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.
This is a preview of subscription content, access via your institution.
References
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Kayaoglu, G. and D. Orstavik. 2004. Virulence factors of Enterococcus faecalis: Relationship to endodontic disease. Crit. Rev. Oral Biol. Med. 15, 308–320.
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.
Love, R.M. 2001. Enterococcus faecalis — a mechanism for its role in endodontic failure. Int. Endod. J. 34, 399–405.
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.
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.
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.
Rams, T.E., D. Feik, V. Young, B.F. Hammond, and J. Slots. 1992. Enterococci in human periodontitis. Oral Microbiol. Immunol. 7, 249–252.
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.
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.
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.
Sherman, J.M. 1937. The streptococci. Bacteriol. Rev. 1, 3–97.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vlková, B., Szemes, T., Minárik, G. et al. Food-borne enterococci and their resistance to oxidative stress. J Microbiol. 49, 657–662 (2011). https://doi.org/10.1007/s12275-011-0296-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-011-0296-x
Keywords
- Enterococcus faecalis
- reactive oxygen species
- oxidative stress
- free radicals
- infection
- virulence