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Microbial Ecology

Long-Term Colonization Dynamics of Enterococcus faecalis in Implanted Devices in Research Macaques

Mia T. Lieberman, Daria Van Tyne, JoAnn Dzink-Fox, Eric J. Ma, Michael S. Gilmore, James G. Fox
Harold L. Drake, Editor
Mia T. Lieberman
Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, USADepartment of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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  • ORCID record for Mia T. Lieberman
Daria Van Tyne
Department of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USADepartment of Microbiology and Immunobiology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
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JoAnn Dzink-Fox
Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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Eric J. Ma
Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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Michael S. Gilmore
Department of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USADepartment of Microbiology and Immunobiology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
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James G. Fox
Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, USADepartment of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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Harold L. Drake
University of Bayreuth
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DOI: 10.1128/AEM.01336-18
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ABSTRACT

Enterococcus faecalis is a common opportunistic pathogen that colonizes cephalic recording chambers (CRCs) of macaques used in cognitive neuroscience research. We previously characterized 15 E. faecalis strains isolated from macaques at the Massachusetts Institute of Technology (MIT) in 2011. The goal of this study was to examine how a 2014 protocol change prohibiting the use of antimicrobials within CRCs affected colonizing E. faecalis strains. We collected 20 E. faecalis isolates from 10 macaques between 2013 and 2017 for comparison to 4 isolates previously characterized in 2011 with respect to the sequence type (ST) distribution, antimicrobial resistance, biofilm formation, and changes in genes that might confer a survival advantage. ST4 and ST55 were predominant among the isolates characterized in 2011, whereas the less antimicrobial-resistant lineage ST48 emerged to dominance after 2013. Two macaques remained colonized by ST4 and ST55 strains for 5 and 4 years, respectively. While the antimicrobial resistance and virulence factors identified in these ST4 and ST55 strains remained relatively stable, we detected an increase in biofilm formation ability over time in both isolates. We also found that ST48 strains were typically robust biofilm formers, which could explain why this ST increased in prevalence. Finally, we identified mutations in the DNA mismatch repair genes mutS and mutL in separate ST55 and ST4 strains and confirmed that strains bearing these mutations displayed a hypermutator phenotype. The presence of a hypermutator phenotype may complicate future antimicrobial treatment for clinically relevant E. faecalis infections in macaques.

IMPORTANCE Enterococcus faecalis is a common cause of health care-associated infections in humans, largely due to its ability to persist in the hospital environment, colonize patients, acquire antimicrobial resistance, and form biofilms. Understanding how enterococci evolve in health care settings provides insight into factors affecting enterococcal survival and persistence. Macaques used in neuroscience research have long-term cranial implants that, despite best practices, often become colonized by E. faecalis. This provides a unique opportunity to noninvasively examine the evolution of enterococci on a long-term indwelling device. We collected E. faecalis strains from cephalic implants over a 7-year period and characterized the sequence type, antimicrobial resistance, virulence factors, biofilm production, and hypermutator phenotypes. Improved antimicrobial stewardship allowed a less-antimicrobial-resistant E. faecalis strain to predominate at the implant interface, potentially improving antimicrobial treatment outcomes if future clinical infections occur. Biofilm formation appears to play an important role in the persistence of the E. faecalis strains associated with these implants.

FOOTNOTES

    • Received 1 June 2018.
    • Accepted 10 July 2018.
    • Accepted manuscript posted online 13 July 2018.
  • Address correspondence to Mia T. Lieberman, mtrl01{at}mit.edu, or James G. Fox, jgfox{at}mit.edu.
  • Citation Lieberman MT, Van Tyne D, Dzink-Fox J, Ma EJ, Gilmore MS, Fox JG. 2018. Long-term colonization dynamics of Enterococcus faecalis in implanted devices in research macaques. Appl Environ Microbiol 84:e01336-18. https://doi.org/10.1128/AEM.01336-18.

  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01336-18.

  • Copyright © 2018 American Society for Microbiology.

All Rights Reserved.

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Long-Term Colonization Dynamics of Enterococcus faecalis in Implanted Devices in Research Macaques
Mia T. Lieberman, Daria Van Tyne, JoAnn Dzink-Fox, Eric J. Ma, Michael S. Gilmore, James G. Fox
Appl. Environ. Microbiol. Aug 2018, 84 (18) e01336-18; DOI: 10.1128/AEM.01336-18

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Long-Term Colonization Dynamics of Enterococcus faecalis in Implanted Devices in Research Macaques
Mia T. Lieberman, Daria Van Tyne, JoAnn Dzink-Fox, Eric J. Ma, Michael S. Gilmore, James G. Fox
Appl. Environ. Microbiol. Aug 2018, 84 (18) e01336-18; DOI: 10.1128/AEM.01336-18
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KEYWORDS

Enterococcus faecalis
animal models
antibiotic resistance
biofilms
implant
macaque
One Health

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Print ISSN: 0099-2240; Online ISSN: 1098-5336