In 2022, the U.S. Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state partners conducted a sample-initiated investigation of a multistate outbreak of Salmonella Senftenberg illnesses linked to peanut butter. Twenty-one illnesses and four hospitalizations were reported in 17 states, with a significant epidemiological signal for peanut butter from Firm A. Whole genome sequence (WGS) data from a Salmonella-positive environmental swab sample collected at Firm A in 2010 yielded the outbreak strain that was a match to the WGS data from the 2022 clinical isolates. Lot code information collected from patients indicated Firm A's facility in Kentucky as a common manufacturing source, and FDA and state partners initiated an inspection. In 2021, Firm A installed two new roasters with at least one of the cooling air supply vents leaking, allowing unfiltered air and rainwater to enter the cooling section after the roasting process. Investigators noted the limitations of Firm A's finished product testing program to identify contamination. Investigative partners from five states collected and analyzed 14 product samples, and FDA collected 205 environmental swabs, and all were negative. Although the exact source and route of the contamination were not determined, epidemiological and traceback evidence confirmed peanut butter consumed by patients was produced by Firm A. Firm A voluntarily recalled all implicated products and provided a plan for corrective actions and restart to FDA. This was the first major domestic investigation of a multistate-foodborne illness outbreak linked to peanut butter since 2012. This investigation demonstrates the importance of caution with reliance on finished product testing, taking appropriate corrective actions when detection occurs, and potential benefits for industry to incorporate WGS as a tool in their environmental monitoring program.

In 2021, the U.S. Food and Drug Administration (FDA), Centers for Disease Control and Prevention (CDC), and state partners investigated a multi-state sample-initiated retrospective outbreak investigation (SIROI) consisting of a cluster of nine Salmonella Weltevreden illnesses associated with frozen, pre-cooked shrimp imported from India. Import surveillance testing identified Salmonella Weltevreden recovered from a cooked shrimp sample from Supplier B. In total, nine patients with clinical isolates highly related via whole genome sequencing were reported in four states with illness onset dates between February 26 and July 17, 2021. Epidemiologic data was gathered by state partners for seven patients, whom all reported exposure to shrimp. Five patients reported consuming shrimp cocktail from the same retailer. A traceback investigation for five of the six patients converged on Supplier B. This evidence demonstrated that the outbreak of Salmonella Weltevreden illnesses was caused by the consumption of cooked, ready-to-eat shrimp manufactured by Supplier B. At the time of the investigation, outbreak and recall information was shared with Indian competent authorities. In March 2022, a follow up inspection of Supplier B's facility in India was conducted, and insanitary conditions and practices were observed. This outbreak investigation highlighted the importance of multidisciplinary national and international public health partnerships. The lessons learned from this investigation should continue to inform investigational activities and food safety guidance for industry.

In 2021, the U.S. Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state and local health and regulatory partners investigated an outbreak of Salmonella enterica serovar Oranienburg infections linked to bulb onions from Mexico, resulting in 1040 illnesses and 260 hospitalizations across 39 states, the District of Columbia, and Puerto Rico. The Kansas Department of Agriculture recovered the outbreak strain of Salmonella Oranienburg from a sample of condiment collected from an ill person's home. The condiment was made with cilantro, lime, and onions, but, at the time of collection, there were no onions remaining in it. FDA conducted traceback investigations for white, yellow, and red bulb onions, cilantro, limes, tomatoes, and jalapeño peppers. Growers in the state of Chihuahua, Mexico, were identified as supplying the implicated onions that could account for exposure to onions for all illnesses included in the traceback investigation, but investigators could not determine a single source or route of contamination. FDA collected product and environmental samples across the domestic supply chain but did not recover the outbreak strain of Salmonella. Binational collaboration and information sharing supported Mexican authorities in collecting environmental samples from two packing plants and onion, water, and environmental samples from 15 farms and firms in Chihuahua, Mexico identified through FDA's traceback investigation, but did not recover the outbreak strain. Distributors of the implicated onions issued voluntary recalls of red, yellow, and white whole, fresh onions imported from the state of Chihuahua, Mexico. This outbreak showcased how investigators overcame significant traceback and epidemiologic challenges, the need for strengthening the ongoing collaboration between U.S. and Mexican authorities and highlighted the need for identifying practices across the supply chain that can help improve the safety of onions. © 2024

Retracing microbial emergence and spread is essential to understanding the evolution and dynamics of pathogens. The bacterial foodborne pathogen Listeria monocytogenes clonal complex 1 (Lm-CC1) is the most prevalent clonal group associated with listeriosis, and is strongly associated with cattle and dairy products. Here we analysed 2,021 Lm-CC1 isolates collected from 40 countries, since the first Lm isolation to the present day, to define its evolutionary history and population dynamics. Our results suggest that Lm-CC1 spread worldwide from North America following the Industrial Revolution through two waves of expansion, coinciding with the transatlantic livestock trade in the second half of the 19th century and the rapid growth of cattle farming in the 20th century. Lm-CC1 then firmly established at a local level, with limited inter-country spread. This study provides an unprecedented insight into Lm-CC1 phylogeography and dynamics and can contribute to effective disease surveillance to reduce the burden of listeriosis.Competing Interest StatementThe authors have declared no competing interest.

The United States are one of the world's leading consumers of melons. In 2020, the Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state health and regulatory partners investigated an outbreak of Salmonella Newport infections linked to melons from southwest Indiana, resulting in 80 ill persons and 18 hospitalizations reported across 15 states. Epidemiologic and traceback data indicated melons as the vehicle for these infections, but the collinearity of melon varieties purchased and consumed together in combination with the traceback investigation that could not rule out either melon type, did not allow investigators to delineate whether the vehicle was cantaloupe alone or, both cantaloupe and watermelons. Analysis of traceback records for cantaloupe and/or watermelon exposures for 12 ill people indicated convergence on a grower in southwest Indiana which supplied cantaloupe to the nine of eleven points of service where ill people purchased cantaloupe; similar convergence was not observed for watermelon. While Salmonella isolates were recovered from environmental samples collected by FDA throughout the growing operation, they were not highly genetically related to the outbreak strain by whole genome sequencing analyses, i.e. greater than a 20 high quality single nucleotide polymorphisms difference. This outbreak illustrates the need for additional efforts to determine the source and extent of environmental contamination in the melon growing region of southwest Indiana and emphasizes the need for outreach and education efforts to help promote farm practices to reduce pathogen contamination of melons. 2023

Foodborne outbreak investigations have traditionally included the detection of a cluster of illnesses first, followed by an epidemiologic investigation to identify a food of interest. The increasing use of whole genome sequencing (WGS) subtyping technology for clinical, environmental, and food isolates of foodborne pathogens, and the ability to share and compare the data on public platforms, present new opportunities to identify earlier links between illnesses and their potential sources. We describe a process called sample-initiated retrospective outbreak investigations (SIROI) used by federal public health and regulatory partners in the United States. SIROIs begin with an evaluation of the genomic similarity between bacterial isolates recovered from food or environmental samples and clusters of clinical isolates while subsequent and parallel epidemiologic and traceback investigations are initiated to corroborate their connection. SIROIs allow for earlier hypothesis generation, followed by targeted collection of information about food exposures and the foods and manufacturer of interest, to confirm a link between the illnesses and their source. This often leads to earlier action that could reduce the breadth and burden of foodborne illness outbreaks. We describe two case studies of recent SIROIs and present the benefits and challenges. Benefits include insight into foodborne illness attribution, international collaboration, and opportunities for enhanced food safety efforts in the food industry. Challenges include resource intensiveness, variability of epidemiologic and traceback data, and an increasingly complex food supply chain. SIROIs are valuable in identifying connections among small numbers of illnesses that may span significant time periods; detecting early signals for larger outbreaks or food safety issues associated with manufacturers; improving our understanding of the scope of contamination of foods; and identifying novel pathogen/commodity pairs.

In 2021, the U.S. Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state partners investigated a multistate outbreak of Salmonella Typhimurium illnesses linked to packaged leafy greens from a controlled environment agriculture (CEA) operation in Illinois. Thirty-one illnesses and four hospitalizations were reported in four states, with a significant epidemiologic signal for packaged leafy greens from Farm A. A traceback investigation for leafy greens included seven points of service (POS) with food exposure data from eight ill people. Each POS was supplied leafy greens by Farm A. FDA investigators observed operations at Farm A and noted that 1) the firm did not consider their indoor hydroponic pond water as agricultural water, 2) condensate dripping from the chiller water supply line inside the building, and 3) unprotected outdoor storage of packaged soilless growth media and pallets used for finished product. FDA collected 25 product, water, and environmental samples from Farm A. The outbreak strain was recovered from a water sample collected from a stormwater drainage basin located on the property adjacent to Farm A. In addition, an isolate of Salmonella Liverpool was recovered from two indoor growing ponds within the same growing house, but no illnesses were linked to the isolate. Farm A voluntarily recalled all implicated products and provided their root cause analysis (RCA) and return-to-market plan to FDA. While the source and route of the contamination were not determined by the RCA, epidemiologic and traceback evidence confirmed the packaged salads consumed by ill persons were produced by Farm A. This was the first investigation of a multistate foodborne illness outbreak associated with leafy greens grown in a CEA operation. This outbreak demonstrated the need for growers using hydroponic methods to review their practices for potential sources and routes of contamination and to reduce food safety risks when identified.

This multi-agency report developed under the Interagency Collaboration for Genomics for Food and Feed Safety (Gen-FS) provides an overview of the use of and transition to Whole-Genome Sequencing (WGS) technology to detect and characterize pathogens transmitted commonly by food and identify their sources. We describe foodborne pathogen analysis, investigation, and harmonization efforts among federal agencies, including the National Institutes of Health (NIH); the Department of Health and Human Services' Centers for Disease Control and Prevention (CDC) and the Food and Drug Administration (FDA); and the U.S. Department of Agriculture's Food Safety and Inspection Service (FSIS), Agricultural Research Service (ARS), and Animal and Plant Health Inspection Service (APHIS). We describe single nucleotide polymorphism (SNP), core-genome (cg) and whole-genome multi-locus sequence typing (wgMLST) data analysis methods as used in CDC's PulseNet and FDA's GenomeTrakr 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 Gen-FS agency partners. We highlight how we apply WGS to pathogen characterization (virulence and antimicrobial resistance profiles), source attribution efforts, and increasing transparency by making the sequences and other data publicly available through the National Center for Biotechnology Information (NCBI). Finally, we highlight the impact of current trends in the use of culture-independent diagnostics tests (CIDT) for human diagnostic testing on analytical approaches related to food safety. Lastly, we highlight what is next for WGS in food safety.

Retracing microbial emergence and spread is essential to understanding the evolution and 40 dynamics of pathogens. The bacterial foodborne pathogen Listeria monocytogenes clonal 41 complex 1 (Lm-CC1) is the most prevalent clonal group associated with listeriosis, and is 42 strongly associated with cattle and dairy products. Here we analysed 2,021 Lm-CC1 43 isolates collected from 40 countries, since the first Lm isolation to the present day, to 44 define its evolutionary history and population dynamics. Our results suggest that Lm-CC1 45 spread worldwide from North America following the Industrial Revolution through two 46 waves of expansion, coinciding with the transatlantic livestock trade in the second half of 47 the 19th century and the rapid growth of cattle farming in the 20th century. Lm-CC1 then 48 firmly established at a local level, with limited inter-country spread. This study provides 49 an unprecedented insight into Lm-CC1 phylogeography and dynamics and can contribute 50 to effective disease surveillance to reduce the burden of listeriosis.