Skip to main content

Advertisement

Log in

Enterococcus faecalis from patients with chronic periodontitis: virulence and antimicrobial resistance traits and determinants

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

Abstract

This study investigated the presence of virulence and resistance traits, as well as their genetic determinants in subgingival Enterococcus faecalis from patients with chronic periodontitis. Twenty-four E. faecalis strains from a previously multi-locus sequence typing (MLST)-characterized strain collection were examined for virulence-associated phenotypes, antimicrobial susceptibility, and virulence- and antimicrobial-resistant determinants. Gelatinase, hemolysin, and biofilm production were detected in 50, 17, and 100% of the strains, respectively. Genes encoding adherence factors such as ace, efaA, and bopD were detected in all isolates. Other putative virulence determinants, i.e., EF3314, gelE, asa, esp, cylA, ef1841/fsrC, and asa373, were found in a portion of the strains. Different levels of resistance were observed in these strains, with two strains expressing high-level resistance to erythromycin and gentamicin. The integrase gene and accessory gene(s) of the Tn916/Tn1545 family were detected in ten strains. A direct link was shown between the presence of Tn916/Tn1545-like elements and resistance to doxycycline and/or erythromycin. The results demonstrated that virulence and antibiotic resistance determinants were prevalent in oral E. faecalis strains. It implicates that oral E. faecalis might play a role in the pathogenesis of chronic periodontitis and be a potential reservoir for the transferable elements of virulence and antimicrobial resistance.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Fisher K, Phillips C (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155(Pt 6):1749–1757

    Article  PubMed  CAS  Google Scholar 

  2. Tendolkar PM, Baghdayan AS, Shankar N (2003) Pathogenic enterococci: new developments in the 21st century. Cell Mol Life Sci 60(12):2622–2636

    Article  PubMed  CAS  Google Scholar 

  3. Palmer KL, Kos VN, Gilmore MS (2010) Horizontal gene transfer and the genomics of enterococcal antibiotic resistance. Curr Opin Microbiol 13(5):632–639

    Article  PubMed  CAS  Google Scholar 

  4. Sundqvist G, Figdor D (2003) Life as an endodontic pathogen. Endod Top 6(1):3–28

    Article  Google Scholar 

  5. Kayaoglu G, Ørstavik D (2004) Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Crit Rev Oral Biol Med 15(5):308–320

    Article  PubMed  Google Scholar 

  6. Pinheiro ET, Gomes BP, Drucker DB, Zaia AA, Ferraz CC, Souza-Filho FJ (2004) Antimicrobial susceptibility of Enterococcus faecalis isolated from canals of root filled teeth with periapical lesions. Int Endod J 37(11):756–763

    Article  PubMed  CAS  Google Scholar 

  7. Dahlén G, Samuelsson W, Molander A, Reit C (2000) Identification and antimicrobial susceptibility of enterococci isolated from the root canal. Oral Microbiol Immunol 15(5):309–312

    Article  PubMed  Google Scholar 

  8. Sun J, Song X, Kristiansen BE, Kjaereng A, Willems RJ, Eriksen HM, Sundsfjord A, Sollid JE (2009) Occurrence, population structure, and antimicrobial resistance of enterococci in marginal and apical periodontitis. J Clin Microbiol 47(7):2218–2225

    Article  PubMed  CAS  Google Scholar 

  9. Rams TE, Feik D, Young V, Hammond BF, Slots J (1992) Enterococci in human periodontitis. Oral Microbiol Immunol 7(4):249–252

    Article  PubMed  CAS  Google Scholar 

  10. Sedgley CM, Molander A, Flannagan SE, Nagel AC, Appelbe OK, Clewell DB, Dahlén G (2005) Virulence, phenotype and genotype characteristics of endodontic Enterococcus spp. Oral Microbiol Immunol 20(1):10–19

    Article  PubMed  CAS  Google Scholar 

  11. Toledo-Arana A, Valle J, Solano C, Arrizubieta MJ, Cucarella C, Lamata M, Amorena B, Leiva J, Penadés JR, Lasa I (2001) The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol 67(10):4538–4545

    Article  PubMed  CAS  Google Scholar 

  12. Creti R, Imperi M, Bertuccini L, Fabretti F, Orefici G, Di Rosa R, Baldassarri L (2004) Survey for virulence determinants among Enterococcus faecalis isolated from different sources. J Med Microbiol 53(Pt 1):13–20

    Article  PubMed  CAS  Google Scholar 

  13. Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15(4):209–215

    Article  PubMed  CAS  Google Scholar 

  14. Gevers D, Masco L, Baert L, Huys G, Debevere J, Swings J (2003) Prevalence and diversity of tetracycline resistant lactic acid bacteria and their tet genes along the process line of fermented dry sausages. Syst Appl Microbiol 26(2):277–283

    Article  PubMed  CAS  Google Scholar 

  15. Ramamurthy NS, Xu JW, Bird J, Baxter A, Bhogal R, Wills R, Watson B, Owen D, Wolff M, Greenwald RA (2002) Inhibition of alveolar bone loss by matrix metalloproteinase inhibitors in experimental periodontal disease. J Periodontal Res 37(1):1–7

    Article  PubMed  CAS  Google Scholar 

  16. Nakayama J, Tanaka E, Kariyama R, Nagata K, Nishiguchi K, Mitsuhata R, Uemura Y, Tanokura M, Kumon H, Sonomoto K (2007) Siamycin attenuates fsr quorum sensing mediated by a gelatinase biosynthesis-activating pheromone in Enterococcus faecalis. J Bacteriol 189(4):1358–1365

    Article  PubMed  CAS  Google Scholar 

  17. Nakayama J, Kariyama R, Kumon H (2002) Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl Environ Microbiol 68(6):3152–3155

    Article  PubMed  CAS  Google Scholar 

  18. Seno Y, Kariyama R, Mitsuhata R, Monden K, Kumon H (2005) Clinical implications of biofilm formation by Enterococcus faecalis in the urinary tract. Acta Med Okayama 59(3):79–87

    PubMed  Google Scholar 

  19. Sandoe JA, Witherden IR, Cove JH, Heritage J, Wilcox MH (2003) Correlation between enterococcal biofilm formation in vitro and medical-device-related infection potential in vivo. J Med Microbiol 52(Pt 7):547–550

    Article  PubMed  Google Scholar 

  20. Dworniczek E, Wojciech Ł, Sobieszczańska B, Seniuk A (2005) Virulence of Enterococcus isolates collected in Lower Silesia (Poland). Scand J Infect Dis 37(9):630–636

    Article  PubMed  CAS  Google Scholar 

  21. Mohamed JA, Huang DB (2007) Biofilm formation by enterococci. J Med Microbiol 56(Pt 12):1581–1588

    Article  PubMed  CAS  Google Scholar 

  22. Hufnagel M, Koch S, Creti R, Baldassarri L, Huebner J (2004) A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J Infect Dis 189(3):420–430

    Article  PubMed  CAS  Google Scholar 

  23. Handal T, Caugant DA, Olsen I (2003) Antibiotic resistance in bacteria isolated from subgingival plaque in a Norwegian population with refractory marginal periodontitis. Antimicrob Agents Chemother 47(4):1443–1446

    Article  PubMed  CAS  Google Scholar 

  24. Jorgensen MG, Slots J (2002) The ins and outs of periodontal antimicrobial therapy. J Calif Dent Assoc 30(4):297–305

    PubMed  Google Scholar 

  25. NORM/NORM-VET (2007) Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. ISSN: 1502-2307

  26. Samaranayake LP (2006) Antimicrobial chemotherapy. Essential microbiology for dentistry. Churchill Livingstone Elsevier, Philadelphia, PA, pp 67–76

    Google Scholar 

  27. Speer BS, Shoemaker NB, Salyers AA (1992) Bacterial resistance to tetracycline: mechanisms, transfer, and clinical significance. Clin Microbiol Rev 5(4):387–399

    PubMed  CAS  Google Scholar 

  28. Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999) Nomenclature for macrolide and macrolide–lincosamide–streptogramin B resistance determinants. Antimicrob Agents Chemother 43(12):2823–2830

    PubMed  CAS  Google Scholar 

  29. Simjee S, Manzoor SE, Fraise AP, Gill MJ (2000) Nature of transposon-mediated high-level gentamicin resistance in Enterococcus faecalis isolated in the United Kingdom. J Antimicrob Chemother 45(5):565–575

    Article  PubMed  CAS  Google Scholar 

  30. Rice LB (1998) Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 42(8):1871–1877

    PubMed  CAS  Google Scholar 

  31. Roberts AP, Mullany P (2009) A modular master on the move: the Tn916 family of mobile genetic elements. Trends Microbiol 17(6):251–258

    Article  PubMed  CAS  Google Scholar 

  32. Larsen J, Schønheyder HC, Lester CH, Olsen SS, Porsbo LJ, Garcia-Migura L, Jensen LB, Bisgaard M, Hammerum AM (2010) Porcine-origin gentamicin-resistant Enterococcus faecalis in humans, Denmark. Emerg Infect Dis 16(4):682–684

    PubMed  Google Scholar 

  33. Freitas AR, Novais C, Ruiz-Garbajosa P, Coque TM, Peixe L (2009) Clonal expansion within clonal complex 2 and spread of vancomycin-resistant plasmids among different genetic lineages of Enterococcus faecalis from Portugal. J Antimicrob Chemother 63(6):1104–1111

    Article  PubMed  CAS  Google Scholar 

  34. Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, Coque TM, Cantón R, Baquero F, Murray BE, del Campo R, Willems RJ (2006) Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol 44(6):2220–2228

    Article  PubMed  CAS  Google Scholar 

  35. Nallapareddy SR, Duh RW, Singh KV, Murray BE (2002) Molecular typing of selected Enterococcus faecalis isolates: pilot study using multilocus sequence typing and pulsed-field gel electrophoresis. J Clin Microbiol 40(3):868–876

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the University of Tromsø, Norway. We thank Harald M. Eriksen, Johanna E. Sollid, and Bjørn Erik Kristiansen for their kind support in organizing the original collection of strains. We also thank Trine Tesserm for the technical assistance with the Etest.

Declaration of interest

Nothing to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to X. Song.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sun, J., Sundsfjord, A. & Song, X. Enterococcus faecalis from patients with chronic periodontitis: virulence and antimicrobial resistance traits and determinants. Eur J Clin Microbiol Infect Dis 31, 267–272 (2012). https://doi.org/10.1007/s10096-011-1305-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1305-z

Keywords

Navigation