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

Eike J. Steinig, Sebastian Duchene, D. Ashley-Robinson, Stefan Monecke, Maho Yokoyama, Maisem Laabei, Peter Slickers, Patiyan Andersson, Deborah Williamson, Angela Kearns, Richard V. Goering, Elizabeth Dickson, Ralf Ehricht, Margaret Ip, Matthew V. N. O'Sullivan, Geoffrey W. Coombs, Andreas Petersen, Grainne Brennan, Anna C. Shore, David C. Coleman & 18 others Annalisa Pantosti, Herminia De Lencastre, Henrik Westh, Nobumichi Kobayashi, Helen Heffernan, Birgit Strommenger, Franziska Layer, Stefan Weber, Hege Vangstein Aamot, Leila Skakni, Sharon J. Peacock, Derek Sarovich, Simon Harris, Julian Parkhill, Ruth C. Massey, Matthew T. G. Holden, Stephen D. Bentley, Stephen Y. C. Tong

Research output: Contribution to journalArticle

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.
Original languageEnglish
Article numbere01105-19
Number of pages20
JournalmBio
Volume10
Issue number6
Early online date26 Nov 2019
DOIs
Publication statusPublished - 26 Nov 2019

Cite this

Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent. / Steinig, Eike J.; Duchene, Sebastian; Ashley-Robinson, D.; 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; Vangstein Aamot, Hege; Skakni, Leila; Peacock, Sharon J.; Sarovich, Derek; Harris, Simon; Parkhill, Julian; Massey, Ruth C.; Holden, Matthew T. G.; Bentley, Stephen D.; Tong, Stephen Y. C.

In: mBio, Vol. 10, No. 6, e01105-19, 26.11.2019.

Research output: Contribution to journalArticle

Steinig, EJ, Duchene, S, Ashley-Robinson, D, 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, Vangstein Aamot, H, 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, vol. 10, no. 6, e01105-19. https://doi.org/10.1128/mBio.01105-19.
Steinig, Eike J. ; Duchene, Sebastian ; Ashley-Robinson, D. ; 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 ; Vangstein Aamot, Hege ; Skakni, Leila ; Peacock, Sharon J. ; Sarovich, Derek ; Harris, Simon ; Parkhill, Julian ; Massey, Ruth C. ; Holden, Matthew T. G. ; Bentley, Stephen D. ; Tong, Stephen Y. C. / Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant Staphylococcus aureus Lineage from the Indian Subcontinent. In: mBio. 2019 ; Vol. 10, No. 6.
@article{304d51435bf649d18cc8f7f86f060dbd,
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.",
author = "Steinig, {Eike J.} and Sebastian Duchene and D. Ashley-Robinson 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 {Vangstein Aamot}, Hege and Leila Skakni and Peacock, {Sharon J.} and Derek Sarovich and Simon Harris and Julian Parkhill and Massey, {Ruth C.} and Holden, {Matthew T. G.} and Bentley, {Stephen D.} and Tong, {Stephen Y. C.}",
year = "2019",
month = "11",
day = "26",
doi = "10.1128/mBio.01105-19.",
language = "English",
volume = "10",
journal = "mBio",
issn = "2161-2129",
publisher = "American Society for Microbiology",
number = "6",

}

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 - Ashley-Robinson, D.

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 - Vangstein Aamot, Hege

AU - Skakni, Leila

AU - Peacock, Sharon J.

AU - Sarovich, Derek

AU - Harris, Simon

AU - Parkhill, Julian

AU - Massey, Ruth C.

AU - Holden, Matthew T. G.

AU - Bentley, Stephen D.

AU - Tong, Stephen Y. C.

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.

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.

U2 - 10.1128/mBio.01105-19.

DO - 10.1128/mBio.01105-19.

M3 - Article

VL - 10

JO - mBio

JF - mBio

SN - 2161-2129

IS - 6

M1 - e01105-19

ER -