Whole Genome Sequence Typing to Investigate the Apophysomyces Outbreak following a Tornado in Joplin, Missouri, 2011

Etienne, Kizee A.; Gillece, John D.; Hilsabeck, Remy; Schupp, Jim; Colman, Rebecca E.; Lockhart, Shawn R.; Gade, Lalitha; Thompson, Elizabeth H.; Sutton, Deanna A.; Neblett-Fanfair, Robyn; Park, Benjamin J.; Turabelidze, George; Keim, Paul; Brandt, Mary E.; Deák, Eszter; Engelthaler, David M.

doi:10.1371/journal.pone.0049989

Cited by 69 publications

(65 citation statements)

References 28 publications

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“…Genomic DNA was prepared using a GenElute genomic DNA isolation kit (Sigma-Aldrich, St. Louis, MO). WGS was performed at TGen North using Illumina technology (100-bp paired-end reads) as described in previous studies (16,17). All WGS data files were deposited in the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov /bioproject) under project number PRJNA251730.…”

Section: Methodsmentioning

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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Section: Methodsmentioning

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 later comparative genomics study, based on the analysis of 10 genomes of each species, determined that the separation of the two species has not remained fully complete and documented possible presence of introgression from hybridization events following species separation (11). As rapid DNA sequencing analysis has become more accessible to research and public health laboratories, approaches such as whole-genome SNP typing (WGST) have been shown to be useful for identifying clonal fungal outbreaks (12)(13)(14)(15). However, genomic epidemiology is also needed to help establish the location of exposure of a nonclonal outbreak and robust phylogenomic analysis is needed for in-depth investigation of the local population structure to better understand pathogen emergence, dispersal, and expansion (15).…”

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Local population structure and patterns of Western Hemisphere dispersal forCoccidioides spp., the fungal cause of Valley Fever

Engelthaler

Roe

Litvintseva³

et al. 2015

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“…Overall, genetic diversity among the control strains of E. rostratum was comparable to diversities observed in other groups of fungi with sequenced genomes. For example, approximately 300,000 fixed SNPs were observed between Coccidioides immitis and Coccidioides posadasii genomes (33), approximately 135,000 SNPs were identified among wild-type isolates of Neurospora crassa from geographically different populations (34), and ap- (21).…”

Section: Discussionmentioning

confidence: 99%

“…This is especially important for outbreaks of fungal infections where rapid laboratory methods to establish the relatedness of different strains may be the critical factor in determining whether a cluster of rare mold infections represent a true outbreak or a just an unusual coincidence. In the past 18 months, the CDC has investigated several potential outbreaks of rare molds that did not have established DNA typing methods, including an outbreak of Bipolaris hawaiiensis associated with compounded triamcinolone for intraocular administration (37), Curvularia (Bipolaris) spicifera in cardiac surgical site infections (CDC unpublished data), and Apophysomyces trapeziformis soft tissue infections occurring after a natural disaster (21). The determination of whether these isolates were related relied on painstaking epidemiologic studies, as typing methods were not initially available.…”

Section: Discussionmentioning

confidence: 99%

“…While whole-genome sequencing (WGS) is a relatively new tool of molecular epidemiology, it has quickly been embraced as a mechanism for inferring phylogenetic relationships among organisms. This has translated to the recent use of whole-genome single nucleotide polymorphism (SNP) typing (whole-genome sequence typing [WGST]) as a mechanism for inferring relatedness of both bacteria (16)(17)(18)(19) and fungi (20,21) during outbreak investigations. One of the benefits of WGST is that prior knowledge of the genome is not necessary to conduct epidemiologic analyses.…”

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Whole-Genome Analysis of Exserohilum rostratum from an Outbreak of Fungal Meningitis and Other Infections

et al. 2014

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Exserohilum rostratum was the cause of most cases of fungal meningitis and other infections associated with the injection of contaminated methylprednisolone acetate produced by the New England Compounding Center (NECC). Until this outbreak, very few human cases of Exserohilum infection had been reported, and very little was known about this dematiaceous fungus, which usually infects plants. Here, we report using whole-genome sequencing (WGS) for the detection of single nucleotide polymorphisms (SNPs) and phylogenetic analysis to investigate the molecular origin of the outbreak using 22 isolates of E. rostratum retrieved from 19 case patients with meningitis or epidural/spinal abscesses, 6 isolates from contaminated NECC vials, and 7 isolates unrelated to the outbreak. Our analysis indicates that all 28 isolates associated with the outbreak had nearly identical genomes of 33.8 Mb. A total of 8 SNPs were detected among the outbreak genomes, with no more than 2 SNPs separating any 2 of the 28 genomes. The outbreak genomes were separated from the next most closely related control strain by ϳ136,000 SNPs. We also observed significant genomic variability among strains unrelated to the outbreak, which may suggest the possibility of cryptic speciation in E. rostratum. Beginning in September, 2012, the United States experienced one of the largest outbreaks of health care-associated infections ever reported. More than 13,000 people were exposed to three lots of contaminated methylprednisolone acetate (MPA) produced by a single compounding pharmacy, and Ͼ750 developed fungal infections following their MPA injections (1-3). Infections included meningitis, as well as localized epidural, paraspinal, and peripheral joint infections, complicated by arachnoiditis and abscess formation (4, 5). Although several fungal species were implicated in the outbreak, the vast majority of infections were caused by Exserohilum rostratum, a saprobic mold found in soil and plant debris worldwide (2, 6-10). Most species of Exserohilum are plant pathogens. Exserohilum rostratum and the species formerly known as Exserohilum longirostratum and Exserohilum mcginnisii are morphologically similar and are the only species known to cause human infections; however, their taxonomic status remains under investigation (11-13).DNA fingerprinting has been used as an epidemiological tool to answer questions pertaining to strain relatedness (14, 15). However, no methodologies for DNA fingerprinting of E. rostratum existed at the time of the outbreak. While whole-genome sequencing (WGS) is a relatively new tool of molecular epidemiology, it has quickly been embraced as a mechanism for inferring phylogenetic relationships among organisms. This has translated to the recent use of whole-genome single nucleotide polymorphism (SNP) typing (whole-genome sequence typing [WGST]) as a mechanism for inferring relatedness of both bacteria (16)(17)(18)(19) and fungi (20, 21) during outbreak investigations. One of the benefits of WGST is that prior knowledge of the genome i...

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Whole Genome Sequence Typing to Investigate the Apophysomyces Outbreak following a Tornado in Joplin, Missouri, 2011

Cited by 69 publications

References 28 publications

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

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

Local population structure and patterns of Western Hemisphere dispersal forCoccidioides spp., the fungal cause of Valley Fever

Whole-Genome Analysis of Exserohilum rostratum from an Outbreak of Fungal Meningitis and Other Infections

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