to identify the infection source, determine risk factors, and make recommendations for prevention.

Escherichia coli O157:H7 Outbreak Associated with Restaurant Beef Grinding.

Escherichia coli O157:H7 is a common cause of foodborne illness in the United States. Beef ground at establishments regulated by the U.S. Department of Agriculture, Food Safety and Inspection Service is routinely tested for E. coli O157:H7. Prior to December 2013, boxed beef product (wholesale cuts of beef, such as beef loin, packaged into bags and boxed for shipping) was not always tested for this pathogen. Downstream processors or retailers may grind the product; and, if the ground beef is not cooked to the recommended temperature, pathogens on the exterior of the beef introduced to the interior through grinding may survive. On 18 October 2013, the Allegheny County Health Department identified two E. coli O157:H7 cases, both of whom were food handlers at restaurant A, a restaurant that ground locally produced boxed beef for hamburgers on site. Case finding was conducted through public messaging, employee surveys, and disease surveillance. All potential cases were interviewed using a standard questionnaire. A confirmed case was defined as laboratory-confirmed E. coli O157:H7 with exposure to restaurant A. A probable case was defined as a patient with compatible symptoms and exposure to restaurant A but without laboratory confirmation. All human and food isolates were characterized by pulsed-field gel electrophoresis and multilocus variable-number tandem repeat analysis. The analysis identified 14 confirmed and 10 probable cases of E. coli; 18 nonintact ground beef samples tested positive for E. coli O157:H7. Nine confirmed cases were restaurant A employees. All confirmed cases recalled eating a restaurant A hamburger in the 10 days before illness onset; most cases reported consuming medium to rare hamburgers. Multiple pulsed-field gel electrophoresis and multilocus variable-number tandem repeat analysis patterns were identified among both the human and ground beef isolates, and the patient isolates matched those found in ground beef samples. Restaurant A voluntarily closed for 1.5 days, changed beef suppliers, ceased grinding beef in-house, and has had no new cases since reopening.

Application of Bayesian techniques to model the burden of human salmonellosis attributable to U.S. food commodities at the point of processing: adaptation of a Danish model.

Mathematical models that estimate the proportion of foodborne illnesses attributable to food commodities at specific points in the food chain may be useful to risk managers and policy makers to formulate public health goals, prioritize interventions, and document the effectiveness of mitigations aimed at reducing illness. Using human surveillance data on laboratory-confirmed Salmonella infections from the Centers for Disease Control and Prevention and Salmonella testing data from U.S. Department of Agriculture Food Safety and Inspection Service's regulatory programs, we developed a point-of-processing foodborne illness attribution model by adapting the Hald Salmonella Bayesian source attribution model. Key model outputs include estimates of the relative proportions of domestically acquired sporadic human Salmonella infections resulting from contamination of raw meat, poultry, and egg products processed in the United States from 1998 through 2003. The current model estimates the relative contribution of chicken (48%), ground beef (28%), turkey (17%), egg products (6%), intact beef (1%), and pork (<1%) across 109 Salmonella serotypes found in food commodities at point of processing. While interpretation of the attribution estimates is constrained by data inputs, the adapted model shows promise and may serve as a basis for a common approach to attribution of human salmonellosis and food safety decision-making in more than one country.

Chicken salad as the source of a case of Listeria monocytogenes infection in Connecticut.

Listeriosis is a severe infection with high morbidity and mortality. We report a fatal case of listeriosis in a patient with a history of Crohn's disease who consumed chicken salad purchased from a retail food establishment before developing listeriosis. As part of the regulatory testing programs, the U.S. Department of Agriculture Food Safety and Inspection Service and the Florida Department of Agriculture and Consumer Affairs found that chicken products from a single food-production establishment were contaminated with Listeria monocytogenes, resulting in a product recall. The case patient's Listeria isolate was subtyped by pulsed-field gel electrophoresis (PFGE) and matched the Listeria isolates from the recalled chicken products. Identification of the source of Listeria involved collaboration among two state public health laboratories and epidemiologists and state and federal regulatory agencies. PFGE typing can be used to reveal correlations between clusters of human illness and contaminated food products and to rapidly identify sources of Listeria infection to allow implementation of corrective actions at both the state and national levels.