Food Safety And Inspection Service Research Articles

Recall characteristics and food safety process control

The Food Safety and Inspection Service (FSIS) initiated 1,073 recalls of meat and poultry products that could cause severe illness or death over 2000–2019. These recalls led to substantial drops in demand that vary by the characteristics of the recall (Zhou and Liu, 2023) and incentivized firms to invest in food safety (Ollinger and Houser, 2020). Following Zhou and Liu (2023) and Ollinger and Houser (2020), this paper examines differences in food safety process control for establishments with different recall characteristics and contrasts that performance with establishments without recalls. Results show that (1) Salmonella share relative to an establishment’s own mean Salmonella share outperforms Salmonella share alone in estimating the likelihood of a recall, (2) 27 percent rather than 12 percent of establishments would have failed to meet the Salmonella standard if a proposed but not yet mandated more stringent standard had been in effect, and (3) most establishments return to normal operating conditions after a recall, but establishments with multiple recalls struggle to regain control of food safety, suggesting they may benefit from an audit of their food safety systems by FSIS or an auditor.

A Survey of the Levels of Selected Metals in U.S. Meat, Poultry, and Siluriformes Fish Samples Taken at Slaughter and Retail, 2017–2022

The U.S. Department of Agriculture (USDA) Food Safety and Inspection Service (FSIS) conducts surveillance of metallic elements in U.S. meat, poultry, and Siluriformes fish samples collected immediately postmortem as part of its National Residue Program (NRP). From 2017 to 2022, 13,966 samples were analyzed under the NRP. The Federal Emergency Response Network (FERN) Cooperative Agreement Program (CAP) tests meat, poultry, and Siluriformes fish products collected at retail in the United States for metals. From 2018 to 2022, 2,902 samples were analyzed by FERN CAP laboratories. Meat and poultry samples collected by FSIS show that most metals were not detected at all or were detected infrequently. Meat is a rich source of iron and zinc, and iron was detected in 22% (1,255/5,623) and zinc was detected in 48% (2,742/5,676) of meat and poultry samples, respectively. The percentage of samples testing positive for manganese, molybdenum, lead, and cadmium were higher in the FERN CAP retail samples than in FSIS samples. Expected human exposure from average levels of lead and cadmium found in meat and poultry was compared to toxicological reference values and was not found to exceed these values. Detections of arsenic and mercury were found more often in Siluriformes fish samples (2017–2022) than in terrestrial animals. Trace amounts of arsenic and mercury were detected in 8% and 4% of Siluriformes samples, respectively, but were not detected at levels that raise concern. On the whole, both the FSIS and FERN CAP datasets provide reassuring evidence of the safety of the FSIS-regulated food supply with regard to the studied elements.

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.

Prevalence and Antibiotic Resistance of Salmonella and Campylobacter Isolates from Raw Chicken Breasts in Retail Markets in the United States and Comparison to Data from the Plant Level

Chicken is the most popular meat in the United States, and consumers may be exposed to multidrug resistant Salmonella and Campylobacter through consumption of retail chicken breasts. This study aimed to (i) determine the percentage of raw, packaged, retail chicken breasts from 27 metro areas that tested positive for Salmonella and Campylobacter; (ii) investigate the antibiotic susceptibility profiles of a subset of the isolates; and (iii) compare the Salmonella prevalence data to establishment level Salmonella categorization data published by the U.S. Department of Agriculture (USDA). USDA Food Safety and Inspection Service (FSIS) Microbiology Laboratory Guidebook (MLG) methodology was used to isolate and identify Salmonella (n = 672), Campylobacter (n = 499) from 400 g samples. National Antimicrobial Resistance Monitoring System (NARMS) methodology was followed for antimicrobial susceptibility testing of Salmonella (n = 52) and Campylobacter (n = 16) isolates. Salmonella was found in 8.6% of samples and Campylobacter in 4.2%. Having a 3 rating in USDA's Salmonella Categorization of Individual Establishments for chicken parts was predictive of having a higher Salmonella percent positive in our data set (p ≤ 0.05). A total of 73.1% of Salmonella isolates, and 62.5% of Campylobacter isolates were resistant to ≥one class of antibiotics, with 48.1% of Salmonella isolates resistant to ≥three classes. Current results support interventions that take a 'farm-to-fork' approach with distinction by poultry types and parts as well as serovars, to lower antibiotic resistant Salmonella infections in humans due to poultry. Highlights:Salmonella was found in 8.6% and Campylobacter in 4.2% of chicken breasts tested; A 3 rating by USDA was predictive of a higher Salmonella percent positive; 48.1% of Salmonella isolates were resistant to 3 or more classes of antibiotics.

Use of Water in Animal Production, Slaughter, and Processing

Water is an essential part of food animal processing, and current processing practices use large volumes of water. Due to climate change, the food industry's access to clean and inexpensive water is increasingly a challenge. The Food Safety and Inspection Service (FSIS) seeks evaluation by the National Advisory Committee on Microbiological Criteria for Food (NACMCF) to facilitate the safe reuse of sources of water in order to reduce water consumption. There should be more collaborations among stakeholders (e.g., industry, academia, government) to collect missing information on water usage and opportunities for reuse. A complete understanding of energy use and plant infrastructure limitations is necessary to effectively understand all opportunities for water conservation and recycling. Characterization of microbial and chemical contaminants in water is a very large topic that requires extensive work. There are quality standards for potable water but not for the recycled water from different processing states, and different water treatment systems. A uniform standard for, and federal regulation of, the quality of reused/recycled water in FSIS-regulated facilities is needed. Standard water analysis methods are available, well-developed, and reliable. Initial monitoring of alternatively sourced water should be extensive, while ongoing performance monitoring should be in real-time and focus on measuring indicators (refer to Glossary). Water for non-food contact uses will require monitoring of fewer parameters. Some water conservation strategies have been published for fish processing establishments; however, economic and other incentives to incorporate conservation practices or recycling technologies do not exist. Companies should develop emergency programs to manage natural disasters, such as flooding.

Comparison and validation of the QuEChERSER mega-method for determination of per- and polyfluoroalkyl substances in foods by liquid chromatography with high-resolution and triple quadrupole mass spectrometry

Instances of food contamination with per- and polyfluoroalkyl substances (PFAS) continue to occur globally, but sample preparation and analytical methods are quite limited and often monitor for a small percentage of known PFAS. This study aimed to evaluate, validate, and compare performance of two instruments with the recently developed “quick, easy, cheap, effective, rugged, safe, efficient, and robust” (QuEChERSER) sample preparation mega-method – a method developed to monitor chemicals over a broad range of physicochemical properties. Initial evaluation of the QuEChERSER mega-method for determination of PFAS in food demonstrated recoveries, matrix interferences, and co-extractive removal comparable to (or better than) US Food and Drug Administration (FDA) and USDA Food Safety and Inspection Service (FSIS) methods. Subsequent validation of QuEChERSER in beef, catfish, chicken, pork, liquid eggs, and powdered eggs on a high-resolution mass spectrometer achieved acceptable recoveries (70–120%) and precision (RSDs ≤20%) for all 33 target analytes at the 1 and 5 ng g−1 levels and 67–88% of analytes at the 0.1 ng g−1 level, depending on the matrix. Additional validation was performed by tandem mass spectrometry on a triple quadrupole instrument. This approach provided no non-detects and better recoveries at the 0.1 ng g−1 level than the HRMS method but exhibited more variability at 1 and 5 ng g−1 spiking levels. Analysis of NIST SRMs 1946 and 1947 gave accuracies of 70–117%. These results demonstrate the capability of combining PFAS analysis with a mega-method previously validated for 350 analytes, while collecting non-target data for future retrospective analysis of emerging alternatives with a high-resolution mass spectrometry method.

Multidrug resistance and virulence genes carried by mobile genomic elements in Salmonella enterica isolated from live food animals, processed, and retail meat in North Carolina, 2018–2019

An estimated 1000,000 domestic salmonellosis cases are attributed to food as a vehicle of exposure. Among Food Safety and Inspection Service (FSIS)-regulated products, approximately 360,000 salmonellosis cases are associated with consumption of meat, poultry, and egg products. Salmonella vaccination programs instituted in U.S. poultry, cattle, and swine production have effectively reduced the prevalence of common Salmonella enterica serotypes Typhimurium, Enteritidis, Choleraesuis (swine), and Dublin (cattle) in the past several years, with some evidence of cross-immunity to other serovars. This study investigated S. enterica (n = 741) from live food animals, meat carcasses at production, and retail meat in North Carolina collected January 2018 to December 2019. Whole-genome sequencing (WGS) and bioinformatics were used to molecularly characterize and compare AMR profiles, virulence, and phylogeny of Salmonella at three stages of food processing. Multidrug-resistant (MDR) plasmids identified also contained the integrase recombinase virulence factor int associated with mobile integrons, qacE conferred quaternary ammonia resistance, and diverse AMR profiles. MDR Plasmid IncFIB(K)_1_Kpn3_JN233704, with virulence factor int had 51 different AMR profiles within poultry S. enterica Infantis isolates. Plasmid-mediated virulence factors also appear to provide a fitness advantage, as the dominant S. enterica serotype Kentucky in chicken retail meat held the greatest diversity of plasmid-mediated colicin virulence genes which are often upregulated by environmental stressors and confer a competitive advantage. Mobile genetic element recombination is increasing pathogen fitness in the food chain through the dissemination of virulence factors and resistance genes to clinically important antibiotics, posing a significant threat to human health.

Consequences of Implementing Neutralizing Buffered Peptone Water in Commercial Poultry Processing on the Microbiota of Whole Bird Carcass Rinses and the Subsequent Microbiological Analyses.

In 2016, the United States Department of Agriculture (USDA) Food Safety and Inspection Service (FSIS) established guidelines which modified the Buffered Peptone Water (BPW) rinsate material to include additional compounds that would better neutralize residual processing aids and allow for better recovery of sublethal injured Salmonella spp. cells. While the added compounds improved the recovery of Salmonella spp., specific data to understand how the new rinse agent, neutralizing Buffered Peptone Water (nBPW), impacts the recovery of other microorganisms such as Campylobacter spp. and indicator microorganisms are lacking. Therefore, this study evaluated the impact of rinse solutions (BPW or nBPW) used in Whole Bird Carcass rinsate (WBCR) collections on the subsequent microbiome and downstream culturing methodologies. Carcasses exiting a finishing chiller were rinsed in 400 ml of BPW or nBPW. Resulting rinsates were analyzed for Enterobacteriaceae (EB), Salmonella, and Campylobacter spp. prevalence and total aerobic bacteria (APC) and EB load. The 16S rDNA of the rinsates and the matrices collected from applied microbiological analyses were sequenced on an Illumina MiSeq®. Log10-transformed counts were analyzed in JMP 15 using ANOVA with means separated using Tukey’s HSD, and prevalence data were analyzed using Pearson’s χ2 (P ≤ 0.05). Diversity and microbiota compositions (ANCOM) were analyzed in QIIME 2.2019.7 (P ≤ 0.05; Q ≤ 0.05). There was an effect of rinsate type on the APC load and Campylobacter spp. prevalence (P < 0.05), but not the quantity or prevalence of EB or Salmonella spp. prevalence. There were differences between the microbial diversity of the two rinsate types and downstream analyses (P < 0.05). Additionally, several taxa, including Streptococcus, Lactobacillus, Aeromonas, Acinetobacter, Clostridium, Enterococcaceae, Burkholderiaceae, and Staphylococcaceae, were differentially abundant in paired populations. Therefore, the rinse buffer used in a WBCR collection causes proportional shifts in the microbiota, which can lead to differences in results obtained from cultured microbial populations.

A quantitative risk metric to support individual sanitary measure reviews in international trade

In order for the United States Department of Agriculture's (USDA) Food Safety and Inspection Service (FSIS) to make an equivalence determination for a foreign meat, poultry or egg products inspection procedure that differs from FSIS inspection procedures (an Individual Sanitary Measure or ISM), a country must demonstrate objectively that its food safety inspection system provides the same level of public health protection as the FSIS inspection system. To evaluate microbiological testing data that such countries may submit to this end, we present a possible risk metric to inform FSIS's assessment of whether products produced under an alternative inspection system in another country pose no greater consumer risk of foodborne illness than products produced under FSIS inspection. This metric requires evaluation of prevalence estimates of pathogen occurrence in products for the foreign country and the U.S. and determining what constitutes an unacceptable deviance of another country's prevalence from the U.S. prevalence, i.e., the margin of equivalence. We define the margin of equivalence as a multiple of the standard error of the U.S. prevalence estimate. Minimizing the margin of equivalence ensures the maximum public health protection for U.S. consumers, but an optimum choice must also avoid undue burden for quantitative data from alternative inspection systems in the foreign country. Across a wide range of U.S. prevalence levels and sample sizes, we determine margin of equivalence values that provide high confidence in conclusions as to whether or not the country's product poses no greater risk of foodborne illness from microbiological pathogens. These margins of equivalence can be used to inform FSIS's equivalence determination for an ISM request from a foreign country. Illustrative examples are used to support this definition of margin of equivalence.This approach is consistent with the World Trade Organization's concept of risk equivalence and is transparent and practical to apply in situations when FSIS makes an equivalence determination for an ISM requested by a foreign country.

Process Humidity Affects Salmonella Lethality at the Surface and Core of Impingement-Cooked Meat and Poultry Products

Recent revisions to U.S. Department of Agriculture, Food Safety and Inspection Service (FSIS) compliance and safe harbor guidelines for ready-to-eat meat and poultry products addressed process humidity requirements. Given the lack of prior data for impingement-cooked products, the present study was conducted to evaluate the impact of process humidity on Salmonella lethality at the product core and surface and compliance of the results with FSIS lethality performance standards. Whole muscle beef strips, ground beef patties, whole muscle chicken breast fillets, and breaded ground chicken patties were inoculated with an eight-serovar cocktail of Salmonella. Beef and chicken samples were cooked in a pilot-scale moist-air impingement oven to a core temperature of 70.0 and 72.8°C, respectively, immediately quenched in liquid nitrogen, and dissected to obtain core and surface samples. Variables included oven temperature (218 and 232°C), air velocity (0.7 and 2.8 m/s), and oven humidity (0.7, 15, 30, or 70% moisture by volume [%, v/v]). Additional treatments were performed to examine the impact of supplemental critical control processes such as increased endpoint temperature, postoven carryover time, and pre- or postoven steam treatments. Salmonella reductions of >7 log units were reliably achieved in chicken patties regardless of the processing variables; however, none of the treatments reliably ensured >6.5-log reductions of Salmonella in ground beef. A majority of whole-muscle samples failed to meet the required performance lethality when processed at 0.7% (v/v) humidity; however, Salmonella inactivation was significantly improved (P < 0.05) at oven humidities of ≥30% (v/v). Dry oven conditions achieved greater Salmonella lethality at the core than at the surface for multiple products (P < 0.05). The efficacies of minimal and supplemental critical controls were dependent on product, process, and humidity (P < 0.05). Overall, process humidity and product variability should be considered in regulatory requirements and process validations.

Initial Reports of Foodborne Illness Drive More Public Attention Than Do Food Recall Announcements

Recall announcements by the U.S. Food and Drug Administration (FDA) and Food Safety and Inspection Service (FSIS) are important communication tools. Nonetheless, previous studies revealed that the effects of recalls on consumer demand are small. Social media analytics can provide insights into public awareness of food safety-related incidents. This study included social listening data to analyze how the public, in social and online media spaces, responds to, interacts with, and references food safety recalls and/or initial announcements of foodborne illness outbreaks as reported by the Centers for Disease Control and Prevention (CDC). Analysis results suggest that mentions quantified in the social and online media searches moved closer in step with the CDC's initial reports of foodborne illness outbreaks than did FDA and FSIS recall announcements. Issuance of recalls may not be a popular source of food risk information in the social media space compared with reactions to the CDC's initial illness reports. This relative popularity reflects people more often sharing or posting about illness risk regardless of whether a recall occurs, suggesting that recall announcements by the FDA and FSIS may not induce changes in consumers' behavior, whereas initial illness reports by the CDC may. Although recalls by the FDA and FSIS may not generate social media posts, their primary role is to take potentially unsafe food items off grocery shelves. Online media analytics provide policy makers with information to guide effective food risk communication; initial CDC reports drive immediate attention more than do FDA and FSIS recalls.

PhageDx™ E. coli O157:H7 Assay in Ground Beef Level 3 Modification to Add 375 g Beef Trim and New Method Procedure for 25 g Ground Beef: AOAC Performance Tested MethodSM 081601.

BackgroundThePhageDx™ E. coli O157:H7 Assay originally required a 5 h enrichment period and a 10 mL test sample for 25 g ground beef. The proposed method modifications seek to include beef trim (375 g) matrix and a new method procedure for 25 g ground beef comprised of 6–7 h enrichment and 1 mL test sample.ObjectiveTo validate the method modifications for PhageDx E. coli O157:H7 Assay to include beef trim (375 g) matrix and modify enrichment time and test sample size for 25 g ground beef.MethodFor both matrixes, pre-warmed tryptic soya broth (TSB; 42 ± 1°C) was added in a 3:1 (media:sample size) ratio, blended, and enriched for 9–10 h (beef trim, 375 g) or 6 h (ground beef, 25 g) at 42 ± 1°C. One milliliter samples were transferred to a microfuge tube, centrifuged, and the supernatant removed. The pellet was resuspended in 0.2 mL of TSB and phage reagent was added. Samples were incubated for 2 h at 37 ± 1°C. After infection, the sample was centrifuged, and 150 µl of the supernatant was transferred to a 96-well plate. Then, lysis buffer and luciferase substrate were added and the sample read on a luminometer to determine the presence or absence of E. coli O157:H7.ResultsNo significant differences were found between the PhageDx E. coli O157:H7 Assay method modifications and the U.S. Department of Agriculture Food Safety and Inspection Service (FSIS) Microbiology Laboratory Guidebook (MLG) reference method.ConclusionsThe independent study demonstrated that the PhageDx E. coli O157:H7 Assay method modifications meet the qualifications for Performance Tested Method SM status.HighlightsThe PhageDx E. coli O157:H7 Assay is a rapid detection method capable of detecting E. coli O157:H7 in 25 g ground beef and 375 g beef trim samples in as little as 8.5 h and 11.5 h total turn around time, respectively.

Validation of PhageDx™Salmonella Assay in Raw Ground Turkey and Powdered Infant Formula: AOAC Performance Tested MethodSM 121904.

BackgroundThe PhageDx™Salmonella Assay is based on the infection of Salmonella spp. by specific bacteriophages and expression of a luciferase reporter gene. Results are generated in as little as 9.5 h for raw ground turkey and 18.5 h for milk-based powdered infant formula (PIF).ObjectiveAn AOAC Performance Tested MethodsSM (PTM) study was conducted to validate the PhageDx Salmonella Assay for the detection of Salmonella in 25 g raw ground turkey and 100 g PIF test portions.MethodThe performance of the PhageDx Salmonella Assay was compared to that of the U.S. Department of Agriculture (USDA), Food Safety and Inspection Service (FSIS) Microbiology Laboratory Guidebook (MLG) 4.10 for raw ground turkey and the U.S. Food and Drug Administration (FDA) Bacteriological Analytical Manual (BAM) Chapter 5 for PIF. Inclusivity/exclusivity, product consistency and stability, and robustness testing were conducted.ResultsThere was no significant difference between the 25 g raw ground turkey and 100 g PIF PhageDx Salmonella Assay and the USDA/FSIS MLG 4.10 and FDA/BAM Chapter 5, respectively. The reporter bacteriophages were specific for Salmonella and infected 108 strains in inclusivity testing. They did not infect 30 non-Salmonella bacteria in exclusivity testing. Robustness testing showed that the method performed well with specific deviations from the standard protocol. Consistency and stability testing demonstrated that the recombinant phage gave consistent results across three production lots and was stable when stored under appropriate conditions for at least eight months.ConclusionsThe data collected in the validation study demonstrate that the PhageDx Salmonella Assay meets the qualifications for PTM status. HighlightsThe PhageDx Salmonella Assay is a rapid, specific, sensitive assay capable of detecting a wide range of Salmonella spp. with a significantly shorter turn around time than the USDA/FSIS and FDA reference methods.

Carriage and Gene Content Variability of the pESI-Like Plasmid Associated with Salmonella Infantis Recently Established in United States Poultry Production.

Salmonella Infantis carrying extended spectrum β-lactamase blaCTX-M-65 on a pESI-like megaplasmid has recently emerged in United States poultry. In order to determine the carriage rate and gene content variability of this plasmid in U.S. Salmonella Infantis, whole genome sequences of Salmonella isolates from humans and animals in the U.S. and internationally containing the pESI-like plasmid were analyzed. The U.S. Department of Agriculture Food Safety and Inspection Service (FSIS) identified 654 product sampling isolates containing pESI-like plasmids through hazard analysis and critical control point (HACCP) verification testing in 2017 and 2018. The Centers for Disease Control and Prevention identified 55 isolates with pESI-like plasmids in 2016–2018 through the National Antimicrobial Resistance Monitoring System. Approximately 49% of pESI-like plasmids from FSIS verification isolates and 71% from CDC NARMS contained blaCTX-M-65. Pan-plasmid genome analysis was also performed. All plasmids contained traN and more than 95% contained 172 other conserved genes; 61% contained blaCTX-M-65. In a hierarchical clustering analysis, some plasmids from U.S. animal sources clustered together and some plasmids from South America clustered together, possibly indicating multiple plasmid lineages. However, most plasmids contained similar genes regardless of origin. Carriage of the pESI-like plasmid in U.S. appears to be limited to Salmonella Infantis and carriage rates increased from 2017 to 2018.

Food Loss Waste in the United States Food Supply Chain: An Analysis of Its Functions, Oversight, and Recent Impacts from the Coronavirus Pandemic

Government oversight of the food supply chain consists of a complicated regulatory framework involving multiple executive branch agencies, congressional committees, and state governments. The agencies primarily involved with food safety issues are the Food and Drug Administration (FDA), the Food Safety and Inspection Service (FSIS), the US Department of Agriculture (USDA), the Environmental Protection Agency (EPA), and the National Marine Fisheries Service (NMFS). Although the above entities divide responsibility for different aspects of food safety and quality, according to a 2019 Government Accountability Office (GAO) report, the patchwork of statutes and regulations has led to “inconsistent oversight, ineffective coordination, and inefficient use of resources.”

Investigations of Possible Multistate Outbreaks of Salmonella, Shiga Toxin-Producing Escherichia coli, and Listeria monocytogenes Infections - United States, 2016.

Investigations of Possible Multistate Outbreaks of Salmonella, Shiga Toxin-Producing Escherichia coli, and Listeria monocytogenes Infections - United States, 2016.

Changes in Salmonella Contamination in Meat and Poultry Since the Introduction of the Pathogen Reduction and Hazard Analysis and Critical Control Point Rule

In 1996, the Food Safety and Inspection Service (FSIS) published its pathogen reduction and hazard analysis and critical control point (PR-HACCP) rule. The intention of this program was to reduce microbial contamination on meat, poultry, and egg products. The program was implemented in stages between January 1998 and January 2000, with sampling for Escherichia coli O157:H7 and/or Salmonella in large production establishments beginning in 1998. As the PR-HACCP program begins its third decade, it is reasonable to question whether there have been reductions in the frequency of pathogen-contaminated meat and poultry products reaching consumers. This study summarizes the results for over 650,000 samples collected by FSIS between 2000 and 2018 in slaughter and processing establishments across the United States and compares these results to the roughly 100,000 retail samples collected by the U.S. Food and Drug Administration between 2002 and 2017. The data demonstrate that there has been an overall reduction in the occurrence of Salmonella on meat and poultry products, but the direction and magnitude of change has not been consistent over time or across commodities. Although the available data do not support the identification of causal factors for the observed changes, a historical review of the timing of various factors and policy decisions generates potential hypotheses for the observed changes.

Occurrence of Listeria monocytogenes in Ready-to-Eat Meat and Poultry Product Verification Testing Samples from U.S. Department of Agriculture–Regulated Producing Establishments, 2005 through 2017

Ready-to-eat (RTE) meat and poultry product samples collected between 2005 and 2017 from RTE-producing establishments for the U.S. Department of Agriculture, Food Safety and Inspection Service (FSIS) ALLRTE/RTEPROD_RAND (random) and RTE001/RTEPROD_RISK (risk-based) sampling projects were tested for Listeria monocytogenes (Lm). Data for 45,897 ALLRTE/RTEPROD_RAND samples collected from 3,607 distinct establishments and 112,347 RTE001/RTEPROD_RISK samples collected from 3,283 distinct establishments were analyzed for the presence of Lm. These data were also analyzed based upon the percentages of establishments with positive samples, annual production volume, sanitation control alternatives, geographic location, and season or month of sample collection. Results revealed low occurrence of Lm-positive samples from the random and risk-based sampling projects, with 152 (0.33%) positive samples for ALLRTE/RTEPROD_RAND and 403 (0.36%) positive samples for RTE001/RTEPROD_RISK. The percentage of positive samples significantly decreased over time, from about 0.7% in 2005 and 2006 to about 0.2% in 2017 (P < 0.05). From 2005 to 2017, 3.9% of establishments sampled under the ALLRTE/RTEPROD_RAND sampling project had at least one Lm-positive sample. Similarly, 10.0% of establishments sampled under the RTE001/RTEPROD_RISK sampling project had at least one positive sample. Samples positive for Lm were found in all geographic regions in all months. Thus, in 13 years of RTE product sampling in FSIS-regulated establishments (2005 through 2017), <0.4% of samples were positive for Lm in both risk-based and random sampling projects. The low prevalence of Lm in these products suggests that the combination of FSIS policies and industry practices may be effective for controlling Lm contamination. Information obtained from these sampling projects is relevant to the ongoing prevention of foodborne Lm illnesses from RTE meat and poultry products.

The Oft Forgotten Part of Nutrition: Lessons from an Integrated Approach to Understand Consumer Food Safety Behaviors

Abstract Objectives A multi-year, integrated methods study showed comprehensive consumer food handling practices when preparing a meal, compared to prevalence of self-reported behaviors. Experimental conditions provided insights on the effectiveness of current and future food safety messages. Methods Demographically-diverse participants were recruited from various communities in one state. Year 1: Participants prepared raw turkey burgers in a simulated home kitchen. Half of participants viewed an educational video on thermometer use before meal preparation; the other half served as a control. Year 2: Participants who self-reported washing poultry prepared raw chicken products. Half of participants received mock social media messages about not washing poultry; the other half served as a control. Food handling behaviors were coded and compared to self-reported actions and attitudes towards food safety, collected via written surveys and in-depth interviews. Results At least one contributing factor to foodborne illness was examined during each observation; cross-contamination actions were always observed. Year 1: Over 60% (n = 383) of participants self-reported owning and using a food thermometer when cooking raw meat and poultry products; however, only 35% of unprompted participants measured final internal temperature with a food thermometer. Year 2: Nearly 25% (n = 300) of participants cross-contaminated a ready-to-eat side; over 50% cross-contaminated due to poor sink sanitation. Differences between self-reported and observed food safety behaviors were seen across participant groups. Lack of sufficient handwashing leading to bacterial cross-contamination was a notable secondary outcome. Conclusions Observations more accurately reflect consumer food handling behaviors and allow for targeted message development to decrease risk of foodborne illness through safe at-home food handling. Findings and messages are shared with health educators, news and social media outlets, and directly to consumers through various resources. Funding Sources This work was funded by the U.S. Department of Agriculture (USDA), Food Safety and Inspection Service (FSIS). All views expressed here are those of the authors and not necessarily of USDA FSIS. USDA is an equal opportunity provider, employer, and lender.

Associations Between Peaks of Foodborne Infections and Food Recalls

Abstract Objectives Food delivery and supply chains represent complex dynamic systems susceptible to pathogen introduction. However, seasonal infections are rarely compared with the timing of food recalls. Gaps between peak infections and recalls illustrate inefficient food inspection and monitoring. We use seasonality features (peak timing and amplitude) to examine associations between peaks of pathogen infectiousness and food recalls. Methods Monthly counts of 3 foodborne infections (Salmonella, Listeria, and Shiga toxin-producing E.coli) were abstracted from the CDC's public database, FoodNet Fast, for 10 representative states (CA, CO, CT, GA, MD, MN, NM, NY, OR, TN) from 1996–2018. We applied Negative Binomial harmonic regression models with the δ-method to derive peak timing and amplitude estimates (with confidence intervals). Food recalls were extracted using the United States Department of Agriculture's (USDA) Food Safety and Inspection Service (FSIS) Recall Case Archive. We extracted recall dates and durations for each infection in each state. We compared lagged associations between infection peaks and recall dates using Spearman correlations. Results Seasonal peaks of Salmonella and Shiga Toxin-producing E.Coli (STEC) are tightly clustered (7.79 [7.71, 7.87], and 7.80 [7.65, 7.95], respectively) while Listeria falls later in August (8.35 [8.05, 8.65]). Peak timing estimates were positively synchronized between New York and Connecticut for Listeria (ρ = 0.780, P = 0.001), and between Georgia and Tennessee for STEC (ρ = 0.666, P = 0.009) indicating possible regional hotspots. From 1996–2018, inspection recalls tended to lag behind peaks of confirmed infections for all infections by 1–2 months, with most recalls occurring during August and September annually. Conclusions Measurements of infection seasonality coupled with food recall information shows lagged associations between population infectiousness and supply chain reporting. This suggests the need for improved food inspection scheduling and monitoring to minimize fiscal and food waste losses. Funding Sources The Office of the Director of National Intelligence (ODNI), Intelligence Advanced Research Projects Activity (IARPA), via 2017–17,072,100,002.