High-throughput bacterial SNP typing identifies distinct clusters of SalmonellaTyphi causing typhoid in Nepalese children

Holt, Kathryn E.; Baker, Stephen; Dongol, Sabina; Basnyat, Buddha; Adhikari, Neelam; Thorson, Stephen; Pulickal, Anoop S.; Song, Yajun; Parkhill, Julian; Farrar, Jeremy; Murdoch, David R.; Kelly, Dominic F.; Pollard, Andrew J.; Dougan, Gordon

doi:10.1186/1471-2334-10-144

Cited by 74 publications

(82 citation statements)

References 36 publications

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“…Next-generation genome sequencing will allow a rapid expansion of SNPs for S. Typhimurium typing, as for S. Typhi (17) and Escherichia coli O157:H7 (6) strains. In this study, we used real-time PCR for typing, but the SNPs can also be used for large-scale typing by the adoption of high-throughput platforms, such as the iPlex MassArray technology (45) or the GoldenGate bead array technology (16). Establishing true relationships based on SNPs would provide a foundation for future genomic studies of differences in the prevalences and virulences of different SNP lineages or phage types.…”

Section: Resultsmentioning

confidence: 99%

Genetic Relationships of Phage Types and Single Nucleotide Polymorphism Typing of Salmonella enterica Serovar Typhimurium

et al. 2012

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Salmonella enterica serovar Typhimurium is one of the leading causes of gastroenteritis in humans. Phage typing has been used for the epidemiological surveillance of S. Typhimurium for over 4 decades. However, knowledge of the evolutionary relationships between phage types is very limited. In this study, we used single nucleotide polymorphisms (SNPs) as molecular markers to determine the relationships between common S. Typhimurium phage types. Forty-four SNPs, including 24 identified in a previous study and 20 from 6 available whole-genome sequences, were used to analyze 215 S. Typhimurium isolates belonging to 45 phage types. Altogether, 215 isolates and 6 genome strains were differentiated into 33 SNP profiles and four distinctive phylogenetic clusters. Fourteen phage types, including DT9, one of the most common phage types in Australia, were differentiated into multiple SNP profiles. These SNP profiles were distributed into different phylogenetic clusters, indicating that they have arisen independently multiple times. This finding suggests that phage typing may not be useful for long-term epidemiological studies over long periods (years) and diverse localities (different countries or continents). SNP typing provided a discriminative power similar to that of phage typing. However, 12 SNP profiles contained more than one phage type, and more SNPs would be needed for further differentiation. SNP typing should be considered as a replacement for phage typing for the identification of S. Typhimurium strains. Salmonella enterica serovar Typhimurium is a broad-host-range pathogen that causes gastroenteritis in humans. The phage typing scheme described by Anderson et al. (3) has been used for the routine epidemiological surveillance of S. Typhimurium infections for many years. Phage types are determined by resistance or sensitivity to a set of 34 phages, and so far, more than 300 definitive phage types (DTs) are recognized (38). Phage typing has been found to be particularly useful for tracking the spatiotemporal distribution of important pathogenic forms. For example, multidrug-resistant DT104 has caused widespread infections in humans and animals in Europe and the United States since 1994 (12, 23), but it remains rare in Australia. In contrast, DT9, DT135, and DT170/108 are common in Australia (34), while DT9 is rare in Europe and the United States. However, knowledge of the evolutionary relationships between phage types is very limited, and the genetic basis for the variation in phage sensitivity remains largely unknown. The discriminatory power of phage typing is often inadequate to track community outbreaks, especially in settings when one particular phage type is dominant. In addition, phage types can change with a few genetic modifications, such as a gain or loss of mobile elements (2, 27, 50).Despite the extensive diversity of phage types in S. Typhimurium, population structure studies using multilocus enzyme electrophoresis (MLEE) showed that the majority of S. Typhimurium isolates are grouped together as a s...

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Section: Resultsmentioning

confidence: 99%

Genetic Relationships of Phage Types and Single Nucleotide Polymorphism Typing of Salmonella enterica Serovar Typhimurium

et al. 2012

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“…The presence of specific SNPs divides the H58 haplogroup in two main lineages and different sublineages (Holt et al 2010) (Fig. 1B).…”

Section: Sub-typing Of H58 S Typhi By Pcr-restriction Fragment Lengtmentioning

confidence: 99%

“…In 2010 there were an estimated 26.9 million cases of typhoid fever, especially in countries with inadequate sanitation, unsafe water and poor hygiene ( Kariuki et al, 2010, Buckle et al, 2012and Wain et al, 2015. The fact that S. Typhi is restricted to humans has resulted in a very low genetic variability in this serovar, and the genomes of distinct isolates are extremely conserved ( Achtman, 2008 andHolt et al, 2010). For this reason, the most widely used molecular typing methods, including Multilocus Sequence Typing (MLST) and Pulsed-Field Gel Electrophoresis (PFGE), are not sufficiently discriminative for phylogenetic and epidemiological analysis of this pathogen ( Achtman, 2008, Octavia and Lan, 2009and Thanh et al, 2013.…”

Section: Introductionmentioning

confidence: 99%

“…The identification of specific SNPs among the H58 population (haplogroup) further defined two principal lineages (I and II) and different sub-lineages (H58A-H58J, H60-H65) ( Holt et al 2008). H58 S. Typhi strains are endemic in Southeast Asia, India and Africa ( Baltazar et al, 2015 andWain et al, 2015), and their wide diffusion has been associated to multidrug-resistance (MDR) to the first-line drugs (ampicillin, chloramphenicol, and trimethoprim-sulfamethoxazole) and to reduced susceptibility to the alternative drugs (fluoroquinolones) used in typhoid fever therapy ( Roumagnac et al, 2006, Achtman, 2008, Holt et al, 2010. The surveillance of H58 S. Typhi is therefore important, especially in areas where typhoid fever is endemic.…”

Section: Introductionmentioning

confidence: 99%

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A novel broadly applicable PCR-RFLP method for rapid identification and subtyping of H58 Salmonella Typhi

Murgia

Rubino

Wain

et al. 2016

Journal of Microbiological Methods

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Salmonella Typhi (S. Typhi), the human-adapted agent of typhoid fever, is genetically monomorphic. SNPs accumulation divided the S. Typhi population in 85 haplotypes (H) of which one, H58, has undergone a clonal expansion. The surveillance of H58 S. Typhi is particularly important, especially in areas where typhoid fever is endemic. We developed a simple PCR and PCR-RFLP method to detect and subtype H58 S. Typhi based on the presence of genomic deletion and specific SNPs. The method was validated against 39 S. Typhi isolates of known haplotype, showing 100% of specificity and high sensitivity, and then used to screen a collection of 99 S. Typhi from Asia, demonstrating a high incidence of H58 S. Typhi in Jordan and India. Our method is designed to be applied in all laboratories with basic molecular biology equipment and few financial resources and allows the surveillance of H58 S. Typhi in resource poor settings.

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“…SNP typing has also been shown to be valuable to study the local population structure and epidemiology of S. enterica serovar Typhi in Indonesia, Kenya, and Nepal (2,7,9). The SNPs and strains typed in the present study form the basis of a future database for international comparison.…”

Section: Vol 48 2010mentioning

confidence: 99%

Single Nucleotide Polymorphism Typing of Global Salmonella enterica Serovar Typhi Isolates by Use of a Hairpin Primer Real-Time PCR Assay

Octavia

Lan

2010

J Clin Microbiol

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Salmonella enterica serovar Typhi is highly homogeneous. Single nucleotide polymorphisms (SNPs) have been shown to be valuable markers for molecular typing of S. enterica serovar Typhi. Here, we used a hairpin primer real-time PCR assay for SNP typing of S. enterica serovar Typhi isolates. Forty-two SNPs were selected from a comparison of 19 published S. enterica serovar Typhi genomes and sequences from other studies. The SNPs were used to type 71 global S. enterica serovar Typhi isolates and differentiated these S. enterica serovar Typhi isolates and the 19 genome sequenced strains into 25 SNP profiles. Phylogenetic analysis revealed that these SNP profiles were grouped into six major clusters. These clusters can be identified by using five SNPs, while the full differentiation of the 25 SNP profiles requires a minimum of 24 SNPs. This real-time PCR-based SNP typing method will be useful for global epidemiological analysis.Salmonella enterica serovar Typhi is highly homogeneous (10,17,18). The lack of genetic diversity is a major challenge to the development of suitable typing methods to differentiate S. enterica serovar Typhi isolates for both phylogenetic and epidemiological purposes. Single nucleotide polymorphisms (SNPs) are considered the most valuable markers, particularly for studying the evolutionary relationships of isolates of homogeneous pathogenic clones, such as Bacillus anthracis (16), Mycobacterium tuberculosis (4), and Yersinia pestis (1).SNPs have been used as markers for molecular typing of S. enterica serovar Typhi in a large study by Roumagnac et al. (17). A total of 88 SNPs, found from analysis of 200 gene fragments from 105 diverse S. enterica serovar Typhi isolates, could differentiate 481 global S. enterica serovar Typhi isolates into 85 haplotypes (SNP profiles) and five major clusters (17). However, despite the large number of SNPs used, each of the five clusters was supported by only a single SNP and there was little resolution of the relationships of the haplotypes within a cluster. Eighty of the SNPs have also been used to differentiate 140 Indonesian S. enterica serovar Typhi isolates into nine haplotypes (2).We have also shown that genome-wide SNPs are useful for molecular typing and determining the relationships of global S. enterica serovar Typhi isolates (14). Thirty-seven SNPs selected from a comparison of the genomes of S. enterica serovar Typhi strains CT18 (15) and Ty2 (3) were typed using restriction enzyme digestion to differentiate 73 global S. enterica serovar Typhi isolates into 23 SNP profiles and four distinct genetic groups. As the SNPs were selected by comparison of only two S. enterica serovar Typhi genomes, this resulted in a phylogenetic bias which revealed the full path of the last common ancestors connecting strains CT18 and Ty2 but only the node locations for the other SNP profiles (14).Advances in technology, such as high-throughput sequencing, allow SNPs to be discovered to obtain a full resolution of the phylogenetic relationships of isolates. A recent stu...

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High-throughput bacterial SNP typing identifies distinct clusters of SalmonellaTyphi causing typhoid in Nepalese children

Cited by 74 publications

References 36 publications

Genetic Relationships of Phage Types and Single Nucleotide Polymorphism Typing of Salmonella enterica Serovar Typhimurium

Genetic Relationships of Phage Types and Single Nucleotide Polymorphism Typing of Salmonella enterica Serovar Typhimurium

A novel broadly applicable PCR-RFLP method for rapid identification and subtyping of H58 Salmonella Typhi

Single Nucleotide Polymorphism Typing of Global Salmonella enterica Serovar Typhi Isolates by Use of a Hairpin Primer Real-Time PCR Assay

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