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.
KW - Anti-Bacterial Agents/pharmacology
KW - Asia/epidemiology
KW - Community-Acquired Infections/epidemiology
KW - Drug Resistance, Multiple, Bacterial
KW - Evolution, Molecular
KW - Genome, Bacterial
KW - Humans
KW - India
KW - Methicillin-Resistant Staphylococcus aureus/classification
KW - Phylogeny
KW - Staphylococcal Infections/epidemiology
KW - Staphylococcus aureus/classification
U2 - 10.1128/mBio.01105-19
DO - 10.1128/mBio.01105-19
M3 - Article (Academic Journal)
C2 - 31772058
SN - 2161-2129
VL - 10
JO - mBio
JF - mBio
IS - 6
ER -