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.

Factors associated with regulatory action involving investigation of illnesses associated with Shiga toxin-producing Escherichia coli in products regulated by the Food Safety and Inspection Service.

We described characteristics of the Escherichia coli O157 and Escherichia coli non-O157 illness investigations conducted by the United States Department of Agriculture's Food Safety and Inspection Service (FSIS) during the 5-year period from 2006 through 2010. We created a multivariable logistic regression model to determine characteristics of these investigations that were associated with FSIS regulatory action, which was defined as having occurred if a product recall occurred or if FSIS personnel performed an environmental health assessment (Food Safety Assessment) at the implicated establishment. During this period, FSIS took regulatory action in 38 of 88 (43%) investigations. Illness investigations in which FoodNet states were involved were more likely to result in regulatory action. Illness investigations in which state and local traceback, or FSIS traceback occurred were more likely to result in regulatory action. Reasons for lack of action included evidence of cross-contamination after the product left a regulated establishment, delayed notification, lack of epidemiological information, and insufficient product information.

Characterization of Salmonella enterica serovar Agona slaughter isolates from the animal arm of the National Antimicrobial Resistance Monitoring System-Enteric Bacteria (NARMS): 1997 through 2003.

A total of 499 Salmonella enterica serovar Agona isolates from cattle, swine, chicken, and turkey samples were assayed for antimicrobial susceptibility and subtyped using pulsed-field gel electrophoresis (PFGE). Salmonella Agona isolates exhibited increased resistance to amoxicillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, cephalothin, and chloramphenicol, and a single isolate was resistant to ceftriaxone. Multiple drug resistance (MDR; resistance >or= 2 antimicrobials) was exhibited in 57% (n=282/499) of the Salmonella Agona isolates and 22% (n=111/499) of these Salmonella Agona isolates were resistant to five or more antimicrobials. PFGE patterns of 482 Salmonella Agona slaughter samples resulted in 165 unique patterns. Cluster analysis indicated that isolates indistinguishable by PFGE appeared to group according to antimicrobial resistance profiles. These data suggest that Salmonella Agona is increasing in prevalence in U.S. cattle presented for slaughter and should be further monitored.

Detection of plasmids and class 1 integrons in Salmonella enterica serovar agona isolated from NARMS slaughter samples collected in the years 1997-2003.

A total of 60 Salmonella enterica serovar Agona isolates (25 pan-susceptible isolates and 35 isolates resistant to five or more antimicrobials) submitted to the National Antimicrobial Resistance Monitoring System-Enteric Bacteria (NARMS) from 1997 through 2003 were examined for plasmids and class 1 integrons. Samples originated from cattle, turkey, chicken, and swine presented at federally inspected slaughter and processing plants. Large plasmids (33-291 kb) were present in 83% of the isolates resistant to five or more antimicrobials; however, 16% of the pan-susceptible isolates also had large plasmids. The presence of large plasmids did not correspond to the isolate source or the year the isolate was recovered but did appear to correspond to XbaI pulsed-field gel electrophoresis (PFGE) patterns. Two sizes of large plasmids appeared most often: 145.4 kb and 97 kb. Class 1 integrons were not detected on plasmids but were detected on the chromosome of 8% (2/25) of the pan-susceptible isolates and 49% (17/35) of the isolates with multiple drug resistance. Expression of multiple drug resistance among S. Agona isolates occurred regardless of the presence of class 1 integrons, suggesting that plasmids play an equally important role in the development of resistant S. Agona. More research is needed to understand better the mechanisms by which S. Agona acquires, harbors, and transfers resistance determinants.

Utility of Combining Whole Genome Sequencing with Traditional Investigational Methods To Solve Foodborne Outbreaks of Salmonella Infections Associated with Chicken: A New Tool for Tackling This Challenging Food Vehicle.

High consumption rates and a multitude of brands make multistate foodborne outbreaks of Salmonella infections associated with chicken challenging to investigate, but whole genome sequencing is a powerful tool that can be used to assist investigators. Whole genome sequencing of pathogens isolated from clinical, environmental, and food samples is increasingly being used in multistate foodborne outbreak investigations to determine with unprecedented resolution how closely related these isolates are to one another genetically. In 2014, federal and state health officials investigated an outbreak of 146 Salmonella Heidelberg infections in 24 states. A follow-up analysis was conducted after the conclusion of the investigation in which 27 clinical and 24 food isolates from the outbreak underwent whole genome sequencing. These isolates formed seven clades, the largest of which contained clinical isolates from a subcluster of case patients who attended a catered party. One isolate from a chicken processed by a large producer was closely related genetically (zero to three single-nucleotide polymorphism differences) to the clinical isolates from these subcluster case patients. Chicken from this large producer was also present in the kitchen of the caterer on the day before the event, thus providing additional evidence that the chicken from this producer was the outbreak source. This investigation highlights how whole genome sequencing can be used with epidemiologic and traceback evidence to identify chicken sources of foodborne outbreaks.

Foodborne Outbreaks Reported to the U.S. Food Safety and Inspection Service, Fiscal Years 2007 through 2012.

The U.S. Department of Agriculture's Food Safety and Inspection Service (FSIS) works closely with federal, state, and local public health partners to investigate foodborne illness outbreaks associated with its regulated products. To provide insight into outbreaks associated with meat and poultry, outbreaks reported to FSIS during fiscal years 2007 through 2012 were evaluated. Outbreaks were classified according to the strength of evidence linking them to an FSIS-regulated product and by their epidemiological, etiological, and vehicle characteristics. Differences in outbreak characteristics between the period 2007 through 2009 and the period 2010 through 2012 were assessed using a chi-square test or Mann-Whitney U test. Of the 163 reported outbreaks eligible for analysis, 89 (55%) were identified as possibly linked to FSIS-regulated products and 74 (45%) were definitively linked to FSIS-regulated products. Overall, these outbreaks were associated with 4,132 illnesses, 772 hospitalizations, and 19 deaths. Shiga toxin-producing Escherichia coli was associated with the greatest proportion of reported outbreaks (55%), followed by Salmonella enterica (34%) and Listeria monocytogenes (7%). Meat and poultry products commercially sold as raw were linked to 125 (77%) outbreaks, and of these, 105 (80%) involved beef. Over the study period, the number of reported outbreaks definitively linked to FSIS-regulated products (P = 0.03) declined, while the proportion of culture-confirmed cases (P = 0.0001) increased. Our findings provide insight into the characteristics of outbreaks associated with meat and poultry products.

Introduction to United States Department of Agriculture VetNet: status of Salmonella and Campylobacter databases from 2004 through 2005.

In 2003 the United States Department of Agriculture established USDA VetNet. It was modeled after PulseNet USA, the national molecular subtyping network for foodborne disease surveillance. The objectives of USDA VetNet are: to use pulsed-field gel electrophoresis (PFGE) to subtype zoonotic pathogens submitted to the animal arm of the National Antimicrobial Resistance Monitoring System (NARMS); examine VetNet and PulseNet PFGE patterns; and use the data for surveillance and investigation of suspected foodborne illness outbreaks. Whereas PulseNet subtypes 7 foodborne disease-causing bacteria- Escherichia coli O157:H7, Salmonella, Shigella, Listeria monocytogenes, Campylobacter, Yersinia pestis, and Vibrio cholerae-VetNet at present subtypes nontyphoidal Salmonella serotypes and Campylobacter from animals, including diagnostic specimens, healthy farm animals, and carcasses of food-producing animals at slaughter. By the end of 2005, VetNet had two functioning databases: the NARMS Salmonella and the NARMS Campylobacter databases. The Salmonella database contained 6763 Salmonella isolates and 2514 unique XbaI patterns, while the Campylobacter database contained 58 Campylobacter isolates and 53 unique SmaI patterns. Both databases contain the PFGE tagged image file format (TIFF) images, demographic information, and the antimicrobial resistance profiles assigned by NARMS. In the future, veterinary diagnostic laboratories will be invited to participate in VetNet. The establishment of USDA VetNet enhances the mission of the agriculture and public health communities in the surveillance and investigation of foodborne illness outbreaks.