Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 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-posi...
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American Society for Microbiology
2019
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antimicrobial resistance Bengal Bay CA-MRSA genomic epidemiology global transmission India Microbiology QR1-502 |
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antimicrobial resistance Bengal Bay CA-MRSA genomic epidemiology global transmission India Microbiology QR1-502 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 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 Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| description |
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. |
| format |
article |
| author |
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 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 |
| author_facet |
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 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 |
| author_sort |
Eike J. Steinig |
| title |
Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| title_short |
Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| title_full |
Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| title_fullStr |
Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| title_full_unstemmed |
Evolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent |
| title_sort |
evolution and global transmission of a multidrug-resistant, community-associated methicillin-resistant <named-content content-type="genus-species">staphylococcus aureus</named-content> lineage from the indian subcontinent |
| publisher |
American Society for Microbiology |
| publishDate |
2019 |
| url |
https://doaj.org/article/8270f31e2ec3455e9b0a91b665756b96 |
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oai:doaj.org-article:8270f31e2ec3455e9b0a91b665756b962021-11-15T15:54:47ZEvolution and Global Transmission of a Multidrug-Resistant, Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage from the Indian Subcontinent10.1128/mBio.01105-192150-7511https://doaj.org/article/8270f31e2ec3455e9b0a91b665756b962019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01105-19https://doaj.org/toc/2150-7511ABSTRACT 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.Eike J. SteinigSebastian DucheneD. Ashley RobinsonStefan MoneckeMaho YokoyamaMaisem LaabeiPeter SlickersPatiyan AnderssonDeborah WilliamsonAngela KearnsRichard V. GoeringElizabeth DicksonRalf EhrichtMargaret IpMatthew V. N. O’SullivanGeoffrey W. CoombsAndreas PetersenGrainne BrennanAnna C. ShoreDavid C. ColemanAnnalisa PantostiHerminia de LencastreHenrik WesthNobumichi KobayashiHelen HeffernanBirgit StrommengerFranziska LayerStefan WeberHege Vangstein AamotLeila SkakniSharon J. PeacockDerek SarovichSimon HarrisJulian ParkhillRuth C. MasseyMathew T. G. HoldenStephen D. BentleySteven Y. C. TongAmerican Society for Microbiologyarticleantimicrobial resistanceBengal BayCA-MRSAgenomic epidemiologyglobal transmissionIndiaMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019) |