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Epidemiology and Surveillance

Topical Antibiotic Use Coselects for the Carriage of Mobile Genetic Elements Conferring Resistance to Unrelated Antimicrobials in Staphylococcus aureus

Glen P. Carter, Mark B. Schultz, Sarah L. Baines, Anders Gonçalves da Silva, Helen Heffernan, Audrey Tiong, Peter H. Pham, Ian R. Monk, Timothy P. Stinear, Benjamin P. Howden, Deborah A. Williamson
Glen P. Carter
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Mark B. Schultz
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Sarah L. Baines
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Anders Gonçalves da Silva
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Helen Heffernan
Institute of Environmental Science and Research, Wellington, New Zealand
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Audrey Tiong
Institute of Environmental Science and Research, Wellington, New Zealand
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Peter H. Pham
Doherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Ian R. Monk
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Timothy P. Stinear
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Benjamin P. Howden
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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Deborah A. Williamson
Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, AustraliaDoherty Applied Microbial Genomics, Doherty Institute, The University of Melbourne, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology & Immunology, Doherty Institute, The University of Melbourne, Melbourne, Australia
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DOI: 10.1128/AAC.02000-17
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ABSTRACT

Topical antibiotics, such as mupirocin and fusidic acid, are commonly used in the prevention and treatment of skin infections, particularly those caused by staphylococci. However, the widespread use of these agents is associated with increased resistance to these agents, potentially limiting their efficacy. Of particular concern is the observation that resistance to topical antibiotics is often associated with multidrug resistance, suggesting that topical antibiotics may play a role in the emergence of multidrug-resistant (MDR) strains. New Zealand (NZ) has some of the highest globally recorded rates of topical antibiotic usage and resistance. Using a combination of Pacific Biosciences single-molecule real-time (SMRT) whole-genome sequencing, Illumina short-read sequencing, and Bayesian phylogenomic modeling on 118 new multilocus sequence type 1 (ST1) community Staphylococcus aureus isolates from New Zealand and 61 publically available international ST1 genome sequences, we demonstrate a strong correlation between the clinical introduction of topical antibiotics and the emergence of MDR ST1 S. aureus. We also provide in vitro experimental evidence showing that exposure to topical antibiotics can lead to the rapid selection of MDR S. aureus isolates carrying plasmids that confer resistance to multiple unrelated antibiotics, from within a mixed population of competitor strains. These findings have important implications regarding the impact of the indiscriminate use of topical antibiotics.

FOOTNOTES

    • Received 29 September 2017.
    • Returned for modification 30 October 2017.
    • Accepted 27 November 2017.
    • Accepted manuscript posted online 11 December 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AAC.02000-17.

  • Copyright © 2018 Carter et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Topical Antibiotic Use Coselects for the Carriage of Mobile Genetic Elements Conferring Resistance to Unrelated Antimicrobials in Staphylococcus aureus
Glen P. Carter, Mark B. Schultz, Sarah L. Baines, Anders Gonçalves da Silva, Helen Heffernan, Audrey Tiong, Peter H. Pham, Ian R. Monk, Timothy P. Stinear, Benjamin P. Howden, Deborah A. Williamson
Antimicrobial Agents and Chemotherapy Jan 2018, 62 (2) e02000-17; DOI: 10.1128/AAC.02000-17

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Topical Antibiotic Use Coselects for the Carriage of Mobile Genetic Elements Conferring Resistance to Unrelated Antimicrobials in Staphylococcus aureus
Glen P. Carter, Mark B. Schultz, Sarah L. Baines, Anders Gonçalves da Silva, Helen Heffernan, Audrey Tiong, Peter H. Pham, Ian R. Monk, Timothy P. Stinear, Benjamin P. Howden, Deborah A. Williamson
Antimicrobial Agents and Chemotherapy Jan 2018, 62 (2) e02000-17; DOI: 10.1128/AAC.02000-17
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KEYWORDS

fusidic acid
mupirocin
Staphylococcus aureus
topical antibiotics
coselection
multidrug resistance
plasmids

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