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Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020

BACKGROUND: The implementation of whole genome sequencing (WGS) by PulseNet, the molecular subtyping network for foodborne diseases, has transformed surveillance, outbreak detection, and public health laboratory practices in the United States. In 2017, the New Hampshire Public Health Laboratories, a...

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Autores principales: Turcotte, Madison R., Smith, Joshua T., Li, Jinfeng, Zhang, Xinglu, Wolfe, Kristin L., Gao, Fengxiang, Benton, Christopher S., Andam, Cheryl P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9308939/
https://www.ncbi.nlm.nih.gov/pubmed/35870884
http://dx.doi.org/10.1186/s12864-022-08769-1
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author Turcotte, Madison R.
Smith, Joshua T.
Li, Jinfeng
Zhang, Xinglu
Wolfe, Kristin L.
Gao, Fengxiang
Benton, Christopher S.
Andam, Cheryl P.
author_facet Turcotte, Madison R.
Smith, Joshua T.
Li, Jinfeng
Zhang, Xinglu
Wolfe, Kristin L.
Gao, Fengxiang
Benton, Christopher S.
Andam, Cheryl P.
author_sort Turcotte, Madison R.
collection PubMed
description BACKGROUND: The implementation of whole genome sequencing (WGS) by PulseNet, the molecular subtyping network for foodborne diseases, has transformed surveillance, outbreak detection, and public health laboratory practices in the United States. In 2017, the New Hampshire Public Health Laboratories, a member of PulseNet, commenced the use of WGS in tracking foodborne pathogens across the state. We present some of the initial results of New Hampshire’s initiative to transition to WGS in tracking Salmonella enterica, a bacterial pathogen that is responsible for non-typhoidal foodborne infections and enteric fever. We characterize the population structure and evolutionary history of 394 genomes of isolates recovered from human clinical cases in New Hampshire from 2017 to 2020. RESULTS: The New Hampshire S. enterica population is phylogenetically diverse, consisting of 78 sequence types (ST) and 67 serotypes. Six lineages dominate the population: ST 11 serotype Enteritidis, ST 19 Typhimurium, ST 32 Infantis, ST 118 Newport, ST 22 Braenderup, and ST 26 Thompson. Each lineage is derived from long ancestral branches in the phylogeny, suggesting their extended presence in the region and recent clonal expansion. We detected 61 genes associated with resistance to 14 antimicrobial classes. Of these, unique genes of five antimicrobial classes (aminocoumarins, aminoglycosides, fluoroquinolones, nitroimidazoles, and peptides) were detected in all genomes. Rather than a single clone carrying multiple resistance genes expanding in the state, we found multiple lineages carrying different combinations of independently acquired resistance determinants. We estimate the time to the most recent common ancestor of the predominant lineage ST 11 serotype Enteritidis (126 genomes) to be 1965 (95% highest posterior density intervals: 1927–1982). Its population size expanded until 1978, followed by a population decline until 1990. This lineage has been expanding since then. Comparison with genomes from other states reveal lack of geographical clustering indicative of long-distance dissemination. CONCLUSIONS: WGS studies of standing pathogen diversity provide critical insights into the population and evolutionary dynamics of lineages and antimicrobial resistance, which can be translated to effective public health action and decision-making. We highlight the need to strengthen efforts to implement WGS-based surveillance and genomic data analyses in state public health laboratories. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08769-1.
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spelling pubmed-93089392022-07-25 Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020 Turcotte, Madison R. Smith, Joshua T. Li, Jinfeng Zhang, Xinglu Wolfe, Kristin L. Gao, Fengxiang Benton, Christopher S. Andam, Cheryl P. BMC Genomics Research BACKGROUND: The implementation of whole genome sequencing (WGS) by PulseNet, the molecular subtyping network for foodborne diseases, has transformed surveillance, outbreak detection, and public health laboratory practices in the United States. In 2017, the New Hampshire Public Health Laboratories, a member of PulseNet, commenced the use of WGS in tracking foodborne pathogens across the state. We present some of the initial results of New Hampshire’s initiative to transition to WGS in tracking Salmonella enterica, a bacterial pathogen that is responsible for non-typhoidal foodborne infections and enteric fever. We characterize the population structure and evolutionary history of 394 genomes of isolates recovered from human clinical cases in New Hampshire from 2017 to 2020. RESULTS: The New Hampshire S. enterica population is phylogenetically diverse, consisting of 78 sequence types (ST) and 67 serotypes. Six lineages dominate the population: ST 11 serotype Enteritidis, ST 19 Typhimurium, ST 32 Infantis, ST 118 Newport, ST 22 Braenderup, and ST 26 Thompson. Each lineage is derived from long ancestral branches in the phylogeny, suggesting their extended presence in the region and recent clonal expansion. We detected 61 genes associated with resistance to 14 antimicrobial classes. Of these, unique genes of five antimicrobial classes (aminocoumarins, aminoglycosides, fluoroquinolones, nitroimidazoles, and peptides) were detected in all genomes. Rather than a single clone carrying multiple resistance genes expanding in the state, we found multiple lineages carrying different combinations of independently acquired resistance determinants. We estimate the time to the most recent common ancestor of the predominant lineage ST 11 serotype Enteritidis (126 genomes) to be 1965 (95% highest posterior density intervals: 1927–1982). Its population size expanded until 1978, followed by a population decline until 1990. This lineage has been expanding since then. Comparison with genomes from other states reveal lack of geographical clustering indicative of long-distance dissemination. CONCLUSIONS: WGS studies of standing pathogen diversity provide critical insights into the population and evolutionary dynamics of lineages and antimicrobial resistance, which can be translated to effective public health action and decision-making. We highlight the need to strengthen efforts to implement WGS-based surveillance and genomic data analyses in state public health laboratories. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08769-1. BioMed Central 2022-07-23 /pmc/articles/PMC9308939/ /pubmed/35870884 http://dx.doi.org/10.1186/s12864-022-08769-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Turcotte, Madison R.
Smith, Joshua T.
Li, Jinfeng
Zhang, Xinglu
Wolfe, Kristin L.
Gao, Fengxiang
Benton, Christopher S.
Andam, Cheryl P.
Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title_full Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title_fullStr Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title_full_unstemmed Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title_short Genome characteristics of clinical Salmonella enterica population from a state public health laboratory, New Hampshire, USA, 2017–2020
title_sort genome characteristics of clinical salmonella enterica population from a state public health laboratory, new hampshire, usa, 2017–2020
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9308939/
https://www.ncbi.nlm.nih.gov/pubmed/35870884
http://dx.doi.org/10.1186/s12864-022-08769-1
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