Quantifying the natural history of biofilm formation in vivo during the establishment of chronic implant-associated Staphylococcus aureus osteomyelitis in mice to identify critical pathogen and host factors

J Orthop Res. 2015 Sep;33(9):1311-9. doi: 10.1002/jor.22907. Epub 2015 May 18.

Abstract

While it is well known that Staphylococcus aureus establishes chronic implant-associated osteomyelitis by generating and persisting in biofilm, research to elucidate pathogen, and host specific factors controlling this process has been limited due to the absence of a quantitative in vivo model. To address this, we developed a murine tibia implant model with ex vivo region of interest (ROI) imaging analysis by scanning electron microscopy (SEM). Implants were coated with Staphylococcus aureus strains (SH1000, UAMS-1, USA300LAC) with distinct in vitro biofilm phenotypes, were used to infect C57BL/6 or Balb/c mice. In contrast to their in vitro biofilm phenotype, results from all bacteria strains in vivo were similar, and demonstrated that biofilm on the implant is established within the first day, followed by a robust proliferation phase peaking on Day 3 in Balb/c mice, and persisting until Day 7 in C57BL/6 mice, as detected by SEM and bioluminescent imaging. Biofilm formation peaked at Day 14, covering ∼40% of the ROI coincident with massive agr-dependent bacterial emigration, as evidenced by large numbers of empty lacunae with few residual bacteria, which were largely culture negative (80%) and PCR positive (87.5%), supporting the clinical relevance of this implant model.

Keywords: Staphylococcus aureus; biofilm; implant; osteomyelitis; scanning electron microscopy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Biofilms*
  • Coated Materials, Biocompatible / chemistry*
  • Disease Models, Animal
  • Female
  • Materials Testing
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Microscopy, Electron, Scanning
  • Osteomyelitis / microbiology*
  • Phenotype
  • Polymerase Chain Reaction
  • Prostheses and Implants / microbiology*
  • Prosthesis-Related Infections / microbiology*
  • Species Specificity
  • Staphylococcal Infections / prevention & control*
  • Stem Cells
  • Tibia / drug effects

Substances

  • Anti-Bacterial Agents
  • Coated Materials, Biocompatible