A Whole-Genome Single Nucleotide Polymorphism-Based Approach To Trace and Identify Outbreaks Linked to a Common Salmonella enterica subsp. enterica Serovar Montevideo Pulsed-Field Gel Electrophoresis Type

Bakker, Henk C. den; Switt, Andrea I. Moreno; Cummings, Craig; Hoelzer, Karin; Degoricija, Lovorka; Rodriguez‐Rivera, Lorraine D.; Wright, Emily; Fang, Rixun; Davis, Margaret A.; Root, Timothy P.; Schoonmaker-Bopp, Dianna; Musser, Kimberlee A.; Villamil, Elizabeth; Waechter, HaeNa; Kornstein, Laura; Furtado, Manohar R.; Wiedmann, Martin

doi:10.1128/aem.06538-11

Cited by 93 publications

(79 citation statements)

References 18 publications

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“…Similar demographic effects are expected to be true for other epidemic pathogens, especially for zoonotic diseases with similar lifestyles, such as Bacillus anthracis and Francisella tularensis (51). Variable mutation rates have also been reported for S. enterica serovar Montevideo, which was associated with a recent food-born outbreak (52). However, we note that although a demographic explanation may explain the observed patterns, we cannot exclude alternative scenarios, such as host density changes driven by climatic factors (53,54), which will also change the number of bacterial replication cycles.…”

Section: Discussionmentioning

confidence: 49%

Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis

Cui

Yan

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

362

442

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The genetic diversity of Yersinia pestis, the etiologic agent of plague, is extremely limited because of its recent origin coupled with a slow clock rate. Here we identified 2,326 SNPs from 133 genomes of Y. pestis strains that were isolated in China and elsewhere. These SNPs define the genealogy of Y. pestis since its most recent common ancestor. All but 28 of these SNPs represented mutations that happened only once within the genealogy, and they were distributed essentially at random among individual genes. Only seven genes contained a significant excess of nonsynonymous SNP, suggesting that the fixation of SNPs mainly arises via neutral processes, such as genetic drift, rather than Darwinian selection. However, the rate of fixation varies dramatically over the genealogy: the number of SNPs accumulated by different lineages was highly variable and the genealogy contains multiple polytomies, one of which resulted in four branches near the time of the Black Death. We suggest that demographic changes can affect the speed of evolution in epidemic pathogens even in the absence of natural selection, and hypothesize that neutral SNPs are fixed rapidly during intermittent epidemics and outbreaks.infectious disease | molecular clock | phylogenomics | NGS | molecular epidemiology

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Section: Discussionmentioning

confidence: 49%

Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis

Cui

Yan

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

362

442

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“…The exceptional performance of WGST in the fine-scale delineation of outbreaks of infectious disease has been demonstrated in recent investigations (24)(25)(26)(27)(28)(29)(30)(31). In the current study, we expanded the evaluation of WGST by retrospectively investigating isolates from15 recent S. enterica serotype Enteritidis outbreaks in the United States and 1 in Mauritius.…”

Section: Discussionmentioning

confidence: 99%

Comparative Analysis of Subtyping Methods against a Whole-Genome-Sequencing Standard for Salmonella enterica Serotype Enteritidis

et al. 2015

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A retrospective investigation was performed to evaluate whole-genome sequencing as a benchmark for comparing molecular subtyping methods for Salmonella enterica serotype Enteritidis and survey the population structure of commonly encountered S. enterica serotype Enteritidis outbreak isolates in the United States. A total of 52 S. enterica serotype Enteritidis isolates representing 16 major outbreaks and three sporadic cases collected between 2001 and 2012 were sequenced and subjected to subtyping by four different methods: (i) whole-genome single-nucleotide-polymorphism typing (WGST), (ii) multiple-locus variablenumber tandem-repeat (VNTR) analysis (MLVA), (iii) clustered regularly interspaced short palindromic repeats combined with multi-virulence-locus sequence typing (CRISPR-MVLST), and (iv) pulsed-field gel electrophoresis (PFGE). WGST resolved all outbreak clusters and provided useful robust phylogenetic inference results with high epidemiological correlation. While both MLVA and CRISPR-MVLST yielded higher discriminatory power than PFGE, MLVA outperformed the other methods in delineating outbreak clusters whereas CRISPR-MVLST showed the potential to trace major lineages and ecological origins of S. enterica serotype Enteritidis. Our results suggested that whole-genome sequencing makes a viable platform for the evaluation and benchmarking of molecular subtyping methods. Salmonella enterica is currently the most common bacterial foodborne pathogen in the United States, causing over 1 million cases of illnesses annually, including approximately 20,000 hospitalizations and 400 deaths (1). Serotyping is commonly used to subtype strains below the species level for epidemiologic purposes. Salmonella enterica serotype Enteritidis was the serotype most commonly linked to foodborne outbreaks between 1998 and 2008 in the United States, with shell eggs being the major vehicle for foodborne transmission (2). In recent years, S. enterica serotype Enteritidis was also found to cause multistate outbreaks associated with other foods such as ground beef (2012), Turkish pine nuts (2011), and alfalfa and spicy sprouts (2011), in addition to shelled eggs (2010) (3).During outbreak investigations, it is critical to employ subtyping methods capable of distinguishing outbreak isolates from epidemiologically distinct but genetically related bacterial strains. Most S. enterica serotype Enteritidis isolates have been shown to be genetically homogeneous, making it difficult for conventional subtyping methods such as pulsed-field gel electrophoresis (PFGE), the current gold standard for strain-level Salmonella subtyping, to discriminate between strains (4, 5). Among the S. enterica serotype Enteritidis isolates reported to PulseNet (6), approximately 45% display a single PFGE pattern using XbaI (JEGX01.0004), rendering PFGE ineffective in some foodborne outbreak investigations. One strategy to improve subtype resolution is to target hypervariable regions (i.e., regions of the bacterial chromosome with less genetic stability) in the ba...

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“…This might favor the implementation of PCRand sequencing-based methods in some laboratories, particularly as advances in sequencing technology might make these methods more attractive. Sequencing-based approaches for serovar determination can also be easily integrated into whole-genome sequencing-based approaches for Salmonella characterization, which are emerging as a viable alternative to other subtyping methods (58,59). Sequence data for fliC, fljB, genes in the rfb cluster, and genes targeted by MLST can be rapidly extracted from full-genome sequence data and used for serovar identification.…”

Section: Discussionmentioning

confidence: 99%

Comparison of Typing Methods with a New Procedure Based on Sequence Characterization for Salmonella Serovar Prediction

et al. 2013

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bAs the development of molecular serotyping approaches is critical for Salmonella spp., which include >2,600 serovars, we performed an initial evaluation of the ability to identify Salmonella serovars using (i) different molecular subtyping methods and (ii) a newly implemented combined PCR-and sequencing-based approach that directly targets O-and H-antigen-encoding genes. Initial testing was performed using 46 isolates that represent the top 40 Salmonella serovars isolated from human and nonhuman sources, as reported by the U.S. Centers for Disease Control and Prevention and the World Health Organization. Multilocus sequence typing (MLST) was able to accurately predict the serovars for 42/46 isolates and showed the best ability to predict serovars among the subtyping methods tested. Pulsed-field gel electrophoresis (PFGE), ribotyping, and repetitive extragenic palindromic sequence-based PCR (rep-PCR) were able to accurately predict the serovars for 35/46, 34/46, and 30/46 isolates, respectively. Among the methods, S. enterica subsp. enterica serovars 4,5,12:i:؊, Typhimurium, and Typhimurium var. 5؊ were frequently not classified correctly, which is consistent with their close phylogenetic relationship. To develop a PCR-and sequence-based serotyping approach, we integrated available data sources to implement a combination PCR-based O-antigen screening and sequencing of internal fliC and fljB fragments. This approach correctly identified the serovars for 42/46 isolates in the initial set representing the most common Salmonella serovars, as well as for 54/63 isolates representing less common Salmonella serovars. Our study not only indicates that different molecular approaches show the potential to allow for rapid serovar classification of Salmonella isolates, but it also provides data that can help with the selection of molecular serotyping methods to be used by different laboratories.

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A Whole-Genome Single Nucleotide Polymorphism-Based Approach To Trace and Identify Outbreaks Linked to a Common Salmonella enterica subsp. enterica Serovar Montevideo Pulsed-Field Gel Electrophoresis Type

Cited by 93 publications

References 18 publications

Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis

Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis

Comparative Analysis of Subtyping Methods against a Whole-Genome-Sequencing Standard for Salmonella enterica Serotype Enteritidis

Comparison of Typing Methods with a New Procedure Based on Sequence Characterization for Salmonella Serovar Prediction

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