Advertisement

Prevalence of the ica operon and insertion sequence IS256 among Staphylococcus epidermidis prosthetic joint infection isolates

  • A. Koskela
  • Å. Nilsdotter-Augustinsson
  • L. Persson
  • B. SöderquistEmail author
Concise Article

Abstract

Joint replacement surgery has improved the quality of life for hundreds of thousands of patients. However, the infection of a joint implant is an important and serious complication, though the prevalence is low. Staphylococcus epidermidis is the most important pathogen involved in foreign-body infections. S. epidermidis is also a commensal that comprises a substantial part of the normal skin flora of humans. The possibility to demonstrate potential specific virulence markers may facilitate the interpretation of the bacteriological findings, as well as the clinical decision. The prevalence of the ica locus and insertion sequence IS256 by using polymerase chain reaction (PCR) among 32 clinical S. epidermidis isolates from prosthetic joint infections (PJIs) and 24 commensal isolates from nares and skin was investigated. Sixteen (50%) of the 32 PJI isolates harbored the ica operon compared with one-third of the commensal isolates obtained from the samples of the skin and nares of healthy individuals. The IS256 was demonstrated in 26 (81%) out of 32 PJI isolates. By contrast, IS256 was found in one of 24 commensal isolates. In conclusion, IS256 may be superior to the ica operon as a marker of the invasive capacity of S. epidermidis, since it was found in most of the PJI isolates, but rarely among commensals.

Keywords

Prosthetic Joint Infection Insertion Sequence IS256 Commensal Isolate Polysaccharide Intercellular Adhesion High Pure Polymerase Chain Reaction Product Purification 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are sincerely obliged to Carolina Berglund for her excellent technical assistance.

References

  1. 1.
    Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G et al (2004) Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294:203–212. doi: 10.1016/j.ijmm.2004.06.015 PubMedCrossRefGoogle Scholar
  2. 2.
    Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microbes Infect 4:481–489. doi: 10.1016/S1286-4579(02)01563-0 PubMedCrossRefGoogle Scholar
  3. 3.
    Arciola CR, Campoccia D, Gamberini S, Rizzi S, Donati ME, Baldassarri L et al (2004) Search for the insertion element IS256 within the ica locus of Staphylococcus epidermidis clinical isolates collected from biomaterial-associated infections. Biomaterials 25:4117–4125. doi: 10.1016/j.biomaterials.2003.11.027 PubMedCrossRefGoogle Scholar
  4. 4.
    Gerke C, Kraft A, Süssmuth R, Schweitzer O, Götz F (1998) Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273:18586–18593. doi: 10.1074/jbc.273.29.18586 PubMedCrossRefGoogle Scholar
  5. 5.
    Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091. doi: 10.1111/j.1365-2958.1996.tb02548.x PubMedCrossRefGoogle Scholar
  6. 6.
    Gu J, Li H, Li M, Vuong C, Otto M, Wen Y et al (2005) Bacterial insertion sequence IS256 as a potential molecular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis. J Hosp Infect 61:342–348. doi: 10.1016/j.jhin.2005.04.017 PubMedCrossRefGoogle Scholar
  7. 7.
    Rohde H, Kalitzky M, Kröger N, Scherpe S, Horstkotte MA, Knobloch JK et al (2004) Detection of virulence-associated genes not useful for discriminating between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J Clin Microbiol 42:5614–5619. doi: 10.1128/JCM.42.12.5614-5619.2004 PubMedCrossRefGoogle Scholar
  8. 8.
    Kozitskaya S, Cho SH, Dietrich K, Marre R, Naber K, Ziebuhr W (2004) The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides. Infect Immun 72:1210–1215. doi: 10.1128/IAI.72.2.1210-1215.2004 PubMedCrossRefGoogle Scholar
  9. 9.
    Ziebuhr W, Krimmer V, Rachid S, Lössner I, Götz F, Hacker J (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32:345–356. doi: 10.1046/j.1365-2958.1999.01353.x PubMedCrossRefGoogle Scholar
  10. 10.
    Hellmark B, Söderquist B, Unemo M (2008) Simultaneous species identification and detection of rifampicin resistance in staphylococci by sequencing of the rpoB gene. Eur J Clin Microbiol Infect Dis. Aug 21. EpubGoogle Scholar
  11. 11.
    Feltham RK, Power AK, Pell PA, Sneath PA (1978) A simple method for storage of bacteria at −76 degrees C. J Appl Bacteriol 44:313–316PubMedGoogle Scholar
  12. 12.
    Frebourg NB, Lefebvre S, Baert S, Lemeland JF (2000) PCR-based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J Clin Microbiol 38:877–880PubMedGoogle Scholar
  13. 13.
    de Silva GD, Kantzanou M, Justice A, Massey RC, Wilkinson AR, Day NP et al (2002) The ica operon and biofilm production in coagulase-negative staphylococci associated with carriage and disease in a neonatal intensive care unit. J Clin Microbiol 40:382–388. doi: 10.1128/JCM.40.02.382-388.2002 PubMedCrossRefGoogle Scholar
  14. 14.
    Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM et al (1985) Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006PubMedGoogle Scholar
  15. 15.
    Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427–5433PubMedGoogle Scholar
  16. 16.
    Freeman DJ, Falkiner FR, Keane CT (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 42:872–874. doi: 10.1136/jcp.42.8.872 PubMedCrossRefGoogle Scholar
  17. 17.
    Galdbart JO, Allignet J, Tung HS, Rydèn C, El Solh N (2000) Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J Infect Dis 182:351–355. doi: 10.1086/315660 PubMedCrossRefGoogle Scholar
  18. 18.
    Frank KL, Hanssen AD, Patel R (2004) icaA is not a useful diagnostic marker for prosthetic joint infection. J Clin Microbiol 42:4846–4849PubMedCrossRefGoogle Scholar
  19. 19.
    Chokr A, Watier D, Eleaume H, Pangon B, Ghnassia JC, Mack D et al (2006) Correlation between biofilm formation and production of polysaccharide intercellular adhesin in clinical isolates of coagulase-negative staphylococci. Int J Med Microbiol 296:381–388. doi: 10.1016/j.ijmm.2006.02.018 PubMedCrossRefGoogle Scholar
  20. 20.
    Petrelli D, Zampaloni C, D’Ercole S, Prenna M, Ballarini P, Ripa S et al (2006) Analysis of different genetic traits and their association with biofilm formation in Staphylococcus epidermidis isolates from central venous catheter infections. Eur J Clin Microbiol Infect Dis 25:773–781. doi: 10.1007/s10096-006-0226-8 PubMedCrossRefGoogle Scholar
  21. 21.
    Vandecasteele SJ, Peetermans WE, Merckx R, Van Eldere J (2003) Expression of biofilm-associated genes in Staphylococcus epidermidis during in vitro and in vivo foreign body infections. J Infect Dis 188:730–737. doi: 10.1086/377452 PubMedCrossRefGoogle Scholar
  22. 22.
    Bradford R, Abdul Manan R, Daley AJ, Pearce C, Ramalingam A, D’Mello D et al (2006) Coagulase-negative staphylococci in very-low-birth-weight infants: inability of genetic markers to distinguish invasive strains from blood culture contaminants. Eur J Clin Microbiol Infect Dis 25:283–290. doi: 10.1007/s10096-006-0130-2 PubMedCrossRefGoogle Scholar
  23. 23.
    Cafiso V, Bertuccio T, Santagati M, Campanile F, Amicosante G, Perilli MG et al (2004) Presence of the ica operon in clinical isolates of Staphylococcus epidermidis and its role in biofilm production. Clin Microbiol Infect 10:1081–1088. doi: 10.1111/j.1469-0691.2004.01024.x PubMedCrossRefGoogle Scholar
  24. 24.
    Klingenberg C, Aarag E, Rønnestad A, Sollid JE, Abrahamsen TG, Kjeldsen G et al (2005) Coagulase-negative staphylococcal sepsis in neonates. Association between antibiotic resistance, biofilm formation and the host inflammatory response. Pediatr Infect Dis J 24:817–822. doi: 10.1097/01.inf.0000176735.20008.cd PubMedCrossRefGoogle Scholar
  25. 25.
    Arciola CR, Campoccia D, Baldassarri L, Donati ME, Pirini V, Gamberini S et al (2006) Detection of biofilm formation in Staphylococcus epidermidis from implant infections. Comparison of a PCR-method that recognizes the presence of ica genes with two classic phenotypic methods. J Biomed Mater Res A 76:425–430. doi: 10.1002/jbm.a.30552 PubMedGoogle Scholar
  26. 26.
    Chaieb K, Mahdouani K, Bakhrouf A (2005) Detection of icaA and icaD loci by polymerase chain reaction and biofilm formation by Staphylococcus epidermidis isolated from dialysate and needles in a dialysis unit. J Hosp Infect 61:225–230. doi: 10.1016/j.jhin.2005.05.014 PubMedCrossRefGoogle Scholar
  27. 27.
    Henning S, Peter-Katalinić J, Pohlentz G (2007) Structure elucidation of glycoproteins by direct nanoESI MS and MS/MS analysis of proteolytic glycopeptides. J Mass Spectrom 42:1415–1421. doi: 10.1002/jms.1265 PubMedCrossRefGoogle Scholar
  28. 28.
    Fitzpatrick F, Humphreys H, O’Gara JP (2005) Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates. J Clin Microbiol 43:1973–1976. doi: 10.1128/JCM.43.4.1973-1976.2005 PubMedCrossRefGoogle Scholar
  29. 29.
    Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster Set al (2007) Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 28:1711–1720. doi: 10.1016/j.biomaterials.2006.11.046 PubMedCrossRefGoogle Scholar
  30. 30.
    Handke LD, Conlon KM, Slater SR, Elbaruni S, Fitzpatrick F, Humphreys H et al (2004) Genetic and phenotypic analysis of biofilm phenotypic variation in multiple Staphylococcus epidermidis isolates. J Med Microbiol 53:367–374. doi: 10.1099/jmm.0.05372-0 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • A. Koskela
    • 1
  • Å. Nilsdotter-Augustinsson
    • 2
  • L. Persson
    • 1
  • B. Söderquist
    • 3
    • 4
    Email author
  1. 1.Clinical Research CenterÖrebro University HospitalÖrebroSweden
  2. 2.Divisions of Infectious Diseases and Medical Microbiology, Department of Molecular and Clinical MedicineLinköping UniversityLinköpingSweden
  3. 3.Department of Clinical MicrobiologyÖrebro University HospitalÖrebroSweden
  4. 4.Department of Infectious DiseasesÖrebro University HospitalÖrebroSweden

Personalised recommendations