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A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak

Whole-genome sequencing (WGS) of Staphylococcus aureus is increasingly used as part of infection prevention practices. In this study, we established a long-read technology-based WGS screening program of all first-episode methicillin-resistant Staphylococcus aureus (MRSA) blood infections at a major...

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Autores principales: Sullivan, Mitchell J., Altman, Deena R., Chacko, Kieran I., Ciferri, Brianne, Webster, Elizabeth, Pak, Theodore R., Deikus, Gintaras, Lewis-Sandari, Martha, Khan, Zenab, Beckford, Colleen, Rendo, Angela, Samaroo, Flora, Sebra, Robert, Karam-Howlin, Ramona, Dingle, Tanis, Hamula, Camille, Bashir, Ali, Schadt, Eric, Patel, Gopi, Wallach, Frances, Kasarskis, Andrew, Gibbs, Kathleen, van Bakel, Harm
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879278/
https://www.ncbi.nlm.nih.gov/pubmed/31578260
http://dx.doi.org/10.1128/JCM.01261-19
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author Sullivan, Mitchell J.
Altman, Deena R.
Chacko, Kieran I.
Ciferri, Brianne
Webster, Elizabeth
Pak, Theodore R.
Deikus, Gintaras
Lewis-Sandari, Martha
Khan, Zenab
Beckford, Colleen
Rendo, Angela
Samaroo, Flora
Sebra, Robert
Karam-Howlin, Ramona
Dingle, Tanis
Hamula, Camille
Bashir, Ali
Schadt, Eric
Patel, Gopi
Wallach, Frances
Kasarskis, Andrew
Gibbs, Kathleen
van Bakel, Harm
author_facet Sullivan, Mitchell J.
Altman, Deena R.
Chacko, Kieran I.
Ciferri, Brianne
Webster, Elizabeth
Pak, Theodore R.
Deikus, Gintaras
Lewis-Sandari, Martha
Khan, Zenab
Beckford, Colleen
Rendo, Angela
Samaroo, Flora
Sebra, Robert
Karam-Howlin, Ramona
Dingle, Tanis
Hamula, Camille
Bashir, Ali
Schadt, Eric
Patel, Gopi
Wallach, Frances
Kasarskis, Andrew
Gibbs, Kathleen
van Bakel, Harm
author_sort Sullivan, Mitchell J.
collection PubMed
description Whole-genome sequencing (WGS) of Staphylococcus aureus is increasingly used as part of infection prevention practices. In this study, we established a long-read technology-based WGS screening program of all first-episode methicillin-resistant Staphylococcus aureus (MRSA) blood infections at a major urban hospital. A survey of 132 MRSA genomes assembled from long reads enabled detailed characterization of an outbreak lasting several months of a CC5/ST105/USA100 clone among 18 infants in a neonatal intensive care unit (NICU). Available hospital-wide genome surveillance data traced the origins of the outbreak to three patients admitted to adult wards during a 4-month period preceding the NICU outbreak. The pattern of changes among complete outbreak genomes provided full spatiotemporal resolution of its progression, which was characterized by multiple subtransmissions and likely precipitated by equipment sharing between adults and infants. Compared to other hospital strains, the outbreak strain carried distinct mutations and accessory genetic elements that impacted genes with roles in metabolism, resistance, and persistence. This included a DNA recognition domain recombination in the hsdS gene of a type I restriction modification system that altered DNA methylation. Transcriptome sequencing (RNA-Seq) profiling showed that the (epi)genetic changes in the outbreak clone attenuated agr gene expression and upregulated genes involved in stress response and biofilm formation. Overall, our findings demonstrate the utility of long-read sequencing for hospital surveillance and for characterizing accessory genomic elements that may impact MRSA virulence and persistence.
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spelling pubmed-68792782019-12-03 A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak Sullivan, Mitchell J. Altman, Deena R. Chacko, Kieran I. Ciferri, Brianne Webster, Elizabeth Pak, Theodore R. Deikus, Gintaras Lewis-Sandari, Martha Khan, Zenab Beckford, Colleen Rendo, Angela Samaroo, Flora Sebra, Robert Karam-Howlin, Ramona Dingle, Tanis Hamula, Camille Bashir, Ali Schadt, Eric Patel, Gopi Wallach, Frances Kasarskis, Andrew Gibbs, Kathleen van Bakel, Harm J Clin Microbiol Epidemiology Whole-genome sequencing (WGS) of Staphylococcus aureus is increasingly used as part of infection prevention practices. In this study, we established a long-read technology-based WGS screening program of all first-episode methicillin-resistant Staphylococcus aureus (MRSA) blood infections at a major urban hospital. A survey of 132 MRSA genomes assembled from long reads enabled detailed characterization of an outbreak lasting several months of a CC5/ST105/USA100 clone among 18 infants in a neonatal intensive care unit (NICU). Available hospital-wide genome surveillance data traced the origins of the outbreak to three patients admitted to adult wards during a 4-month period preceding the NICU outbreak. The pattern of changes among complete outbreak genomes provided full spatiotemporal resolution of its progression, which was characterized by multiple subtransmissions and likely precipitated by equipment sharing between adults and infants. Compared to other hospital strains, the outbreak strain carried distinct mutations and accessory genetic elements that impacted genes with roles in metabolism, resistance, and persistence. This included a DNA recognition domain recombination in the hsdS gene of a type I restriction modification system that altered DNA methylation. Transcriptome sequencing (RNA-Seq) profiling showed that the (epi)genetic changes in the outbreak clone attenuated agr gene expression and upregulated genes involved in stress response and biofilm formation. Overall, our findings demonstrate the utility of long-read sequencing for hospital surveillance and for characterizing accessory genomic elements that may impact MRSA virulence and persistence. American Society for Microbiology 2019-11-22 /pmc/articles/PMC6879278/ /pubmed/31578260 http://dx.doi.org/10.1128/JCM.01261-19 Text en Copyright © 2019 Sullivan et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Epidemiology
Sullivan, Mitchell J.
Altman, Deena R.
Chacko, Kieran I.
Ciferri, Brianne
Webster, Elizabeth
Pak, Theodore R.
Deikus, Gintaras
Lewis-Sandari, Martha
Khan, Zenab
Beckford, Colleen
Rendo, Angela
Samaroo, Flora
Sebra, Robert
Karam-Howlin, Ramona
Dingle, Tanis
Hamula, Camille
Bashir, Ali
Schadt, Eric
Patel, Gopi
Wallach, Frances
Kasarskis, Andrew
Gibbs, Kathleen
van Bakel, Harm
A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title_full A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title_fullStr A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title_full_unstemmed A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title_short A Complete Genome Screening Program of Clinical Methicillin-Resistant Staphylococcus aureus Isolates Identifies the Origin and Progression of a Neonatal Intensive Care Unit Outbreak
title_sort complete genome screening program of clinical methicillin-resistant staphylococcus aureus isolates identifies the origin and progression of a neonatal intensive care unit outbreak
topic Epidemiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879278/
https://www.ncbi.nlm.nih.gov/pubmed/31578260
http://dx.doi.org/10.1128/JCM.01261-19
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