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Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent

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Harvard

Steinig, EJ, Duchene, S, Robinson, DA, Monecke, S, Yokoyama, M, Laabei, M, Slickers, P, Andersson, P, Williamson, D, Kearns, A, Goering, RV, Dickson, E, Ehricht, R, Ip, M, O'Sullivan, MVN, Coombs, GW, Petersen, A, Brennan, G, Shore, AC, Coleman, DC, Pantosti, A, de Lencastre, H, Westh, H, Kobayashi, N, Heffernan, H, Strommenger, B, Layer, F, Weber, S, Aamot, HV, Skakni, L, Peacock, SJ, Sarovich, D, Harris, S, Parkhill, J, Massey, RC, Holden, MTG, Bentley, SD & Tong, SYC 2019, 'Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent' mBio, bind 10, nr. 6, s. 1-20. https://doi.org/10.1128/mBio.01105-19

APA

CBE

Steinig EJ, Duchene S, Robinson DA, Monecke S, Yokoyama M, Laabei M, Slickers P, Andersson P, Williamson D, Kearns A, Goering RV, Dickson E, Ehricht R, Ip M, O'Sullivan MVN, Coombs GW, Petersen A, Brennan G, Shore AC, Coleman DC, Pantosti A, de Lencastre H, Westh H, Kobayashi N, Heffernan H, Strommenger B, Layer F, Weber S, Aamot HV, Skakni L, Peacock SJ, Sarovich D, Harris S, Parkhill J, Massey RC, Holden MTG, Bentley SD, Tong SYC. 2019. Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent. mBio. 10(6):1-20. https://doi.org/10.1128/mBio.01105-19

MLA

Vancouver

Author

Steinig, Eike J ; Duchene, Sebastian ; Robinson, D Ashley ; Monecke, Stefan ; Yokoyama, Maho ; Laabei, Maisem ; Slickers, Peter ; Andersson, Patiyan ; Williamson, Deborah ; Kearns, Angela ; Goering, Richard V ; Dickson, Elizabeth ; Ehricht, Ralf ; Ip, Margaret ; O'Sullivan, Matthew V N ; Coombs, Geoffrey W ; Petersen, Andreas ; Brennan, Grainne ; Shore, Anna C ; Coleman, David C ; Pantosti, Annalisa ; de Lencastre, Herminia ; Westh, Henrik ; Kobayashi, Nobumichi ; Heffernan, Helen ; Strommenger, Birgit ; Layer, Franziska ; Weber, Stefan ; Aamot, Hege Vangstein ; Skakni, Leila ; Peacock, Sharon J ; Sarovich, Derek ; Harris, Simon ; Parkhill, Julian ; Massey, Ruth C ; Holden, Mathew T G ; Bentley, Stephen D ; Tong, Steven Y C. / Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent. I: mBio. 2019 ; Bind 10, Nr. 6. s. 1-20.

Bibtex

@article{6a456d00f2ee4fc49198c0c5adf84c6d,
title = "Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent",
abstract = "The evolution and global transmission of antimicrobial resistance have been well documented for Gram-negative bacteria and health care-associated epidemic pathogens, often emerging from regions with heavy antimicrobial use. However, the degree to which similar processes occur with Gram-positive bacteria in the community setting is less well understood. In this study, we traced the recent origins and global spread of a multidrug-resistant, community-associated Staphylococcus aureus lineage from the Indian subcontinent, the Bengal Bay clone (ST772). We generated whole-genome sequence data of 340 isolates from 14 countries, including the first isolates from Bangladesh and India, to reconstruct the evolutionary history and genomic epidemiology of the lineage. Our data show that the clone emerged on the Indian subcontinent in the early 1960s and disseminated rapidly in the 1990s. Short-term outbreaks in community and health care settings occurred following intercontinental transmission, typically associated with travel and family contacts on the subcontinent, but ongoing endemic transmission was uncommon. Acquisition of a multidrug resistance integrated plasmid was instrumental in the emergence of a single dominant and globally disseminated clade in the early 1990s. Phenotypic data on biofilm, growth, and toxicity point to antimicrobial resistance as the driving force in the evolution of ST772. The Bengal Bay clone therefore combines the multidrug resistance of traditional health care-associated clones with the epidemiological transmission of community-associated methicillin-resistant S. aureus (MRSA). Our study demonstrates the importance of whole-genome sequencing for tracking the evolution of emerging and resistant pathogens. It provides a critical framework for ongoing surveillance of the clone on the Indian subcontinent and elsewhere.IMPORTANCE The Bengal Bay clone (ST772) is a community-associated and multidrug-resistant Staphylococcus aureus lineage first isolated from Bangladesh and India in 2004. In this study, we showed that the Bengal Bay clone emerged from a virulent progenitor circulating on the Indian subcontinent. Its subsequent global transmission was associated with travel or family contact in the region. ST772 progressively acquired specific resistance elements at limited cost to its fitness and continues to be exported globally, resulting in small-scale community and health care outbreaks. The Bengal Bay clone therefore combines the virulence potential and epidemiology of community-associated clones with the multidrug resistance of health care-associated S. aureus lineages. This study demonstrates the importance of whole-genome sequencing for the surveillance of highly antibiotic-resistant pathogens, which may emerge in the community setting of regions with poor antibiotic stewardship and rapidly spread into hospitals and communities across the world.",
author = "Steinig, {Eike J} and Sebastian Duchene and Robinson, {D Ashley} and Stefan Monecke and Maho Yokoyama and Maisem Laabei and Peter Slickers and Patiyan Andersson and Deborah Williamson and Angela Kearns and Goering, {Richard V} and Elizabeth Dickson and Ralf Ehricht and Margaret Ip and O'Sullivan, {Matthew V N} and Coombs, {Geoffrey W} and Andreas Petersen and Grainne Brennan and Shore, {Anna C} and Coleman, {David C} and Annalisa Pantosti and {de Lencastre}, Herminia and Henrik Westh and Nobumichi Kobayashi and Helen Heffernan and Birgit Strommenger and Franziska Layer and Stefan Weber and Aamot, {Hege Vangstein} and Leila Skakni and Peacock, {Sharon J} and Derek Sarovich and Simon Harris and Julian Parkhill and Massey, {Ruth C} and Holden, {Mathew T G} and Bentley, {Stephen D} and Tong, {Steven Y C}",
note = "Copyright {\circledC} 2019 Steinig et al.",
year = "2019",
month = "11",
day = "26",
doi = "10.1128/mBio.01105-19",
language = "English",
volume = "10",
pages = "1--20",
journal = "mBio",
issn = "2161-2129",
publisher = "American Society for Microbiology",
number = "6",

}

RIS

TY - JOUR

T1 - Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent

AU - Steinig, Eike J

AU - Duchene, Sebastian

AU - Robinson, D Ashley

AU - Monecke, Stefan

AU - Yokoyama, Maho

AU - Laabei, Maisem

AU - Slickers, Peter

AU - Andersson, Patiyan

AU - Williamson, Deborah

AU - Kearns, Angela

AU - Goering, Richard V

AU - Dickson, Elizabeth

AU - Ehricht, Ralf

AU - Ip, Margaret

AU - O'Sullivan, Matthew V N

AU - Coombs, Geoffrey W

AU - Petersen, Andreas

AU - Brennan, Grainne

AU - Shore, Anna C

AU - Coleman, David C

AU - Pantosti, Annalisa

AU - de Lencastre, Herminia

AU - Westh, Henrik

AU - Kobayashi, Nobumichi

AU - Heffernan, Helen

AU - Strommenger, Birgit

AU - Layer, Franziska

AU - Weber, Stefan

AU - Aamot, Hege Vangstein

AU - Skakni, Leila

AU - Peacock, Sharon J

AU - Sarovich, Derek

AU - Harris, Simon

AU - Parkhill, Julian

AU - Massey, Ruth C

AU - Holden, Mathew T G

AU - Bentley, Stephen D

AU - Tong, Steven Y C

N1 - Copyright © 2019 Steinig et al.

PY - 2019/11/26

Y1 - 2019/11/26

N2 - The evolution and global transmission of antimicrobial resistance have been well documented for Gram-negative bacteria and health care-associated epidemic pathogens, often emerging from regions with heavy antimicrobial use. However, the degree to which similar processes occur with Gram-positive bacteria in the community setting is less well understood. In this study, we traced the recent origins and global spread of a multidrug-resistant, community-associated Staphylococcus aureus lineage from the Indian subcontinent, the Bengal Bay clone (ST772). We generated whole-genome sequence data of 340 isolates from 14 countries, including the first isolates from Bangladesh and India, to reconstruct the evolutionary history and genomic epidemiology of the lineage. Our data show that the clone emerged on the Indian subcontinent in the early 1960s and disseminated rapidly in the 1990s. Short-term outbreaks in community and health care settings occurred following intercontinental transmission, typically associated with travel and family contacts on the subcontinent, but ongoing endemic transmission was uncommon. Acquisition of a multidrug resistance integrated plasmid was instrumental in the emergence of a single dominant and globally disseminated clade in the early 1990s. Phenotypic data on biofilm, growth, and toxicity point to antimicrobial resistance as the driving force in the evolution of ST772. The Bengal Bay clone therefore combines the multidrug resistance of traditional health care-associated clones with the epidemiological transmission of community-associated methicillin-resistant S. aureus (MRSA). Our study demonstrates the importance of whole-genome sequencing for tracking the evolution of emerging and resistant pathogens. It provides a critical framework for ongoing surveillance of the clone on the Indian subcontinent and elsewhere.IMPORTANCE The Bengal Bay clone (ST772) is a community-associated and multidrug-resistant Staphylococcus aureus lineage first isolated from Bangladesh and India in 2004. In this study, we showed that the Bengal Bay clone emerged from a virulent progenitor circulating on the Indian subcontinent. Its subsequent global transmission was associated with travel or family contact in the region. ST772 progressively acquired specific resistance elements at limited cost to its fitness and continues to be exported globally, resulting in small-scale community and health care outbreaks. The Bengal Bay clone therefore combines the virulence potential and epidemiology of community-associated clones with the multidrug resistance of health care-associated S. aureus lineages. This study demonstrates the importance of whole-genome sequencing for the surveillance of highly antibiotic-resistant pathogens, which may emerge in the community setting of regions with poor antibiotic stewardship and rapidly spread into hospitals and communities across the world.

AB - The evolution and global transmission of antimicrobial resistance have been well documented for Gram-negative bacteria and health care-associated epidemic pathogens, often emerging from regions with heavy antimicrobial use. However, the degree to which similar processes occur with Gram-positive bacteria in the community setting is less well understood. In this study, we traced the recent origins and global spread of a multidrug-resistant, community-associated Staphylococcus aureus lineage from the Indian subcontinent, the Bengal Bay clone (ST772). We generated whole-genome sequence data of 340 isolates from 14 countries, including the first isolates from Bangladesh and India, to reconstruct the evolutionary history and genomic epidemiology of the lineage. Our data show that the clone emerged on the Indian subcontinent in the early 1960s and disseminated rapidly in the 1990s. Short-term outbreaks in community and health care settings occurred following intercontinental transmission, typically associated with travel and family contacts on the subcontinent, but ongoing endemic transmission was uncommon. Acquisition of a multidrug resistance integrated plasmid was instrumental in the emergence of a single dominant and globally disseminated clade in the early 1990s. Phenotypic data on biofilm, growth, and toxicity point to antimicrobial resistance as the driving force in the evolution of ST772. The Bengal Bay clone therefore combines the multidrug resistance of traditional health care-associated clones with the epidemiological transmission of community-associated methicillin-resistant S. aureus (MRSA). Our study demonstrates the importance of whole-genome sequencing for tracking the evolution of emerging and resistant pathogens. It provides a critical framework for ongoing surveillance of the clone on the Indian subcontinent and elsewhere.IMPORTANCE The Bengal Bay clone (ST772) is a community-associated and multidrug-resistant Staphylococcus aureus lineage first isolated from Bangladesh and India in 2004. In this study, we showed that the Bengal Bay clone emerged from a virulent progenitor circulating on the Indian subcontinent. Its subsequent global transmission was associated with travel or family contact in the region. ST772 progressively acquired specific resistance elements at limited cost to its fitness and continues to be exported globally, resulting in small-scale community and health care outbreaks. The Bengal Bay clone therefore combines the virulence potential and epidemiology of community-associated clones with the multidrug resistance of health care-associated S. aureus lineages. This study demonstrates the importance of whole-genome sequencing for the surveillance of highly antibiotic-resistant pathogens, which may emerge in the community setting of regions with poor antibiotic stewardship and rapidly spread into hospitals and communities across the world.

U2 - 10.1128/mBio.01105-19

DO - 10.1128/mBio.01105-19

M3 - Journal article

VL - 10

SP - 1

EP - 20

JO - mBio

JF - mBio

SN - 2161-2129

IS - 6

ER -

ID: 58465167