Characterization of a multidrug-resistant Salmonella enterica serovar Heidelberg outbreak strain in commercial turkeys: Colonization, transmission, and host transcriptional response

Authors: Bearson, Bradley - Brad; Bearson, Shawn; Looft, Torey; Cai, Guohong; Shippy, Daniel

Submitted to: Frontiers in Veterinary Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/7/2017
Publication Date: 9/25/2017
Publication URL: https://handle.nal.usda.gov/10113/6472225
Citation: Bearson, B.L., Bearson, S.M., Looft, T., Cai, G., Shippy, D.C. 2017. Characterization of a multidrug-resistant Salmonella enterica serovar Heidelberg outbreak strain in commercial turkeys: Colonization, transmission, and host transcriptional response. Frontiers in Veterinary Science. 4:156. https://doi.org/10.3389/fvets.2017.00156.
DOI: https://doi.org/10.3389/fvets.2017.00156

Interpretive Summary: Salmonella is a foodborne pathogen that can cause illness following the consumption of contaminated meat and poultry. There are over 2,500 types or serovars of Salmonella, and colonization of food-producing animals by Salmonella on the farm is a foodborne risk for transmission of this pathogen into the food supply. In recent years, multidrug-resistant (MDR) Salmonella enterica serovar Heidelberg has been associated with numerous human foodborne illness outbreaks due to consumption of poultry. For example, in 2011 MDR Salmonella Heidelberg was associated with a foodborne illness outbreak in ground turkey that sickened 136 individuals and resulted in 1 death. In response to this multistate outbreak, 36 million pounds of ground turkey were recalled, one of the largest meat recalls in U.S. history. The MDR Salmonella Heidelberg strain associated with this ground turkey outbreak was resistant to four antibiotic classes, and this characteristic makes medical treatment for Salmonella infections more difficult. In this study, turkeys were inoculated with an MDR Salmonella Heidelberg strain isolated during the outbreak investigation to determine the ability of this bacterium to colonize commercial turkeys and be transmitted to penmates that were not infected. Turkey gene expression in response to MDR Salmonella Heidelberg exposure was also investigated. Although turkeys were colonized following inoculation with MDR Salmonella Heidelberg, the turkeys did not induce a strong host response to the presence of the bacterium. The limited response by turkeys following inoculation with MDR Salmonella Heidelberg may be beneficial for Salmonella to establish colonization and persistence. Young turkeys that were exposed to penmates that had been inoculated with MDR Salmonella Heidelberg were colonized to the same extent, as if they had also been inoculated. This indicates that Salmonella transmission between penmates is efficient and young turkeys are vulnerable to colonization with MDR Salmonella Heidelberg. This research provides knowledge concerning the ability of MDR Salmonella Heidelberg to colonize turkeys. To reduce the introduction of MDR Salmonella Heidelberg into the food supply, preventative strategies must target young turkeys that are susceptible to colonization by Salmonella.

Technical Abstract: In recent years, multidrug-resistant (MDR) Salmonella enterica serovar Heidelberg has been associated with numerous human foodborne illness outbreaks due to consumption of poultry. For example, in 2011, an MDR S. Heidelberg outbreak associated with ground turkey sickened 136 individuals and resulted in 1 death. In response to this outbreak, 36 million pounds of ground turkey were recalled, one of the largest meat recalls in U.S. history. To investigate colonization of turkeys with an MDR S. Heidelberg strain isolated during the ground turkey outbreak, two turkey trials were performed. In experiment 1, 3-week old turkeys were inoculated with 108 or 1010 CFU of the MDR S. Heidelberg isolate, and fecal shedding and tissue colonization were determined following colonization for up to 14-days. Turkey gene expression in response to S. Heidelberg exposure revealed 18 genes that were differentially expressed at 2 days following inoculation compared to pre-inoculation. In a second trial, 1-day old poults were inoculated with 104 CFU of MDR S. Heidelberg to monitor transmission of Salmonella from inoculated poults (index group) to naive penmates (sentinel group). The transmission of MDR S. Heidelberg from index to sentinel poults was efficient with ceca colonization increasing 2 Log10 CFU above the inoculum dose at 9 days post-inoculation. This differed from the 3-week old poults inoculated with 1010 CFU of MDR S. Heidelberg in experiment 1 as Salmonella fecal shedding and tissue colonization decreased over the 14 day period compared to the inoculum dose. These data suggest that young poults are susceptible to colonization by MDR S. Heidelberg, and interventions must target turkeys when they are most vulnerable to prevent Salmonella colonization and transmission in the flock. Together, the data support the growing body of literature indicating that Salmonella establishes a commensal-like condition in livestock and poultry, contributing to the asymptomatic carrier status of the human foodborne pathogen in our animal food supply.