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mBio. 2019 Nov 26;10(6). pii: e01105-19. doi: 10.1128/mBio.01105-19.

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

Author information

1
Menzies School of Health Research, Darwin, Australia.
2
Australian Institute of Tropical Health and Medicine, Townsville, Australia.
3
Department of Microbiology and Immunology, University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia.
4
University of Mississippi Medical Center, Jackson, Mississippi, USA.
5
Leibniz Institute of Photonic Technology (IPHT), Jena, Germany.
6
InfectoGnostics Research Campus, Jena, Germany.
7
Technical University of Dresden, Dresden, Germany.
8
Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom.
9
Doherty Applied Microbial Genomics, Department of Microbiology & Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia.
10
Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia.
11
Public Health England, National Infection Service, London, United Kingdom.
12
Creighton University, Omaha, Nebraska, USA.
13
Scottish Microbiology Reference Laboratories, Glasgow, United Kingdom.
14
The Chinese University of Hong Kong, Hong Kong.
15
Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, Australia, and New Wales Health Pathology, Westmead Hospital, Sydney, Australia.
16
School of Veterinary and Laboratory Sciences, Murdoch University, Murdoch, Australia.
17
Statens Serum Institut, Copenhagen, Denmark.
18
National MRSA Reference Laboratory, St. James's Hospital, Dublin, Ireland.
19
Microbiology Research Unit, School of Dental Science, University of Dublin, Trinity College Dublin, Dublin, Ireland.
20
Istituto Superiore di Sanità, Rome, Italy.
21
Instituto de Tecnologia Química e Biológica, Oeiras, Portugal.
22
The Rockefeller University, New York, New York, USA.
23
University of Copenhagen, Copenhagen, Denmark.
24
Hvidovre University Hospital, Hvidovre, Denmark.
25
Sapporo Medical University, Sapporo, Japan.
26
Institute of Environmental Science and Research, Wellington, New Zealand.
27
Robert Koch Institute, Wernigerode, Germany.
28
Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates.
29
Akershus University Hospital, Lørenskog, Norway.
30
King Fahd Medical City, Riyadh, Kingdom of Saudi Arabia.
31
London School of Hygiene and Tropical Medicine, London, United Kingdom.
32
Sunshine Coast University, Sippy Downs, Australia.
33
Wellcome Sanger Institute, Cambridge, United Kingdom.
34
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
35
School of Cellular and Molecular Medicine, University of Bristol, Bristol, United Kingdom.
36
University of St. Andrews, St. Andrews, United Kingdom.
37
Menzies School of Health Research, Darwin, Australia steven.tong@mh.org.au.
38
Victorian Infectious Disease Service, The Royal Melbourne Hospital, and Doherty Department, University of Melbourne, Peter Doherty Institute for Infection and Immunity, Victoria, Australia.

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:

Bengal Bay; CA-MRSA; India; ST772; South Asia; Staphylococcus aureus ; WGS; antimicrobial resistance; genomic epidemiology; global transmission; phenotyping; phylodynamics

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