SpringerLink
Log in

Virulence factors among Staphylococcus lugdunensis are associated with infection sites and clonal spread

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Staphylococcus lugdunensis has emerged as a significant human pathogen, with distinct clinical and microbiological characteristics. Our goal was to identify the virulence factors in S. lugdunensis recovered from infected patients of two Greek hospitals during a six-year period (2008–2013). A collection of 38 S. lugdunensis was tested for biofilm formation, antimicrobial susceptibility, clonal distribution, virulence factors (ica operon, fbl, atlL, vwbl, slush) and antibiotic resistance genes (mecA, ermC) carriage. Strains were classified into pulsotypes by pulsed-field gel electrophoresis (PFGE) of SmaI DNA digests. The majority (22) was isolated from skin and soft tissue infections (SSTIs), nine from deep-sited infections (DSIs), including three bacteraemias and seven from prosthetic device-associated infections (PDAIs). All isolates were oxacillin-susceptible, mecA-negative and fbl-positive. The highest resistance rate was detected for ampicillin (50 %), followed by erythromycin and clindamycin (18.4 %). Fourteen isolates (36.8 %) produced biofilm, whereas 26/38 (68.4 %) carried the ica operon. Biofilm formation was more frequent in isolates from PDAIs. Thirty-six strains (94.7 %) carried atlL and 31 (81.6 %) carried vwbl, whereas slush was detected in 15 (39.5 %). PFGE revealed a low level of genetic diversity: strains were classified into seven pulsotypes, with two major clones (C: 22 and D: nine strains). Type C strains recovered from all infection sites prevailed in biofilm formation and ermC carriage, whereas type D strains associated with SSTIs and DSIs carried more frequently vwbl, slush or both genes. Despite susceptibility to antimicrobials, the clonal expansion and carriage of virulence factors, combined with biofilm-producing ability, render this species an important pathogen that should not be ignored.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Frank KL, Del Pozo JL, Patel R (2008) From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 21(1):111–133. doi:10.1128/CMR.00036-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Frank KL, Reichert EJ, Piper KE, Patel R (2007) In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrob Agents Chemother 51(3):888–895. doi:10.1128/AAC.01052-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. van der Mee-Marquet N, Achard A, Mereghetti L, Danton A, Minier M, Quentin R (2003) Staphylococcus lugdunensis infections: high frequency of inguinal area carriage. J Clin Microbiol 41(4):1404–1409

    Article  PubMed Central  PubMed  Google Scholar 

  4. Liu C, Shen D, Guo J, Wang K, Wang H, Yan Z, Chen R, Ye L (2012) Clinical and microbiological characterization of Staphylococcus lugdunensis isolates obtained from clinical specimens in a hospital in China. BMC Microbiol 12:168. doi:10.1186/1471-2180-12-168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Spiliopoulou I, Petinaki E, Papandreou P, Dimitracopoulos G (2004) erm(C) is the predominant genetic determinant for the expression of resistance to macrolides among methicillin-resistant Staphylococcus aureus clinical isolates in Greece. J Antimicrob Chemother 53(5):814–817. doi:10.1093/jac/dkh197

    Article  CAS  PubMed  Google Scholar 

  6. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178(1):175–183

    PubMed Central  CAS  PubMed  Google Scholar 

  8. Spiliopoulou AI, Krevvata MI, Kolonitsiou F, Harris LG, Wilkinson TS, Davies AP, Dimitracopoulos GO, Karamanos NK, Mack D, Anastassiou ED (2012) An extracellular Staphylococcus epidermidis polysaccharide: relation to Polysaccharide Intercellular Adhesin and its implication in phagocytosis. BMC Microbiol 12:76. doi:10.1186/1471-2180-12-76

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Nilsson M, Bjerketorp J, Wiebensjö A, Ljungh A, Frykberg L, Guss B (2004) A von Willebrand factor-binding protein from Staphylococcus lugdunensis. FEMS Microbiol Lett 234(1):155–161. doi:10.1016/j.femsle.2004.03.024

    Article  CAS  PubMed  Google Scholar 

  10. Vischer UM, de Moerloose P (1999) von Willebrand factor: from cell biology to the clinical management of von Willebrand’s disease. Crit Rev Oncol Hematol 30(2):93–109

    Article  CAS  PubMed  Google Scholar 

  11. Mitchell J, Tristan A, Foster TJ (2004) Characterization of the fibrinogen-binding surface protein Fbl of Staphylococcus lugdunensis. Microbiology 150(Pt 11):3831–3841. doi:10.1099/mic.0.27337-0

    Article  CAS  PubMed  Google Scholar 

  12. Chatzigeorgiou KS, Siafakas N, Petinaki E, Zerva L (2010) fbl gene as a species-specific target for Staphylococcus lugdunensis identification. J Clin Lab Anal 24(2):119–122. doi:10.1002/jcla.20352

    Article  CAS  PubMed  Google Scholar 

  13. Donvito B, Etienne J, Greenland T, Mouren C, Delorme V, Vandenesch F (1997) Distribution of the synergistic haemolysin genes hld and slush with respect to agr in human staphylococci. FEMS Microbiol Lett 151(2):139–144

    Article  CAS  PubMed  Google Scholar 

  14. Gibert L, Didi J, Marlinghaus L, Lesouhaitier O, Legris S, Szabados F, Pons JL, Pestel-Caron M (2014) The major autolysin of Staphylococcus lugdunensis, AtlL, is involved in cell separation, stress-induced autolysis and contributes to bacterial pathogenesis. FEMS Microbiol Lett 352(1):78–86. doi:10.1111/1574-6968.12374

    Article  CAS  PubMed  Google Scholar 

  15. The European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0, 2014. http://www.eucast.org

  16. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115(8):891–899. doi:10.1111/j.1600-0463.2007.apm_630.x

    Article  PubMed  Google Scholar 

  17. Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S (1991) Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 29(10):2240–2244

    PubMed Central  CAS  PubMed  Google Scholar 

  18. Sandoe JA, Longshaw CM (2001) Ventriculoperitoneal shunt infection caused by Staphylococcus lugdunensis. Clin Microbiol Infect 7(7):385–387

    Article  CAS  PubMed  Google Scholar 

  19. Szabados F, Nowotny Y, Marlinghaus L, Korte M, Neumann S, Kaase M, Gatermann SG (2011) Occurrence of genes of putative fibrinogen binding proteins and hemolysins, as well as of their phenotypic correlates in isolates of S. lugdunensis of different origins. BMC Res Notes 4:113. doi:10.1186/1756-0500-4-113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain ty**. J Clin Microbiol 33(9):2233–2239

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Miragaia M, Carriço JA, Thomas JC, Couto I, Enright MC, de Lencastre H (2008) Comparison of molecular ty** methods for characterization of Staphylococcus epidermidis: proposal for clone definition. J Clin Microbiol 46(1):118–129. doi:10.1128/JCM.01685-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Santos Sanches I, Mato R, de Lencastre H, Tomasz A; CEM/NET Collaborators and the International Collaborators (2000) Patterns of multidrug resistance among methicillin-resistant hospital isolates of coagulase-positive and coagulase-negative staphylococci collected in the international multicenter study RESIST in 1997 and 1998. Microb Drug Resist 6(3):199–211

    Article  CAS  PubMed  Google Scholar 

  23. Zinkernagel AS, Zinkernagel MS, Elzi MV, Genoni M, Gubler J, Zbinden R, Mueller NJ (2008) Significance of Staphylococcus lugdunensis bacteremia: report of 28 cases and review of the literature. Infection 36(4):314–321. doi:10.1007/s15010-008-7287-9

    Article  CAS  PubMed  Google Scholar 

  24. Lambe DW Jr, Jeffery C, Ferguson KP, Cooper MD (1994) Examination of the glycocalyx of four species of Staphylococcus by transmission electron microscopy and image analysis. Microbios 78(316):133–143

    PubMed  Google Scholar 

  25. Frank KL, Patel R (2007) Poly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBC-positive Staphylococcus lugdunensis isolates. Infect Immun 75(10):4728–4742. doi:10.1128/IAI.00640-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Pereira EM, Teixeira CA, Alvarenga AL, Schuenck RP, Giambiagi-Demarval M, Holandino C, Mattos-Guaraldi AL, dos Santos KR (2012) A Brazilian lineage of Staphylococcus lugdunensis presenting rough colony morphology may adhere to and invade lung epithelial cells. J Med Microbiol 61(Pt 4):463–469. doi:10.1099/jmm.0.033001-0

    Article  CAS  PubMed  Google Scholar 

  27. Hellbacher C, Törnqvist E, Söderquist B (2006) Staphylococcus lugdunensis: clinical spectrum, antibiotic susceptibility, and phenotypic and genotypic patterns of 39 isolates. Clin Microbiol Infect 12(1):43–49. doi:10.1111/j.1469-0691.2005.01296.x

    Article  CAS  PubMed  Google Scholar 

  28. Bourgeois I, Camiade E, Biswas R, Courtin P, Gibert L, Götz F, Chapot-Chartier MP, Pons JL, Pestel-Caron M (2009) Characterization of AtlL, a bifunctional autolysin of Staphylococcus lugdunensis with N-acetylglucosaminidase and N-acetylmuramoyl-l-alanine amidase activities. FEMS Microbiol Lett 290(1):105–113. doi:10.1111/j.1574-6968.2008.01414.x

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Anastasia Spiliopoulou MD, PhD for her assistance in collecting the isolates. The Ethics Committee of the University Hospital of Patras approved this study and waived the need for informed consent (approval no.: 316). Part of this work was presented as a poster presentation at the 24th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID 2014), May 2014, Barcelona, Spain.

Funding

This research was supported by funding from the National Staphylococcal Reference Laboratory, Greece, under the scientific responsibility of I.S. and E.D.A. (grant C954, Hellenic Centre for Disease Control and Prevention, HCDCP/KEELPNO).

Conflict of interest

Nothing to declare.

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Medicine, University of Patras, 26504, Rion, Patras, Greece

    N. Giormezis, F. Kolonitsiou, M. Christofidou, E. D. Anastassiou & I. Spiliopoulou

  2. National Reference Laboratory for Staphylococci, Patras, Greece

    N. Giormezis, F. Kolonitsiou, E. D. Anastassiou & I. Spiliopoulou

  3. Laboratory of Microbiology, General Children Hospital Pentelis, Athens, Greece

    A. Makri & A. Vogiatzi

Authors
  1. N. Giormezis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Kolonitsiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Makri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Vogiatzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Christofidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. D. Anastassiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. Spiliopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Spiliopoulou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giormezis, N., Kolonitsiou, F., Makri, A. et al. Virulence factors among Staphylococcus lugdunensis are associated with infection sites and clonal spread. Eur J Clin Microbiol Infect Dis 34, 773–778 (2015). https://doi.org/10.1007/s10096-014-2291-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2291-8

Keywords

Search

Navigation