Improving resolution of public health surveillance for human Salmonella entericaserovar Typhimurium infection: 3 years of prospective multiple-locus variable-number tandem-repeat analysis (MLVA)

Sintchenko, Vitali; Wang, Qinning; Howard, Peter; Ha, Connie; Kardamanidis, Katina; Musto, Jennie; Gilbert, Gwendolyn L.

doi:10.1186/1471-2334-12-78

Cited by 39 publications

(40 citation statements)

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“…All the serial S. Typhimurium isolates from the same patient were grouped together. Isolates from patients 4, 6, 8, and 10 clustered together, and based on their relationship with the DT170 isolates, it is likely that they belonged to phage type DT170, the most common phage type in NSW, Australia, where the patients resided (7). The phylogenetic analysis showed that the isolates from carriers did not belong to a single clone.…”

Section: Resultsmentioning

confidence: 97%

“…In the state of New South Wales (NSW), the notification rate has been around 50 cases per 100,000 population (5). Sequencing of S. Typhimurium genomes or analyses of tandem repeats within the genome have increasingly been employed for tracking community outbreaks and transmission chains (6,7). However, the magnitude of genomic variation in isolates associated with carriage remains unknown.…”

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confidence: 99%

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Genomic Variability of Serial Human Isolates of Salmonella enterica Serovar Typhimurium Associated with Prolonged Carriage

et al. 2015

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c Salmonella enterica serovar Typhimurium is an important foodborne human pathogen that often causes self-limiting but severe gastroenteritis. Prolonged excretion of S. Typhimurium after the infection can lead to secondary transmissions. However, little is known about within-host genomic variation in bacteria associated with asymptomatic shedding. Genomes of 35 longitudinal isolates of S. Typhimurium recovered from 11 patients (children and adults) with culture-confirmed gastroenteritis were sequenced. There were three or four isolates obtained from each patient. Single nucleotide polymorphisms (SNPs) were analyzed in these isolates, which were recovered between 1 and 279 days after the initial diagnosis. Limited genomic variation (5 SNPs or fewer) was associated with short-and long-term carriage of S. Typhimurium. None of the isolates was shown to be due to reinfection. SNPs occurred randomly, and the majority of the SNPs were nonsynonymous. Two nonsense mutations were observed. A nonsense mutation in flhC rendered the isolate nonmotile, whereas the significance of a nonsense mutation in yihV is unknown. The estimated mutation rate is 1.49 ؋ 10 ؊6 substitution per site per year. S. Typhimurium isolates excreted in stools following acute gastroenteritis in children and adults demonstrated limited genomic variability over time, regardless of the duration of carriage. These findings have important implications for the detection of possible transmission events suspected by public health genomic surveillance of S. Typhimurium infections. Nontyphoid Salmonella (NTS) infections generally result in a short-term, self-limiting gastroenteritis. However, NTS can be excreted continually and asymptomatically in stools for many weeks, even after the initial diarrheal episode has been resolved. Children are the more common carriers, especially children under the age of 3 years (1, 2). Fecal shedding of NTS after an intestinal infection can last for up to 4 weeks in adults and 7 weeks in children (3). In a very small proportion of cases, carriage can last for a year after the initial onset of the disease (3). Carriers excrete large numbers of bacteria in their feces and can facilitate the transmission of Salmonella to other hosts by contaminating water and food sources. The persistence of fecal shedding in asymptomatic patients can have a duration similar to that for patients with clinical disease (4). Antibiotic treatment of NTS disease is rarely indicated, as it does not assist in clearance of infection but may increase the duration of asymptomatic shedding (4).Salmonella enterica serovar Typhimurium is one of the leading causes of NTS gastroenteritis in humans in Australia and other countries. Salmonellosis is a notifiable disease in all Australian states and territories. In the state of New South Wales (NSW), the notification rate has been around 50 cases per 100,000 population (5). Sequencing of S. Typhimurium genomes or analyses of tandem repeats within the genome have increasingly been employed for tracking community ou...

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Genomic Variability of Serial Human Isolates of Salmonella enterica Serovar Typhimurium Associated with Prolonged Carriage

et al. 2015

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“…Multilocus sequence typing (MLST) has a low resolution to type S. Typhimurium, as the majority of isolates belong to sequence type 19 (ST19) (10). Multilocus variable-number tandem-repeat analysis (MLVA) has been adopted as a standardized method in Australia (9,11) and Europe (12). However, the numerical dominance of endemic MLVA types reduces the power of MLVA for outbreak investigations.…”

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confidence: 99%

Defining the Core Genome of Salmonella enterica Serovar Typhimurium for Genomic Surveillance and Epidemiological Typing

Octavia

Tanaka

et al. 2015

J Clin Microbiol

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c Salmonella enterica serovar Typhimurium is the most common Salmonella serovar causing foodborne infections in Australia and many other countries. Twenty-one S. Typhimurium strains from Salmonella reference collection A (SARA) were analyzed using Illumina high-throughput genome sequencing. Single nucleotide polymorphisms (SNPs) in 21 SARA strains ranged from 46 to 11,916 SNPs, with an average of 1,577 SNPs per strain. Together with 47 strains selected from publicly available S. Typhimurium genomes, the S. Typhimurium core genes (STCG) were determined. The STCG consist of 3,846 genes, a set that is much larger than that of the 2,882 Salmonella core genes (SCG) found previously. The STCG together with 1,576 core intergenic regions (IGRs) were defined as the S. Typhimurium core genome. Using 93 S. Typhimurium genomes from 13 epidemiologically confirmed community outbreaks, we demonstrated that typing based on the S. Typhimurium core genome (STCG plus core IGRs) provides superior resolution and higher discriminatory power than that based on SCG for outbreak investigation and molecular epidemiology of S. Typhimurium. STCG and STCG plus core IGR typing achieved 100% separation of all outbreaks compared to that of SCG typing, which failed to separate isolates from two outbreaks from background isolates. Defining the S. Typhimurium core genome allows standardization of genes/regions to be used for high-resolution epidemiological typing and genomic surveillance of S. Typhimurium.

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“…Therefore, phage typing has limited resolution for outbreak detection. More recently, multilocus variable-number tandem-repeat (VNTR) analysis (MLVA) has been adopted in public health reference laboratories across Australia for epidemiological typing because of its relatively high discriminatory power and ability to be harmonized (1). MLVA has also been used as a standardized method for outbreak detection in Europe (2,3).…”

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confidence: 99%

“…In New South Wales (NSW), Australia, all Salmonella isolates from public and private pathology providers are routinely referred to the NSW Enteric Reference Laboratory, Institute for Clinical Pathology and Medical Research (ICPMR), Westmead Hospital, for serotyping and MLVA typing using five VNTR loci (MLVA-5) (1). Prospective MLVA typing of S. Typhimurium has been useful for identifying outbreak clusters (1).…”

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Delineating Community Outbreaks of Salmonella enterica Serovar Typhimurium by Use of Whole-Genome Sequencing: Insights into Genomic Variability within an Outbreak

et al. 2015

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c Whole-genome next-generation sequencing (NGS) was used to retrospectively examine 57 isolates from five epidemiologically confirmed community outbreaks (numbered 1 to 5) caused by Salmonella enterica serovar Typhimurium phage type DT170. Most of the human and environmental isolates confirmed epidemiologically to be involved in the outbreaks were either genomically identical or differed by one or two single nucleotide polymorphisms (SNPs), with the exception of those in outbreak 1. The isolates from outbreak 1 differed by up to 12 SNPs, which suggests that the food source of the outbreak was contaminated with more than one strain while each of the other four outbreaks was caused by a single strain. In addition, NGS analysis ruled in isolates that were initially not considered to be linked with the outbreak, which increased the total outbreak size by 107%. The mutation process was modeled by using known mutation rates to derive a cutoff value for the number of SNP difference to determine whether or not a case was part of an outbreak. For an outbreak with less than 1 month of ex vivo/in vivo evolution time, the maximum number of SNP differences between isolates is two or four using the lowest or highest mutation rate, respectively. NGS of S. Typhimurium significantly increases the resolution of investigations of community outbreaks. It can also inform a more targeted public health response by providing important supplementary evidence that cases of disease are or are not associated with food-borne outbreaks of S. Typhimurium. Salmonella enterica serovar Typhimurium is the most common serovar isolated from humans and animals in Australia. Traditionally, surveillance and outbreak investigations of S. Typhimurium rely upon phage typing, which is based on the susceptibility of isolates to a set of bacteriophages. Phage type DT170 has been increasing steadily over the last decade in Australia and became the most frequent phage type in 2004. Therefore, phage typing has limited resolution for outbreak detection. More recently, multilocus variable-number tandem-repeat (VNTR) analysis (MLVA) has been adopted in public health reference laboratories across Australia for epidemiological typing because of its relatively high discriminatory power and ability to be harmonized (1). MLVA has also been used as a standardized method for outbreak detection in Europe (2, 3).In New South Wales (NSW), Australia, all Salmonella isolates from public and private pathology providers are routinely referred to the NSW Enteric Reference Laboratory, Institute for Clinical Pathology and Medical Research (ICPMR), Westmead Hospital, for serotyping and MLVA typing using five VNTR loci (MLVA-5) (1). Prospective MLVA typing of S. Typhimurium has been useful for identifying outbreak clusters (1). In our current practice, recovery of five or more geographically clustered isolates of the same MLVA profile from patients with diarrhea within a 4-week period (cases in the same household are counted as one episode) signals that an outbreak has occurred and...

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Improving resolution of public health surveillance for human Salmonella entericaserovar Typhimurium infection: 3 years of prospective multiple-locus variable-number tandem-repeat analysis (MLVA)

Cited by 39 publications

References 31 publications

Genomic Variability of Serial Human Isolates of Salmonella enterica Serovar Typhimurium Associated with Prolonged Carriage

Genomic Variability of Serial Human Isolates of Salmonella enterica Serovar Typhimurium Associated with Prolonged Carriage

Defining the Core Genome of Salmonella enterica Serovar Typhimurium for Genomic Surveillance and Epidemiological Typing

Delineating Community Outbreaks of Salmonella enterica Serovar Typhimurium by Use of Whole-Genome Sequencing: Insights into Genomic Variability within an Outbreak

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