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Comparison of Salmonella enterica serovar Heidelberg isolates from human patients with those from animal and food sources.

ABSTRACT: Seventy-eight Salmonella enterica serovar Heidelberg isolates from humans were tested for antimicrobial susceptibility, resistance genes, and plasmids and genotyped by pulsed-field gel electrophoresis (PFGE). Most (88%) contained plasmids, and 47% were resistant to antimicrobials. The overall results were compared to those of previous S. Heidelberg studies of food- and animal-related sources, and multiple similarities were observed.

SUBMITTER: Han J

PROVIDER: S-EPMC3067730 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Comparison of Salmonella enterica serovar Heidelberg isolates from human patients with those from animal and food sources.

Han Jing J David Donna E DE Deck Joanna J Lynne Aaron M AM Kaldhone Pravin P Nayak Rajesh R Stefanova Rossina R Foley Steven L SL

Journal of clinical microbiology 20101222 3

Seventy-eight Salmonella enterica serovar Heidelberg isolates from humans were tested for antimicrobial susceptibility, resistance genes, and plasmids and genotyped by pulsed-field gel electrophoresis (PFGE). Most (88%) contained plasmids, and 47% were resistant to antimicrobials. The overall results were compared to those of previous S. Heidelberg studies of food- and animal-related sources, and multiple similarities were observed. ...[more]

PMID: 21177888

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Project description: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.

Project description:Salmonella enterica is one of the most common bacterial foodborne pathogens in the United States, causing illnesses that range from self-limiting gastroenteritis to more severe, life threatening invasive disease. Many Salmonella strains contain plasmids that carry virulence, antimicrobial resistance, and/or transfer genes which allow them to adapt to diverse environments, and these can include incompatibility group (Inc) FIB plasmids. This study was undertaken to evaluate the genomic and phenotypic characteristics of IncFIB-positive Salmonella enterica serovar Typhimurium isolates from food animal sources, to identify their plasmid content, assess antimicrobial resistance and virulence properties, and compare their genotypic isolates with more recently isolated S. Typhimurium isolates from food animal sources. Methods: We identified 71 S. Typhimurium isolates that carried IncFIB plasmids. These isolates were subjected to whole genome sequencing and evaluated for bacteriocin production, antimicrobial susceptibility, the ability to transfer resistance plasmids, and a subset was evaluated for their ability to invade and persist in intestinal human epithelial cells. Results: Approximately 30% of isolates (n = 21) displayed bacteriocin inhibition of Escherichia coli strain J53. Bioinformatic analyses using PlasmidFinder software confirmed that all isolates contained IncFIB plasmids along with multiple other plasmid replicon types. Comparative analyses showed that all strains carried multiple antimicrobial resistance genes and virulence factors including iron acquisition genes, such as iucABCD (75%), iutA (94%), sitABCD (76%) and sitAB (100%). In 17 cases (71%), IncFIB plasmids, along with other plasmid replicon types, were able to conjugally transfer antimicrobial resistance and virulence genes to the susceptible recipient strain. For ten strains, persistence cell counts (27%) were noted to be significantly higher than invasion bacterial cell counts. When the genome sequences of the study isolates collected from 1998-2003 were compared to those published from subsequent years (2005-2018), overlapping genotypes were found, indicating the perseverance of IncFIB positive strains in food animal populations. This study confirms that IncFIB plasmids can play a potential role in disseminating antimicrobial resistance and virulence genes amongst bacteria from several food animal species.

Project description:Salmonella enterica serovar Heidelberg is isolated from poultry-producing regions around the world. In Brazil, S. Heidelberg has been frequently detected in poultry flocks, slaughterhouses, and chicken meat. The goal of the present study was to assess the population structure, recent temporal evolution, and some important genetic characteristics of S. Heidelberg isolated from Brazilian poultry farms. Phylogenetic analysis of 68 S. Heidelberg genomes sequenced here and additional whole-genome data from NCBI demonstrated that all isolates from the Brazilian poultry production chain clustered into a monophyletic group, here called S. Heidelberg Brazilian poultry lineage (SH-BPL). Bayesian analysis defined the time of the most recent common ancestor (tMRCA) as 2004, and the overall population size (Ne) was constant until 2008, when an ∼10-fold Ne increase was observed until circa 2013. SH-BPL presented at least two plasmids with replicons ColpVC (n = 68; 100%), IncX1 (n = 66; 97%), IncA/C2 (n = 65; 95.5%), ColRNAI (n = 43; 63.2%), IncI1 (n = 32; 47%), ColMG828, Col156, IncHI2A, IncHI2, IncQ1, IncX4, IncY, and TrfA (each with n < 4; <4% each). Antibiotic resistance genes were found, with high frequencies of fosA7 (n = 68; 100%), mdf(A) (n = 68; 100%), tet(34) (n = 68; 100%), sul2 (n = 64; 94.1%), and blaCMY-2 (n = 56; 82.3%), along with an overall multidrug resistance (MDR) profile. Ten Salmonella pathogenicity islands (SPI1 to SPI5, SPI9, and SPI11 to SPI14) and 139 virulence genes were also detected. The SH-BPL profile was like those of other previous S. Heidelberg isolates from poultry around the world in the 1990s. In conclusion, the present study demonstrates the recent introduction (2004) and high level of dissemination of an MDR S. Heidelberg lineage in Brazilian poultry operations. IMPORTANCE S. Heidelberg is the most frequent serovar in several broiler farms from the main Brazilian poultry-producing regions. Therefore, avian-source foods (mainly chicken carcasses) commercialized in the country and exported to other continents are contaminated with this foodborne pathogen, generating several national and international economic losses. In addition, isolates of this serovar are usually resistant to antibiotics and can cause human invasive and septicemic infection, representing a public health concern. This study demonstrates the use of whole-genome sequencing (WGS) to obtain epidemiological information for one S. Heidelberg lineage highly spread among Brazilian poultry farms. This information will help to define biosecurity measures to control this important Salmonella serovar in Brazilian and worldwide poultry operations.

Dataset Information

Comparison of Salmonella enterica serovar Heidelberg isolates from human patients with those from animal and food sources.

Publications

Comparison of Salmonella enterica serovar Heidelberg isolates from human patients with those from animal and food sources.

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