Preprint open access publication

Evolution and global transmission of a multidrug-resistant, community-associated MRSA lineage from the Indian subcontinent

bioRxiv, Cold Spring Harbor Laboratory,

2017

DOI:10.1101/233395, Dimensions: pub.1099740933,

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  1. (1) Australian Institute of Tropical Health and Medicine, grid.488664.0
  2. (2) Menzies School of Health Research, grid.271089.5
  3. (3) University of Melbourne, grid.1008.9
  4. (4) University of Mississippi Medical Center, grid.410721.1
  5. (5) TU Dresden, grid.4488.0
  6. (6) InfectoGnostics Research Campus, Jena, Germany
  7. (7) Abbott (Germany), grid.472830.a
  8. (8) University of Bath, grid.7340.0
  9. (9) Public Health England, grid.271308.f
  10. (10) Creighton University, grid.254748.8
  11. (11) Scottish Microbiology Reference Laboratories, Glasgow, United Kingdom
  12. (12) Chinese University of Hong Kong, grid.10784.3a
  13. (13) University of Sydney, grid.1013.3
  14. (14) Murdoch University, grid.1025.6
  15. (15) State Serum Institute, grid.6203.7
  16. (16) St. James's Hospital, grid.416409.e
  17. (17) Trinity College Dublin, grid.8217.c
  18. (18) Istituto Superiore di Sanità, grid.416651.1
  19. (19) Rockefeller University, grid.134907.8
  20. (20) Universidade Nova de Lisboa, grid.10772.33
  21. (21) Hvidovre Hospital, grid.411905.8, Capital Region
  22. (22) University of Copenhagen, grid.5254.6, KU
  23. (23) Sapporo Medical University, grid.263171.0
  24. (24) Institute of Environmental Science and Research, grid.419706.d
  25. (25) Robert Koch Institute, grid.13652.33
  26. (26) Shaikh Khalifa Medical City, grid.415670.1
  27. (27) Akershus University Hospital, grid.411279.8
  28. (28) King Fahd Medical City, grid.415277.2
  29. (29) London School of Hygiene & Tropical Medicine, grid.8991.9
  30. (30) University of the Sunshine Coast, grid.1034.6
  31. (31) Wellcome Sanger Institute, grid.10306.34
  32. (32) University of Bristol, grid.5337.2
  33. (33) University of St Andrews, grid.11914.3c
  34. (34) Victorian Infectious Disease Service, The Royal Melbourne Hospital, and The University of Melbourne, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Australia

Description

Abstract The evolution and global transmission of antimicrobial resistance has been well documented in Gram-negative bacteria and healthcare-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. Here, we trace 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 shows that the clone emerged on the Indian subcontinent in the early 1970s and disseminated rapidly in the 1990s. Short-term outbreaks in community and healthcare 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 divergence 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 healthcare-associated clones with the epidemiological transmission of community-associated 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-acquired and multidrug-resistant Staphylococcus aureus lineage first isolated from Bangladesh and India in 2004. In this study, we show 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 healthcare outbreaks. The Bengal Bay clone therefore combines the virulence potential and epidemiology of community-associated clones with the multidrug-resistance of healthcare-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.

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