State and local partners, in collaboration with the Centers for Disease Control and Prevention (CDC), identify outbreaks of foodborne illness through public health surveillance and epidemiologic investigation. If a food product regulated by the U.S. Food and Drug Administration (FDA) is involved, then FDA collaborates with partners to conduct a traceback investigation and determine the origin of the identified food. State and local authorities, in collaboration with FDA, may use product and environmental sampling, as well as laboratory analyses, to further confirm the identified food as the outbreak source. Throughout the course of any given investigation, communication tools are also used to inform the public of outbreaks and provide information on how consumers can protect themselves from illness. To stop outbreaks and protect public health, FDA may use regulatory actions, such as recalls, import alerts, and others, informed by available investigational data to remove products from the market or to refuse entry of imports.

In 2011, the same year that FDA's Food Safety Modernization Act (FSMA) was signed into law, FDA established the Coordinated Outbreak Response and Evaluation (CORE) Network to serve as the agency's focal point for response coordination and evaluation of foodborne illness outbreaks.^1,2 The primary role of FDA CORE is to conduct outbreak surveillance, manage the response efforts, and initiate post-outbreak activities related to incidents involving multiple illnesses linked to FDA-regulated human food, dietary supplements, and cosmetic products. CORE is comprised of the Signals and Surveillance Team (SST), multiple Response Teams (RT), the Outbreak Evaluation Team (OE), the Outbreak Analytics Team (OA), and the Communications Team. Between 2011 and 2022, CORE teams have coordinated surveillance activities for 1,042 illness clusters, responded to 274 outbreaks potentially linked to FDA-regulated products, identified a specific product in 109 outbreaks, and warned consumers to avoid those products through nearly 500 public notifications.

The CORE SST evaluates emerging outbreak and disease surveillance information and, when an FDA-regulated food may be involved, passes relevant information to an RT to coordinate FDA's response efforts.² Similarly, RTs "hunt" for the specific outbreak vehicle to control and stop the outbreak by coordinating investigations, inspections, and sampling, and by tracing product distribution.³ The Communications Team, which is embedded in the response phase of outbreak investigations, follows ongoing investigations to determine when public communications are needed and coordinates those messages with external partners. Once outbreak response activities have ended, the OE and OA Teams collect outbreak information and analyze data, including lessons learned, potential actions moving forward, and trends over time. Findings are then disseminated via publications and presentations in various venues, and are intended to inform policymaking, scientific research, and the public of outbreak investigations and opportunities to reduce foodborne illness.

Even after successful investigations, specific aspects may be identified that can streamline the outbreak investigation process and address food safety prevention approaches to minimize future outbreak impact. After outbreak closure, CORE receives feedback in the form of recommendations from investigative partners, which can guide prevention efforts and improve response to future incidents. Since its launch, CORE's procedures have benefited from the incorporation of internal and external feedback, updated processes, novel technologies, and enhanced federal regulations. Here, the authors discuss some of the pivotal milestones that have impacted the way CORE investigates outbreaks or shares information with partners and the public. Continual improvement is a critical component of the CORE concept, and these examples demonstrate key aspects of CORE's perpetual evolution.

Pivotal Milestones During the Ongoing Evolution of CORE: Processes and Technologies

Incident Command System. Shortly after its 2011 launch, CORE adapted the National Incident Management System principles to standardize outbreak coordination. The incident command system (ICS) allows the CORE organizational structure to scale in a modular fashion, depending on the magnitude and complexity of an outbreak.³ As outbreak complexity increases, the established structure expands from the top down, and responsibilities can be delegated accordingly. CORE uses ICS principles during outbreak investigations, regardless of size, which standardizes operations and establishes clear communication channels and explicit outcomes. Consequently, ICS principles enable CORE to manage multiple outbreaks simultaneously, coordinate with investigative partners to determine next steps through consensus, and collaborate on necessary regulatory and public health actions.

Rapid Response Teams. CORE coordination with FDA's Office of Regulatory Affairs (ORA) and state partners is a frequent occurrence and includes close cooperation during incidents. Rapid Response Teams (RRTs) are multi-agency, multi-disciplinary teams that collaborate through ORA with CORE and CDC in detecting, mitigating, and preventing additional exposures to contaminated foods, thereby preventing potential foodborne illness. RRTs were first funded by FDA in 2008, and are intended to minimize the time between agency notification of a human or animal food contamination event and implementation of effective control measures.^4,5 Today, 24 states maintain RRTs, with 21 receiving over $5 million in FDA support annually and three participating in the program voluntarily.⁶ RRTs have responded to hundreds of local and interstate incidents, including traditional foodborne illness outbreaks, acts of intentional food adulteration, and natural disasters, with the intention to limit impacts on the food supply and public health.⁶ FDA partners with RRTs to harness the unique expertise possessed by state food safety professionals, serving as an example of a fully integrated food safety system.

The Produce Safety Network. The finalization of the Produce Safety Rule in 2015 led FDA to build the Produce Safety Network (PSN) with specialists from FDA's Center for Food Safety and Applied Nutrition (CFSAN) and ORA to further capitalize on expertise across the agency.⁷ ORA and CFSAN PSN staff collaborate with CORE on traceback and record collection during outbreak investigations linked to produce commodities and conduct on-farm investigations. With the establishment of PSN, CORE now has consistent access to a high level of experience and expertise from produce safety specialists. Since its inception, the PSN has been steadfastly engaged with CORE and has provided investigative breakthroughs in outbreaks linked to melons and hydroponically produced leafy greens in 2020.^8,9

“Application of whole genome sequencing during CORE outbreak response activities has enhanced cluster detection, hypothesis development, and aided in the formulation of traceback theories.”

Whole Genome Sequencing. The use of new technologies during outbreak investigations has also led to significant breakthroughs. Such was the case with whole genome sequencing (WGS) and FDA's GenomeTrakr, which is a decade-old distributed network of both domestic and international public health and academic laboratories that utilize WGS to identify pathogens collected primarily from food and environmental sources.¹⁰ CDC's PulseNet is another critical database rounding out the foodborne pathogen surveillance network, and predominantly handles the sequencing of U.S. clinical isolates from public health labs. PulseNet WGS surveillance of Listeria monocytogenes began in 2013.^10,11

Data from both GenomeTrakr and PulseNet are deposited to the Pathogen Detection Project at the National Center for Biotechnology Information (NCBI), which also includes direct submissions from industry, researchers, and others. Contributors to these databases can see how their new isolates are related to the real-time foodborne pathogen surveillance program established in the U.S. and a few other countries. Compared to previous techniques, WGS can detect more illness clusters and those consisting of a smaller number of ill individuals.¹² The causal source of listeriosis outbreaks was also more often identified when a combination of WGS, epidemiologic, and traceback data was used during investigations as compared to previous laboratory techniques combined with established epidemiologic and traceback methods.¹³

WGS has become the standard tool for PulseNet surveillance and cluster detection of L. monocytogenes, as well as other prominent foodborne bacterial pathogens, such as Salmonella and Shiga toxin-producing Escherichia coli. For example, during a series of Salmonella outbreaks linked to papaya between 2017 and 2019, WGS helped decipher which isolates were genetically related and, therefore, more likely related to a single contamination source.¹⁴ Additionally, WGS and papaya sampling at import enhanced the strength of evidence between papaya and illnesses. Ultimately, application of WGS during CORE outbreak response activities has enhanced cluster detection, hypothesis development, and aided in the formulation of traceback theories.¹⁵

Sample-Initiated Retrospective Outbreak Investigations. CORE has developed a process to address early linkages between human and non-human isolates that may indicate emerging outbreaks. Specifically, using WGS, genetic similarity between a food or environmental sample, even those collected and analyzed prior to WGS, and clinical isolates can trigger a process referred to as a sample-initiated retrospective outbreak investigation (SIROI).¹⁶ Epidemiologic and traceback investigations can then be initiated to support the WGS linkage, which may lead to earlier firm or product action, thereby protecting public health before a larger outbreak occurs.¹⁶

A recent SIROI in 2021 involved Salmonella Weltevreden isolates collected from imported frozen shrimp approximately one month before genetically related clinical samples. Of the six ill people with available information, five reported eating shrimp, and four provided purchase details. An import alert was issued for shrimp from a single firm in India, and frozen cooked shrimp from the same firm was recalled.¹⁷ Another SIROI in 2022 involved historical peanut butter isolates and environmental swabs, some of which were collected more than a decade prior to an outbreak of Salmonella Senftenberg illnesses. Of the 21 illnesses investigated, 13 ill persons provided information about foods they consumed, and all reported consuming Brand A peanut butter. Within approximately one month of detecting the SIROI, regulatory actions including a recall, public notices, and warnings were issued.¹⁸

International Collaborations. FDA has established partnerships with international collaborators to streamline the flow of critical outbreak response information. FDA is part of the World Health Organization’s International Food Safety Authorities Network (INFOSAN), which disseminates important global food safety information and helps the international public health community prevent and respond to acute public health risks that have the potential to cross borders.

An example of FDA CORE's engagement with INFOSAN was during the 2016–2020 multinational outbreak of Listeria monocytogenes infections linked to enoki mushrooms imported from the Republic of Korea, where CORE shared critical information regarding the outbreak that helped stave off additional illnesses due to dissemination of the implicated vehicle in the international marketplace. This outbreak also serves as an example of how communication between regulatory agencies in the U.S. and Canada allowed each country to make informed decisions regarding sampling and regulatory actions. These arrangements complement existing Confidentiality Commitments, which prioritize information exchange during recalls/outbreaks and food-related emergencies to maximize consumer protection.¹⁹

Another example of international collaboration is the FDA-SENASICA-Cofepris Food Safety Partnership (FSP), which was established in September 2020 between FDA and Mexico's National Service of Agro-Alimentary Health, Safety, and Quality (SENASICA) and the Federal Commission for Protection against Sanitary Risk (Cofepris). The goal of this partnership is to prevent foodborne illnesses using modern, preventive practices based on technical and scientific evidence, health surveillance, and verification measures.²⁰

Other examples of FDA global partnership include INFOSAN and its partner, the Food and Agriculture Organization of the United Nations (FAO). INFOSAN facilitates the rapid exchange of information across borders and between members, during hundreds of food safety events, as an essential component for achieving global health security. CORE Signals is also engaged in multiple international partnerships with the UK and the EU to help improve international genomic data-sharing (an international surveillance priority) and collaborations during outbreak investigations.

Dedicated Communications Team. In 2019, CORE created a dedicated, embedded Communications Team to monitor the status of outbreak investigations and work with federal and state partners to determine when public communications are needed. FDA will warn the public when an outbreak is ongoing, when a specific product has been identified that is a risk to consumers, and when there is actionable advice to provide.

The average reading time on a CORE webpage is 2–4 minutes, indicating that readers are spending time reading outbreak advisories. These advisories highlight details on implicated products and any relevant recalls, the number and location of illnesses, a description of symptoms, an explanation of risk, and instructions for consumers and industry (e.g., throw away or return the product). Outbreak advisories are developed in collaboration with stakeholders and are disseminated via FDA's website, e-mail updates, and FDA social media channels. State and local partners help disseminate the messaging. The number of pageviews for outbreak advisories can range widely, from less than 10,000 to over 1 million; the most viewed outbreak advisory page in 2022 was "Outbreak Investigation of Salmonella: Peanut Butter (May 2022)," with a total of 2.176 million pageviews.¹⁸

CORE Investigation Table. The CORE Investigation Table (CIT) was launched in November 2020 to further increase transparency and early communication for foodborne illness outbreaks. The CIT shares information on FDA foodborne illness outbreak investigations, even during the initial stages. These incidents are typically added as soon as FDA begins its response to the outbreak to give consumers awareness of developing multistate outbreaks occurring across the U.S. Once investigation activities end, the CORE Communications Team "closes" the outbreak on the CIT, and when applicable, updates the outbreak advisory. In rare circumstances where CORE confirms the vehicle after the active investigation is over, CORE shares information about the vehicle and explains that although the vehicle has been confirmed, it is no longer on the market and the public does not need to take any action. In 2022, the total number of pageviews for the CIT was estimated at around 180,000, averaging approximately 15,000 total pageviews per month.

“To support end-to-end traceability for certain foods, FDA has recently defined additional recordkeeping requirements for foods on the Food Traceability List in the final Food Traceability Rule.”

Recent Integral Regulations and Food Safety Initiatives

Traceback Investigation Improvements. Historically, FDA has encountered numerous challenges during traceback investigations including limited epidemiologic information, difficulty obtaining product records, and insufficient data-tracing across supply chains. These challenges have highlighted gaps in the availability and standardization of data, as well as regulatory coverage for farms and restaurants, which have hindered CORE's traceback investigations. However, to support end-to-end traceability for certain foods, FDA has recently defined additional recordkeeping requirements for foods on the Food Traceability List (FTL) in the final rule Requirements for Additional Traceability Records for Certain Foods (Food Traceability Rule), which requires compliance by January 20, 2026.²¹ This new regulation will enable FDA to effectively trace the movement of food products and ingredients on the FTL across supply chains and better inform future CORE traceback investigations.

Foodborne Outbreak Response Improvement Plan. FDA's New Era of Smarter Food Safety blueprint, announced in July 2020, established goals to enhance product traceability through the food supply and called for improved predictive analytics, quicker and more rapid response to outbreaks, a way to address new business models, reduced contamination of food, and the development of a stronger food safety system.^22,23 An accomplishment of the New Era initiative is FDA's Foodborne Outbreak Response Improvement Plan (FORIP), which is focused on enhancing the speed, effectiveness, coordination, and communications of outbreak investigations.²⁴ To address these goals, CORE has revised traceback requests to encourage industry to provide information in a digital format. In some situations, the Food Traceability Rule will allow FDA to request that records be provided in an electronic, sortable spreadsheet. Technology-enabled traceability often narrows the scope of traceback requests and increases CORE's efficiency in identifying and extracting the data elements necessary to further outbreak investigations.

CORE Support of FDA Prevention Efforts

Once outbreak response activities are completed, stakeholders seek answers to important questions, such as, "How can we prevent this outbreak from happening again?" These questions guide the missions of the OE and OA Teams, who work in collaboration with FDA stakeholders, state and local regulatory partners, the CDC, and the U.S. Department of Agriculture (USDA), to examine all aspects of an outbreak and recommend preventive measures. Here, we shed light on the post-outbreak phase to support FDA foodborne illness outbreak prevention efforts.

The CORE Outbreak Evaluation Team. The CORE OE Team assesses historical outbreak data related to various pathogen-commodity pairs to improve FDA's outbreak coordination and support prevention efforts. The OE Team analyzes and shares historical data with internal and external stakeholders, which are then used to support prevention activities such as guidance for industry, consumer assessments, outbreak investigation reports, and surveillance assignments.

One critical function of the OE Team is to produce internal reports on historical outbreaks linked to pathogen-commodity pairs of concern. The aim of these reports is to identify trends and generate proposed actions for prevention efforts based on analysis of investigational data and information. Potential underlying causes of repeat outbreaks and potential preventive actions are shared with FDA program offices to inform FDA decision-making. The OE Team also provides expertise during the response phase. For example, at the beginning of an outbreak investigation, a point of contact (POC) from the OE Team provides the involved RT with an overview of historical outbreak information relevant to the pathogen-commodity pair of interest. The OE Team POC monitors outbreak response activities and shares relevant historical information as investigations unfold. Although most of the information the OE Team shares is targeted within FDA, notable research findings are also shared by the OE Team at scientific meetings.

The CORE Outbreak Analytics Team. The CORE OA Team was established in 2019 to conduct post-outbreak activities intended to anticipate, address, and learn from past outbreaks with the aim of reducing the frequency and impact of future outbreaks. Primary OA Team functions include the following: conducting statistical analyses on outbreak data; communicating outbreak findings and research with the food safety community through publications; contributing expertise through multi-agency collaborations such as the Interagency Food Safety Analytics Collaboration²⁵ and Foodborne Diseases Active Surveillance Network (FoodNet);²⁶ and providing input on future FDA sampling and inspection strategies by analyzing various data sources related to novel and repeat outbreaks.

An essential role of the OA Team is to lead or guide CORE's efforts in sharing outbreak investigation findings and prevention efforts through publications, conferences, and stakeholder meetings, as most CORE staff members function in an emergency response capacity. Publication projects include articles that showcase foodborne outbreak response efforts or that employ analytical tools to highlight patterns that may lead to adverse public health events. In 2022 , CORE produced a total of 17 publications, which tripled previous years' publishing efforts (an average of five publications per calendar year between 2012 and 2020).²⁷ Through collaboration on publication projects, the OA Team has further strengthened relationships with stakeholders, both internally within FDA and externally. These efforts can inform practical, evidence-based foodborne outbreak prevention strategies and demonstrate CORE's ability to use scientific insight to advance FDA's public health mission.

“As events in one state, region, or foreign country can have public health and economic impact across borders, foodborne outbreak investigations require engagement from all involved public health agencies to be successful.”

Future Directions and Challenges

Imported Foods and International Information Sharing. Approximately 19 percent of food in the U.S. is imported; consequently, according to Gould et al., there has been a corresponding increase in outbreaks attributed to imported foods between 1973 and 2014.²⁸ As events in one state, region, or foreign country can have public health and economic impact across borders, foodborne outbreak investigations require engagement from all involved public health agencies to be successful. One such example of this collaboration is the sharing of WGS data with international partners, which can decrease the time required to resolve outbreaks and reduce the public health burden of foodborne illness.²⁹ With the rapid development of epidemiologic, laboratory, and traceback information, CORE routinely serves as a hub to share data, enabling partners to take the appropriate regulatory and public health actions.¹⁴

Reoccurring, Emerging, and Persisting Genetic Bacterial Strains. CORE has collaborated with CDC and USDA's Food Safety and Inspection Service (FSIS) to develop and implement the concept of reoccurring, emerging, and persisting (REP) genetic strains.³⁰ These are specific bacterial strains of concern that warrant some type of heightened or alternative surveillance or investigation because of their unique presentation of illness in the U.S. population. Some REP strains have similar geographic specificity or similar commodity associations. Although heightened surveillance of REP strains and tracking repeat pathogen-commodity pairs can aid outbreak hypothesis development, prevention of a reoccurring pathogen in a specific geographic area or commodity is challenging. The use of genetic ancestry may help identify how a pathogen transverses environments or supply chains, and this information may prevent the conditions for introduction of future contamination events.

Smaller Outbreaks. With the implementation of WGS as the primary subtyping method at the state and federal levels, illness clusters can be detected sooner and with a smaller number of illnesses, which allows for earlier response to outbreaks. Smaller outbreaks may impact the number of ill people whose exposure history can be utilized in a traceback investigation. Genetically related isolates and the broader genetic sequencing tree may also provide clues for traceback and source attribution. Without traceback clarity, FDA and investigational partners may need additional sampling within the supply chain or at farms to identify a source. Ultimately, additional investigational resources will be required to prevent outbreaks from expanding.

Atypical Pathogen-Commodity Pairs. Through the years, CORE has investigated a variety of atypical pathogen-commodity pairs that emerge due to changing food production practices and consumer behaviors, which create opportunities for contamination in the food supply. The identification of these foods, along with causes and routes of contamination, enable CORE and investigational partners to target outbreak response and prevention strategies. Examples of past outbreaks attributed to atypical pathogen-commodity pairs include salmonellosis outbreaks linked to organic sprouted chia seed powder in 2014, powdered meal replacement containing a Moringa leaf powder ingredient in 2016, and products reported to contain Kratom in 2018; Escherichia coli O157:H7 infections linked to soy nut butter in 2017; and Vibrio parahaemolyticus infections linked to crab meat in 2018.³¹

Culture-Independent Diagnostic Tests. Culture-independent diagnostic tests (CIDT) are lab tests that can detect pathogens in patient samples, specifically by detecting the presence of a gene or antigen associated with a specific pathogen.^32,33 Numerous benefits are associated with the use of these types of tests, including faster patient diagnosis and reduced costs. However, as these tests do not require culturing of bacteria, they do not produce the isolates necessary for WGS analysis and antibiotic resistance testing. The development of genetic techniques for strain identification and characterization of antibiotic resistance that are not dependent on bacterial isolates is one potential future solution to this increasingly difficult challenge.³²

Metagenomics and Foodborne Outbreaks. Metagenomics is a technology that offers considerable promise for outbreak investigation, particularly as CIDTs limit the availability of clinical isolates. Specifically, metagenomic techniques capture genetic information on all organisms in a sample, rather than just those that are culturable.³⁴ Methods that are under development for microorganisms of public health interest may accelerate both detection and characterization of foodborne pathogens.³⁵ Direct analysis of clinical samples via metagenomic techniques could permit one assay to characterize pathogens, which would mitigate the negative impact of widespread CIDT adoption and potentially improve outbreak detection and response.³⁶ As metagenomic techniques are unable to distinguish between live, pathogenic bacteria and residual genetic material, viability discrimination presents a greater challenge for environmental and food samples, as opposed to clinical samples.

Food Product Traceability. The Food Traceability Rule will lead to significant benefits for public health and the food industry, including enhanced FDA and industry traceback efficiency, which will increase the likelihood and speed with which the sources of contaminated food products are identified. Beyond faster traceback, standardization of key data elements used in traceability will likely increase the precision and expediency of recalls, reduce costs and resources used by FDA and industry for traceback investigations, improve supply chain management and inventory control, and reduce food waste. However, because the Food Traceability Rule is limited to food products included on the FTL (as required by statute), information collection and investigational challenges will likely remain for those food items not covered by the rule.

Retail and Foodservice Technology. The use of technology and the smaller information gap between the retailer or food establishment and the consumer can also speed up traceback investigations.³⁷ As consumers have increasing access to more detailed electronic data on their food purchases, traceback investigations could start sooner and with narrowed product information. The way consumers obtain their food is also changing as more grocery and food delivery services become popular. For example, outbreak cases may be able to provide documentation and easily share recent purchases if they utilize a grocery store loyalty/discount card number, are able to obtain detailed consumer purchase data through their credit card or the retailer's website, or order groceries/meals via a grocery or delivery application/website. It is yet to be determined how these changes in consumer behavior will affect the way in which traceback investigations are initiated. FDA continues to explore how different technologies can improve traceability in the food supply system.³⁷

“Each step in the 'rings of defense' must be used consciously and with proper consideration, as it may be obvious what caused the noncompliance, and its resolution may be straightforward, simple, and not costly.”

Takeaway

Since CORE was established in 2011, CORE staff has engaged in surveillance activities, coordinated response efforts to foodborne outbreaks, coordinated regulatory activities, and warned the public to avoid implicated foods. CORE's dedicated staff has been the driving force behind its ability to adapt to an ever-changing foodborne illness outbreak investigation landscape.

Although technologies improve and novel pathogen-commodity pairs arise, CORE is built on the principles of flexibility, resilience, and collaboration. As a result, CORE continues to evolve, based on lessons learned from past outbreaks, and find innovative solutions to protect public health in the future.

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