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.
Salmonella enterica serovar Heidelberg is currently the 12th most common serovar of Salmonella enterica causing salmonellosis in the United States and results in twice the average incidence of blood infections caused by nontyphoidal salmonellae. Multiple outbreaks of salmonellosis caused by Salmonella Heidelberg resulted from the same poultry processor, which infected 634 people during 2013 and 2014. The hospitalization and invasive illness rates were 38% and 15%, respectively. We hypothesized that the outbreak strains of Salmonella Heidelberg had enhanced stress tolerance and virulence capabilities. We sourced nine food isolates collected during the outbreak investigation and three reference isolates to assess their tolerance to heat and sanitizers, ability to attach to abiotic surfaces, and invasiveness in vitro. We performed RNA sequencing on three isolates (two outbreak-associated isolates and a reference Salmonella Heidelberg strain) with various levels of heat tolerance to gain insight into the mechanism behind the isolates' enhanced heat tolerance. We also performed genomic analyses to determine the genetic relationships among the outbreak isolates. Ultimately, we determined that (i) six Salmonella Heidelberg isolates associated with the foodborne outbreak had enhanced heat tolerance, (ii) one outbreak isolate with enhanced heat tolerance also had an enhanced biofilm-forming ability under stressful conditions, (iii) exposure to heat stress increased the expression of Salmonella Heidelberg multidrug efflux and virulence genes, and (iv) outbreak-associated isolates were likely transcriptionally primed to better survive processing stresses and, potentially, to cause illness. IMPORTANCE This study provides a deep analysis of the intrinsic stress tolerance and virulence capabilities of Salmonella Heidelberg that may have contributed to the length and severity of a recent salmonellosis outbreak. Additionally, this study provides a comprehensive analysis of the transcriptomic response of S. enterica strains to heat stress conditions and compares baseline stationary-phase gene expression among outbreak-and non-outbreak-associated Salmonella Heidelberg isolates. These data can be used in assay development to screen isolates for stress tolerance and subsequent survival. This study adds to our understanding of the strains associated with the outbreak and informs ongoing regulatory discussions on Salmonella in poultry.
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