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1 April 2008

Volume 197, Number 7
The Journal of Infectious Diseases 2008;197:1028–1035
© 2008 by the Infectious Diseases Society of America. All rights reserved.
0022-1899/2008/19707-0015$15.00
DOI: 10.1086/528992
MAJOR ARTICLE

Biofilm Formation Induces C3a Release and Protects Staphylococcus epidermidis from IgG and Complement Deposition and from Neutrophil‐Dependent Killing

Sascha A. Kristian,1,a

Timo A. Birkenstock,3

Ursula Sauder,2

Dietrich Mack,4

Friedrich Götz,3 and

Regine Landmann1

1Division of Infectious Diseases, Department of Research, University Hospitals Basel, and 2Center for Microscopy, Pharmazentrum, Basel, Switzerland; 3Microbial Genetics, University of Tübingen, Tübingen, Germany; 4Medical Microbiology and Infectious Diseases, School of Medicine, University of Wales Swansea, Swansea, United Kingdom

Background.Biofilm formation is considered to be an important virulence factor of the opportunistic pathogen Staphylococcus epidermidis. We hypothesized that biofilm formation could interfere with the deposition of immunoglobulins and complement on the bacterial surface, leading to diminished activation of the complement system and protection from killing by human phagocytes.

Methods.The killing of biofilm‐encased and planktonically grown wild‐type (wt) S. epidermidis and the killing of an isogenic biofilm‐negative ica mutant (ica−) by human polymorphonuclear neutrophils (PMNs) were compared. C3a induction and deposition of C3b and immunoglobulin G (IgG) on the bacteria after opsonization with human serum were assessed by enzyme‐linked immunosorbent assay, flow cytometry, and electron microscopy. The virulence of the bacterial strains was compared in a mouse model of catheter‐associated infection.

Results.Biofilm‐embedded wt S. epidermidis was killed less well by human PMNs and induced more C3a than planktonically grown wt and ica− S. epidermidis. However, the deposition of C3b and IgG on the bacterial surface was diminished in biofilm‐encased staphylococci. wt S. epidermidis was more virulent in implant‐associated infections and was killed more slowly than ica− in ex vivo assays of killing by PMNs.

Conclusions.The results indicate that prevention of C3b and IgG deposition on the bacterial surface contributes to the biofilm‐mediated protection of S. epidermidis from killing by PMNs.

Received 13 June 2007; accepted 10 October 2007; electronically published 4 March 2008.

Reprints or correspondence: Dr. Regine Landmann, Div. of Infectious Diseases, Dept. of Research, University Hospitals Basel, Hebelstrasse 20, CH‐4031 Basel, Switzerland ().

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Online publication date: 1-Mar-2009.
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D. Hudetz, S. Ursic Hudetz, L. G. Harris, R. Luginbühl, N. F. Friederich, R. Landmann. (2009) Weak effect of metal type and ica genes on staphylococcal infection of titanium and stainless steel implants. Clinical Microbiology and Infection 14:12, 1135-1145
Online publication date: 1-Jan-2009.
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K. Flemming, C. Klingenberg, J. P. Cavanagh, M. Sletteng, W. Stensen, J. S. Svendsen, T. Flaegstad. (2008) High in vitro antimicrobial activity of synthetic antimicrobial peptidomimetics against staphylococcal biofilms. Journal of Antimicrobial Chemotherapy 63:1, 136-145
Online publication date: 18-Nov-2008.
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  • Potential conflicts of interest: none reported.

    Presented in part: 11th International Symposium on Staphylococci and Staphylococcal Infections, Charleston, South Carolina, 24–27 October 2004 (abstract PA‐20); International Endotoxin and Innate Immunity Society, Kyoto, Japan, 15–18 November 2004 (abstract 188A).

    Financial support: AO Research Foundation (grant 03‐L63 to R.L.).

  • Present affiliation: Division of Pediatric Infectious Diseases, Department of Pediatrics, University of California, San Diego, La Jolla.

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