Enhanced pathogenicity of biofilm-negative Staphylococcus epidermidis isolated from platelet preparations

Authors

  • Scott D. Hodgson,

    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
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    • These authors contributed equally to this work.
  • Valerie Greco-Stewart,

    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
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    • These authors contributed equally to this work.
  • Celine S. Jimenez,

    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
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  • Costi D. Sifri,

    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
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  • Ann Karen C. Brassinga,

    Corresponding author
    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
    • Address reprint requests to: Ann Karen C. Brassinga, Department of Microbiology (Fort Garry Campus), University of Manitoba, Room 418, Buller Building, 45 Chancellor's Circle, Winnipeg, MB, Canada, R3T 2N2; e-mail: karen_brassinga@umanitoba.ca.

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  • Sandra Ramirez-Arcos

    1. Department of Microbiology, Faculty of Science, University of Manitoba, Winnipeg, Manitoba, Canada
    2. Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
    3. Canadian Blood Services, Ottawa, Ontario, Canada
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  • This work was supported by University of Manitoba Start-Up funds, Natural Sciences and Engineering Research Council (NSERC), Manitoba Health Research Council (MHRC) Establishment Grant and Canadian Foundation for Innovation (CFI) to AKCB, a University of Manitoba Faculty of Science Undergraduate Student Research award to SDH and CJ, a University of Manitoba Vice President (Research) Undergraduate Student Summer Research Award to SDH, and a Canadian Blood Services Post-Doctoral Fellowship award to VGS. Additional funding of this research was provided by Canadian Blood Services and Health Canada to SRA and a Howard Hughes Medical Institute Early Career award to CDS.

Abstract

Background

The platelet (PLT) storage environment triggers the formation of surface-attached aggregates known as biofilms by the common PLT contaminant Staphylococcus epidermidis. The biofilm matrix is largely composed of polysaccharide intercellular adhesin (PIA) mediated by the icaADBC operon. However, PIA-negative S. epidermidis has been reported to form biofilms in PLT concentrates (PCs). Since biofilm formation is associated with increased virulence, this study was aimed at determining if PIA-negative S. epidermidis grown in PCs presents enhanced virulence using the nematode Caenorhabditis elegans as a host model for bacterial pathogenesis.

Study Design and Methods

Biofilm-positive S. epidermidis ATCC 35984 and 9142, which carry the icaADBC operon, and biofilm-negative S. epidermidis ATCC 12228 and 9142 ΔicaA were grown in regular media and in PCs and biofilm formation was quantified using a crystal violet assay. The virulence of these strains after passage through PCs was tested using nematode killing assays. Nematode survival was calculated using the Kaplan-Meier method and statistical differences were determined by log-rank analysis.

Results

All S. epidermidis strains were able to form biofilms in PCs. Although persistence of a biofilm-positive phenotype in the biofilm-negative strains grown in PCs was not observed after passage in regular medium, the virulence of all strains was significantly increased as demonstrated by shortened life spans of the nematodes in C. elegans killing assays.

Conclusion

Our findings highlight the potential of an increased risk of nosocomial infections caused by S. epidermidis in transfusion recipients since PC storage conditions promote biofilm formation, and possibly pathogenicity, of strains traditionally known to be attenuated for virulence.

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