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, Mathew T.G. Holden, Stephen D. Bentley, Steven Y.C. Tong

    Research output: Contribution to journalArticleResearchpeer-review

    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.

    Original languageEnglish
    Article numbere01105-19
    Pages (from-to)1-20
    Number of pages20
    JournalmBio
    Volume10
    Issue number6
    DOIs
    Publication statusPublished - 26 Nov 2019

    Fingerprint

    Methicillin-Resistant Staphylococcus aureus
    Clone Cells
    Multiple Drug Resistance
    Staphylococcus aureus
    Community Health Services
    Bangladesh
    Genome
    Delivery of Health Care
    Disease Outbreaks
    India
    Epidemiology
    Anti-Bacterial Agents
    Gram-Positive Bacteria
    Biofilms
    Gram-Negative Bacteria
    Virulence
    Plasmids
    History
    Costs and Cost Analysis
    Growth

    Cite this

    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. In: mBio. 2019 ; Vol. 10, No. 6. pp. 1-20.
    @article{e33f95ebb31844f1a2643398883d0fbf,
    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.",
    keywords = "antimicrobial resistance, Bengal Bay, CA-MRSA, genomic epidemiology, global transmission, India, phenotyping, phylodynamics, South Asia, ST772, Staphylococcus aureus, WGS",
    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.}",
    year = "2019",
    month = "11",
    day = "26",
    doi = "10.1128/mBio.01105-19",
    language = "English",
    volume = "10",
    pages = "1--20",
    journal = "mBio",
    issn = "2150-7511",
    publisher = "American Society for Microbiology",
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    }

    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, vol. 10, no. 6, e01105-19, pp. 1-20. https://doi.org/10.1128/mBio.01105-19

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

    In: mBio, Vol. 10, No. 6, e01105-19, 26.11.2019, p. 1-20.

    Research output: Contribution to journalArticleResearchpeer-review

    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.

    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.

    KW - antimicrobial resistance

    KW - Bengal Bay

    KW - CA-MRSA

    KW - genomic epidemiology

    KW - global transmission

    KW - India

    KW - phenotyping

    KW - phylodynamics

    KW - South Asia

    KW - ST772

    KW - Staphylococcus aureus

    KW - WGS

    UR - http://www.scopus.com/inward/record.url?scp=85075641618&partnerID=8YFLogxK

    U2 - 10.1128/mBio.01105-19

    DO - 10.1128/mBio.01105-19

    M3 - Article

    VL - 10

    SP - 1

    EP - 20

    JO - mBio

    JF - mBio

    SN - 2150-7511

    IS - 6

    M1 - e01105-19

    ER -