Skip to main content

Advertisement

SpringerLink
Log in

Colonisation and interaction between S. epidermidis and S. aureus in the nose and throat of healthy adolescents

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

Abstract

Nasal colonisation with Staphylococcus aureus is a risk factor for developing nosocomial infections. It has been reported that S. epidermidis may produce a serine protease (Esp) inhibiting S. aureus biofilm formation and nasal colonisation. We aimed to analyse the correlation between S. aureus nasal and/or throat carriage and co-colonisation with S. epidermidis strains carrying esp, and the inhibitory effects of S. epidermidis culture supernatants on S. aureus biofilm formation and growth. We obtained 114 S. epidermidis isolates from the nose and 74 S. aureus from the nose and/or throat of healthy adolescents. S. aureus biofilm formation was analysed in a microtitre plate assay and the prevalence of ica, encoding biofilm formation, and esp was analysed with polymerase chain reaction (PCR). Inhibitory effects of S. epidermidis culture supernatants on S. aureus biofilm formation and growth was analysed in vitro. esp prevalence and expression was correlated with inhibitory effects. We detected biofilm formation in 45/74 (61 %) S. aureus strains. The ica operon was more prevalent in isolates colonising the nose (12/15; 80 %) versus isolates colonising the throat only (8/46; 17 %). Almost two-thirds of S. epidermidis culture supernatants displayed high (≥50 %) S. aureus biofilm inhibitory activity, without affecting growth. We found no correlation between the level of inhibitory activity and S. aureus colonisation. esp was ubiquitous in S. epidermidis, but esp expression did not correlate with biofilm inhibitory activity. S. epidermidis culture supernatants inhibit S. aureus biofilm formation, but do not affect bacterial growth. esp expression was not correlated with the inhibitory effects observed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Aires de Sousa M, de Lencastre H (2004) Bridges from hospitals to the laboratory: genetic portraits of methicillin-resistant Staphylococcus aureus clones. FEMS Immunol Med Microbiol 40:101–111

    Article  CAS  PubMed  Google Scholar 

  2. van Belkum A (2011) Novel technology to study co-evolution of humans and Staphylococcus aureus: consequences for interpreting the biology of colonisation and infection. Adv Exp Med Biol 697:273–288

    Article  PubMed  Google Scholar 

  3. Wertheim HF, Vos MC, Boelens HA, Voss A, Vandenbroucke-Grauls CM, Meester MH, Kluytmans JA, van Keulen PH, Verbrugh HA (2004) Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect 56:321–325

    Article  CAS  PubMed  Google Scholar 

  4. Ten Broeke-Smits NJ, Kummer JA, Bleys RL, Fluit AC, Boel CH (2010) Hair follicles as a niche of Staphylococcus aureus in the nose; is a more effective decolonisation strategy needed? J Hosp Infect 76:211–214

    Article  PubMed  Google Scholar 

  5. von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344:11–16

    Article  Google Scholar 

  6. Luzar MA, Coles GA, Faller B, Slingeneyer A, Dah GD, Briat C, Wone C, Knefati Y, Kessler M, Peluso F (1990) Staphylococcus aureus nasal carriage and infection in patients on continuous ambulatory peritoneal dialysis. N Engl J Med 322:505–509

    Article  CAS  PubMed  Google Scholar 

  7. Tong SY, Chen LF, Fowler VG Jr (2012) Colonization, pathogenicity, host susceptibility, and therapeutics for Staphylococcus aureus: what is the clinical relevance? Semin Immunopathol 34:185–200

    Article  PubMed  Google Scholar 

  8. Bode LG, Kluytmans JA, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, Roosendaal R, Troelstra A, Box AT, Voss A, van der Tweel I, van Belkum A, Verbrugh HA, Vos MC (2010) Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 362:9–17

    Article  CAS  PubMed  Google Scholar 

  9. Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR (2010) The human nasal microbiota and Staphylococcus aureus carriage. PLoS One 5:e10598

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lina G, Boutite F, Tristan A, Bes M, Etienne J, Vandenesch F (2003) Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 69:18–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wos-Oxley ML, Plumeier I, von Eiff C, Taudien S, Platzer M, Vilchez-Vargas R, Becker K, Pieper DH (2010) A poke into the diversity and associations within human anterior nare microbial communities. ISME J 4:839–851

    Article  PubMed  Google Scholar 

  12. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–349

    Article  CAS  PubMed  Google Scholar 

  13. Sugimoto S, Iwamoto T, Takada K, Okuda K, Tajima A, Iwase T, Mizunoe Y (2013) Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host–pathogen interaction. J Bacteriol 195:1645–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Krismer B, Peschel A (2011) Does Staphylococcus aureus nasal colonization involve biofilm formation? Future Microbiol 6:489–493

    Article  PubMed  Google Scholar 

  15. Otto M (2009) Staphylococcus epidermidis—the ‘accidental’ pathogen. Nat Rev Microbiol 7:555–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cantero D, Cooksley C, Bassiouni A, Wormald PJ, Vreugde S (2013) Staphylococcus aureus biofilm activates the nucleotide-binding oligomerization domain containing 2 (Nod2) pathway and proinflammatory factors on a human sinonasal explant model. Int Forum Allergy Rhinol 3:877–884

    Article  PubMed  Google Scholar 

  17. Gelardi M, Passalacqua G, Fiorella ML, Quaranta N (2013) Assessment of biofilm by nasal cytology in different forms of rhinitis and its functional correlations. Eur Ann Allergy Clin Immunol 45:25–29

    CAS  PubMed  Google Scholar 

  18. Cantero D, Cooksley C, Jardeleza C, Bassiouni A, Jones D, Wormald PJ, Vreugde S (2013) A human nasal explant model to study Staphylococcus aureus biofilm in vitro. Int Forum Allergy Rhinol 3:556–562

    Article  PubMed  Google Scholar 

  19. Fitzpatrick F, Humphreys H, O’Gara JP (2006) Environmental regulation of biofilm development in methicillin-resistant and methicillin-susceptible Staphylococcus aureus clinical isolates. J Hosp Infect 62:120–122

    Article  CAS  PubMed  Google Scholar 

  20. Hanssen AM, Kjeldsen G, Sollid JU (2004) Local variants of Staphylococcal cassette chromosome mec in sporadic methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococci: evidence of horizontal gene transfer? Antimicrob Agents Chemother 48:285–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH (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 22:996–1006

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Fredheim EG, Klingenberg C, Rohde H, Frankenberger S, Gaustad P, Flaegstad T, Sollid JE (2009) Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47:1172–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Knobloch JK, Horstkotte MA, Rohde H, Mack D (2002) Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol 191:101–106

    Article  CAS  PubMed  Google Scholar 

  24. Ikeda Y, Ohara-Nemoto Y, Kimura S, Ishibashi K, Kikuchi K (2004) PCR-based identification of Staphylococcus epidermidis targeting gseA encoding the glutamic-acid-specific protease. Can J Microbiol 50:493–498

    Article  CAS  PubMed  Google Scholar 

  25. Klingenberg C, Aarag E, Rønnestad A, Sollid JE, Abrahamsen TG, Kjeldsen G, Flaegstad T (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

    Article  PubMed  Google Scholar 

  26. Flemming K, Klingenberg C, Cavanagh JP, Sletteng M, Stensen W, Svendsen JS, Flaegstad T (2009) High in vitro antimicrobial activity of synthetic antimicrobial peptidomimetics against staphylococcal biofilms. J Antimicrob Chemother 63:136–145

    Article  CAS  PubMed  Google Scholar 

  27. Papa R, Parrilli E, Sannino F, Barbato G, Tutino ML, Artini M, Selan L (2013) Anti-biofilm activity of the Antarctic marine bacterium Pseudoalteromonas haloplanktis TAC125. Res Microbiol 164:450–456

    Article  CAS  PubMed  Google Scholar 

  28. Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL, Enright MC (2007) Improved multilocus sequence typing scheme for Staphylococcus epidermidis. J Clin Microbiol 45:616–619

    Article  PubMed  Google Scholar 

  29. Sangvik M, Olsen RS, Olsen K, Simonsen GS, Furberg AS, Sollid JU (2011) Age- and gender-associated Staphylococcus aureus spa types found among nasal carriers in a general population: the Tromso Staph and Skin Study. J Clin Microbiol 49:4213–4218

    Article  PubMed  PubMed Central  Google Scholar 

  30. Faria NA, Conceição T, Miragaia M, Bartels MD, de Lencastre H, Westh H (2014) Nasal carriage of methicillin resistant staphylococci. Microb Drug Resist 20:108–117

    Article  CAS  PubMed  Google Scholar 

  31. Rolo J, de Lencastre H, Miragaia M (2012) Strategies of adaptation of Staphylococcus epidermidis to hospital and community: amplification and diversification of SCCmec. J Antimicrob Chemother 67:1333–1341

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Jon Anders Fjose, Merethe Sletteng and Caio Fernando de Oliveira for their technical assistance, particularly in the collection of the strains and MLST. We thank Dr. Anne Sofie Furberg for extracting the data from the Fit Futures database and Prof. Johanna E. Sollid for the critical feedback on the project and manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Paediatrics, University Hospital of North Norway, Tromsø, Norway

    E. G. A. Fredheim, T. Flægstad & C. Klingenberg

  2. Paediatric Research Group, Department of Clinical Medicine, University of Tromsø, Tromsø, Norway

    E. G. A. Fredheim, T. Flægstad & C. Klingenberg

  3. Research Group for Host–Microbe Interactions, Department of Medical Biology, University of Tromsø, Tromsø, Norway

    F. Askarian

Authors
  1. E. G. A. Fredheim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Flægstad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Askarian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Klingenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. G. A. Fredheim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fredheim, E.G.A., Flægstad, T., Askarian, F. et al. Colonisation and interaction between S. epidermidis and S. aureus in the nose and throat of healthy adolescents. Eur J Clin Microbiol Infect Dis 34, 123–129 (2015). https://doi.org/10.1007/s10096-014-2197-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2197-5

Keywords

Search

Navigation