Advertisement

Food-borne enterococci and their resistance to oxidative stress

  • Barbora VlkováEmail author
  • Tomáš Szemes
  • Gabriel Minárik
  • Ľubomíra Tóthová
  • Hana Drahovská
  • Ján Turňa
  • Peter Celec
Articles

Abstract

Enterococci are important food-borne pathogens that cause serious infections. Several virulence factors have been described including aggregation substance, gelatinase, cytolysin, and enterococcal surface protein. The ability to cause infections is mainly dependent on the response to oxidative stress due to the production of reactive oxygen species by immune cells. The aim of our study was to analyze the resistance of enterococcal strains from food to clinically relevant antiseptic agents with regard to the presence of selected virulence factors, and to uncover potential mechanisms of the antioxidative resistance. Eighty-two enterococcal isolates from Bryndza cheese were tested using in vitro growth assays to study the ability of these isolates to survive exposure to antiseptic agents — hydrogen peroxide, hypochlorite, and Chlorhexidine. Virulence genotypes of the isolates were determined by PCR, and RT real time PCR was used for gene expression under oxidative stress. Resistance against antiseptic agents depends on the concentration of applied chemicals, on the time of exposure, but also on virulence factors of the enterococcal strains. Oxidative stress induces the expression of antioxidative enzymes and down-regulates the expression of prooxidative enzymes. These effects are dependent on the virulence genotype of the enterococcal strains. These findings are important for future research, especially concerning the role of enterococci in oral diseases.

Keywords

Enterococcus faecalis reactive oxygen species oxidative stress free radicals infection virulence 

References

  1. Bizzini, A., C. Zhao, Y. Auffray, and A. Hartke. 2009. The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J. Antimicrob. Chemother. 64, 1196–1202.PubMedCrossRefGoogle Scholar
  2. Dametto, F.R., C.C.R. Ferraz, B. Paula, F.D. Gomes, A.A. Zaia, F.B. Teixeira, and F.J. de Souza. 2005. In vitro assessment of the immediate and prolonged antimicrobial action of chlorhexidine gel as an endodontic irrigant against Enterococcus faecalis. Oral Surg. Oral Med. Oral Pathol. 99, 768–772.Google Scholar
  3. Davis, J.M., J. Maki, and J.K. Bahcall. 2007. An in vitro comparison of the antimicrobial effects of various endodontic medicaments on Enterococcus faecalis. J. Endod. 33, 567–569.PubMedCrossRefGoogle Scholar
  4. Del Papa, M.F., L.E. Hancock, V.C. Thomas, and M. Perego. 2007. Full activation of Enterococcus faecalis gelatinase by a c-terminal proteolytic cleavage. J. Bacteriol. 189, 8835–8843.PubMedCrossRefGoogle Scholar
  5. Dunavant, T.R., J.D. Regan, G.N. Glickman, E.S. Solomon, and A.L. Honeyman. 2006. Comparative evaluation of endodontic irrigant against Enterococcus faecalis biofilms. J. Endod. 32, 527–531.PubMedCrossRefGoogle Scholar
  6. Dutkamalen, S., S. Evers, and P. Courvalin. 1995. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 33, 24–27.Google Scholar
  7. Galli, D. and R. Wirth. 1991. Comparative analysis of Enterococcus faecalis sex pheromone plasmids identifies a single homologous DNA region which codes for aggregation substance. J. Bacteriol. 173, 3029–3033.PubMedGoogle Scholar
  8. Giraffa, G., D. Carminati, and E. Neviani. 1997. Enterococci isolated from dairy products: A review of risks and potential technological use. J. Food Prot. 60, 732–737.Google Scholar
  9. Haas, W. and M.S. Gilmore. 1999. Molecular nature of a novel bacterial toxin: The cytolysin of enterococcus faecalis. Med. Microbiol. Immunol. (Berl.). 187, 183–190.CrossRefGoogle Scholar
  10. Hidron, A.I., J.R. Edwards, J. Patel, T.C. Horan, D.M. Sievert, D.A. Pollock, and S.K. Fridkin. 2008. Antimicrobial-resistant pathogens associated with healthcare-associated infections: Annual summary of data reported to the national healthcare safety network at the centers for disease control and prevention, 2006–2007. Infect. Control Hosp. Epidemiol. 29, 996–1011.PubMedCrossRefGoogle Scholar
  11. Huycke, M.M., D.F. Sahm, and M.S. Gilmore. 1998. Multiple-drug resistant enterococci: The nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4, 239–249.PubMedCrossRefGoogle Scholar
  12. Jang, H.C., S. Lee, K.H. Song, J.H. Jeon, W.B. Park, S.W. Park, H.B. Kim, and et al. 2010. Clinical features, risk factors and outcomes of bacteremia due to enterococci with high-level gentamicin resistance: Comparison with bacteremia due to enterococci without high-level gentamicin resistance. J. Korean Med. Sci. 25, 3–8.PubMedCrossRefGoogle Scholar
  13. Kayaoglu, G. and D. Orstavik. 2004. Virulence factors of Enterococcus faecalis: Relationship to endodontic disease. Crit. Rev. Oral Biol. Med. 15, 308–320.PubMedCrossRefGoogle Scholar
  14. La Carbona, S., N. Sauvageot, J.C. Giard, A. Benachour, B. Posteraro, Y. Auffray, M. Sanguinetti, and A. Hartke. 2007. Comparative study of the physiological roles of three peroxidases (nadh peroxidase, alkyl hydroperoxide reductase and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of enterococcus faecalis. Mol. Microbiol. 66, 1148–1163.PubMedCrossRefGoogle Scholar
  15. Love, R.M. 2001. Enterococcus faecalis — a mechanism for its role in endodontic failure. Int. Endod. J. 34, 399–405.PubMedCrossRefGoogle Scholar
  16. Low, D.E., N. Keller, A. Barth, and R.N. Jones. 2001. Clinical prevalence, antimicrobial susceptibility, and geographic resistance patterns of enterococci: Results from the sentry antimicrobial surveillance program, 1997–1999. Clin. Infect. Dis. 32, S133–S145.PubMedCrossRefGoogle Scholar
  17. Nakajo, K., R. Komori, S. Ishikawa, T. Ueno, Y. Suzuki, Y. Iwami, and N. Takahashi. 2006. Resistance to acidic and alkaline environments in the endodontic pathogen Enterococcus faecalis. Oral Microbiol. Immunol. 21, 283–288.PubMedCrossRefGoogle Scholar
  18. Oliveira, D.P., J.V.B. Barbizam, M. Trope, and F.B. Teixeira. 2007. In vitro antibacterial efficacy of endodontic irrigants against Enterococcus faecalis. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 103, 702–706.PubMedCrossRefGoogle Scholar
  19. Rams, T.E., D. Feik, V. Young, B.F. Hammond, and J. Slots. 1992. Enterococci in human periodontitis. Oral Microbiol. Immunol. 7, 249–252.PubMedCrossRefGoogle Scholar
  20. Riboulet, E., N. Verneuil, S. La Carbona, N. Sauvageot, Y. Auffray, A. Hartke, and J.C. Giard. 2007. Relationships between oxidative stress response and virulence in Enterococcus faecalis. J. Mol. Microbiol. Biotechnol. 13, 140–146.PubMedCrossRefGoogle Scholar
  21. Rozdzinski, E., R. Marre, M. Susa, R. Wirth, and A. Muscholl-Silberhorn. 2001. Aggregation substance-mediated adherence of Enterococcus faecalis to immobilized extracellular matrix proteins. Microb. Pathog. 30, 211–220.PubMedCrossRefGoogle Scholar
  22. Shaked, H., Y. Carmeli, D. Schwartz, and Y. Siegman-Igra. 2006. Enterococcal bacteraemia: Epidemiological, microbiological, clinical and prognostic characteristics, and the impact of high level gentamicin resistance. Scand. J. Infect. Dis. 38, 995–1000.PubMedCrossRefGoogle Scholar
  23. Sherman, J.M. 1937. The streptococci. Bacteriol. Rev. 1, 3–97.PubMedGoogle Scholar
  24. Su, Y.A., M.C. Sulavik, P. He, K.K. Makinen, P.L. Makinen, S. Fiedler, R. Wirth, and D.B. Clewell. 1991. Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. Liquefaciens. Infect. Immun. 59, 415–420.PubMedGoogle Scholar
  25. Toledo-Arana, A., J. Valle, C. Solano, M.J. Arrizubieta, C. Cucarella, M. Lamata, B. Amorena, J. Leiva, J.R. Penades, and I. Lasa. 2001. The enterococcal surface protein, esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67, 4538–4545.PubMedCrossRefGoogle Scholar
  26. Vankerckhoven, V., T. Van Autgaerden, C. Vael, C. Lammens, S. Chapelle, R. Rossi, D. Jabes, and H. Goossens. 2004. Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in Enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J. Clin. Microbiol. 42, 4473–4479.PubMedCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg  2011

Authors and Affiliations

  • Barbora Vlková
    • 1
    • 2
    • 3
    Email author
  • Tomáš Szemes
    • 1
    • 2
  • Gabriel Minárik
    • 1
    • 2
    • 3
  • Ľubomíra Tóthová
    • 2
  • Hana Drahovská
    • 2
  • Ján Turňa
    • 2
  • Peter Celec
    • 1
    • 2
    • 3
    • 4
  1. 1.Geneton IncBratislavaSlovakia
  2. 2.Department of Molecular BiologyComenius UniversityBratislavaSlovakia
  3. 3.Institute of Molecular BiomedicineComenius UniversityBratislavaSlovakia
  4. 4.Institute of PathophysiologyComenius UniversityBratislavaSlovakia

Personalised recommendations