Observed Potential Cross-Contamination in Retail Delicatessens.

ABSTRACT: Listeria monocytogenes is a persistent public health concern in the United States and is the third leading cause of death from foodborne illness. Cross-contamination of L. monocytogenes (between contaminated and uncontaminated equipment, food, and hands) is common in delicatessens and likely plays a role in the foodborne illness associated with retail deli meats. In 2012, the Centers for Disease Control and Prevention's Environmental Health Specialists Network conducted a study to describe deli characteristics related to cross-contamination with L. monocytogenes. The study included 298 retail delis in six state and local health departments' jurisdictions and assessed how well deli practices complied with the U.S. Food and Drug Administration Food Code provisions. Among delis observed using wet wiping cloths for cleaning, 23.6% did not store the cloths in a sanitizing solution between uses. Observed potential cross-contamination of raw meats and ready-to-eat foods during preparation (e.g., same knife used on raw meats and ready-to-eat foods, without cleaning in between) was present in 9.4% of delis. In 24.6% of delis with a cold storage unit, raw meats were not stored separately from ready-to-eat products in containers, bins, or trays. A proper food safety management plan can reduce gaps in cross-contamination prevention and should include adopting procedures to minimize food safety risks, instituting training with instruction and in-person demonstrations and certifying staff on those procedures, and monitoring to ensure the procedures are followed.

Enhanced Sanitation Standard Operating Procedures Have Limited Impact on Listeria monocytogenes Prevalence in Retail Delis.

In a recent longitudinal surveillance study in 30 U.S. retail delicatessens, 9.7% of environmental surfaces were positive for Listeria monocytogenes, and we found substantial evidence of persistence. In this study, we aimed to reduce the prevalence and persistence of L. monocytogenes in the retail deli environment by developing and implementing practical and feasible intervention strategies (i.e., sanitation standard operating procedures; SSOPs). These SSOPs were standardized across the 30 delis enrolled in this study. SSOP implementation was verified by systems inherent to each retailer. Each deli also was equipped with ATP monitoring systems to verify effective sanitation. We evaluated intervention strategy efficacy by testing 28 food and nonfood contact surfaces for L. monocytogenes for 6 months in all 30 retail delis. The efficacy of the intervention on the delis compared with preintervention prevalence level was not statistically significant; we found that L. monocytogenes could persist despite implementation of enhanced SSOPs. Systematic and accurate use of ATP monitoring systems varied widely among delis. The findings indicate that intervention strategies in the form of enhanced daily SSOPs were not sufficient to eliminate L. monocytogenes from highly prevalent and persistently contaminated delis and that more aggressive strategies (e.g., deep cleaning or capital investment in redesign or equipment) may be necessary to fully mitigate persistent contamination.

Evaluation of Third-Party Deep Cleaning as a Listeria monocytogenes Control Strategy in Retail Delis.

The objective of this study was to develop and assess the efficacy of an aggressive deep cleaning sanitation standard operating procedure (DC-SSOP) in nine retail delicatessens to reduce persistent Listeria monocytogenes environmental contamination. The DC-SSOP was developed from combined daily SSOPs recommended by the Food Marketing Institute and input from experts in Listeria control from food manufacturing and sanitation. The DC-SSOP was executed by a trained professional cleaning service during a single 12-h shutdown period. A modified protocol from the U.S. Food and Drug Administration Bacteriological Analytical Manual was used to detect L. monocytogenes in samples from 28 food and nonfood contact surfaces that were collected immediately before and after each cleaning and in samples collected monthly for 3 months. The DC-SSOP significantly reduced L. monocytogenes prevalence overall during the 3-month follow-up period and produced variable results for persistent L. monocytogenes isolates. Six delis with historically low to moderate L. monocytogenes prevalence had no significant changes in the number of samples positive for L. monocytogenes after deep cleaning. Deep cleaning in very high prevalence delis (20 to 30% prevalence) reduced L. monocytogenes by 25.6% (Padj < 0.0001, n = 294) overall during the follow-up period. Among delis with extremely high prevalence (>30%), positive samples from nonfood contact surfaces were reduced by 19.6% (Padj = 0.0002, n = 294) during the follow-up period. The inability of deep cleaning to completely eliminate persistent L. monocytogenes was likely due to the diverse infrastructures in each deli, which may require more individualized intervention strategies.

Aerobic plate counts and ATP levels correlate with Listeria monocytogenes detection in retail delis.

Listeria monocytogenes is a foodborne pathogen that causes an estimated 1,591 cases of illness and 255 deaths annually in the United States, the majority of which are attributed to ready-to-eat deli meats processed in retail delis. Because retail delis distribute product directly to consumers, rapid methods to validate cleaning and sanitation are needed to improve retail food safety. This study investigated the relationships among ATP levels, standard aerobic plate count (APC), and L. monocytogenes presence in fully operational delis. Fifteen full-service delis were concurrently sampled for ATP, APC, and L. monocytogenes during preoperational hours once monthly for 3 months. Fifteen additional delis were recruited for 6 months of operational sampling (n = 30). A 1-log increase in APC was equivalent to a 3.3-fold increase in the odds of detecting L. monocytogenes (P < 0.001) and a 1.9-log increase in L monocytogenes population (P = 0.03). An ATP level increase of 1 log relative light unit correlated to a 0.22-log increase in APC (P < 0.001). A preoperational ATP level mean increase by 1 log relative light unit increased the odds of detecting L. monocytogenes concurrently fourfold. A 0.5-log increase in mean ATP level during preoperational sampling corresponded to a 2% increase in the predicted L. monocytogenes prevalence during operation (P < 0.01). Additionally, 10 statistically representative sites were identified and recommended for use in sanitation monitoring programs. Our data support the use of ATP as a rapid method to validate effective cleaning and sanitation to reduce L. monocytogenes in retail delis.

Persistent and transient Listeria monocytogenes strains from retail deli environments vary in their ability to adhere and form biofilms and rarely have inlA premature stop codons.

Based on recent risk assessments, up to 83% of listeriosis cases from deli meat in the United States are predicted to be from ready-to-eat deli meats contaminated during processing at retail grocery stores. Listeria monocytogenes is known to use sanitizer tolerance and biofilm formation to survive, but interplay of these mechanisms along with virulence potential and persistence mechanisms specific to deli environments had yet to be elucidated. In this study, 442 isolates from food and nonfood contact surfaces in 30 retail delis over 9 months were tested for inlA premature stop codons (PMSCs); inlA encodes InlA, which is necessary to cause listeriosis. A total of 96 isolates, composed of 23 persistent and 73 transient strains, were tested for adhesion and biofilm-forming ability and sanitizer tolerance. Only 10/442 isolates had inlA PMSCs (p<0.001). Strains with PMSCs were not persistent, even in delis with other persistent strains. Most (7/10) PMSC-containing isolates were collected from food contact surfaces (p<0.001); 6/10 PMSC-containing isolates were found in moderate prevalence delis (p<0.05). Persistent strains had enhanced adhesion on day 1 of a 5-day adhesion-biofilm formation assay. However, there was no significant difference in sanitizer tolerance between persistent and transient strains. Results suggest that foods contaminated with persistent L. monocytogenes strains from the retail environment are (1) likely to have wild-type virulence potential and (2) may persist due to increased adhesion and biofilm formation capacity rather than sanitizer tolerance, thus posing a significant public health risk.