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Characterization of antibiotic resistance determinants in oral biofilms

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Abstract

Oral biofilms contain numerous antibiotic resistance determinants that can be transferred within or outside of the oral cavity. The aim of this study was to evaluate the prevalence and the relative level of antibiotic resistance determinants from oral biofilms. Oral biofilm samples that were collected from healthy subjects and periodontitis patients were subjected to qualitative and quantitative analyses for selected antibiotic resistance determinants using PCR. The prevalence of tet(Q), tet(M), cfxA, and bla TEM was very high both in the patient and the healthy subject group, with a tendency toward higher values in the patient group, with the exception of erm(F), which was more prevalent in the healthy group. The two extended spectrum β-lactam (ESBL) resistance determinants bla SHV and bla TEM showed a dramatic difference, as bla TEM was present in all of the samples and bla SHV was not found at all. The aacA-aphD, vanA, and mecA genes were rarely detected, suggesting that they are not common in oral bacteria. A quantitative PCR analysis showed that the relative amount of resistance determinants present in oral biofilms of the patient group was much greater than that of the healthy group, exhibiting 17-, 13-, 145-, and 3-fold increases for tet(Q), tet(M), erm(F), and cfxA, respectively. The results of this study suggest that the oral antibiotic resistome is more diverse and abundant in periodontitis patients than in healthy subjects, suggesting that there is a difference in the diversity and distribution of antibiotic resistance in oral biofilms associated with health and disease.

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References

  • Aas, J.A., B.J. Paster, L.N. Stokes, I. Olsen, and F.E. Dewhirst. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43, 5721–5732.

    Article  PubMed  Google Scholar 

  • Amann, R.I., W. Ludwig, and K.H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–169.

    PubMed  CAS  Google Scholar 

  • Bradford, P.A. 2001. Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 14, 933–951, table.

    Article  PubMed  CAS  Google Scholar 

  • Chung, W.O., J. Gabany, G.R. Persson, and M.C. Roberts. 2002. Distribution of erm(F) and tet(Q) genes in 4 oral bacterial species and genotypic variation between resistant and susceptible isolates. J. Clin. Periodontol. 29, 152–158.

    Article  PubMed  CAS  Google Scholar 

  • D’Costa, V.M., K.M. McGrann, D.W. Hughes, and G.D. Wright. 2006. Sampling the antibiotic resistome. Science 311, 374–377.

    Article  PubMed  Google Scholar 

  • Diaz-Torres, M.L., R. McNab, D.A. Spratt, A. Villedieu, N. Hunt, M. Wilson, and P. Mullany. 2003. Novel tetracycline resistance determinant from the oral metagenome. Antimicrob. Agents Chemother. 47, 1430–1432.

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Torres, M.L., A. Villedieu, N. Hunt, R. McNab, D.A. Spratt, E. Allan, P. Mullany, and M. Wilson. 2006. Determining the antibiotic resistance potential of the indigenous oral microbiota of humans using a metagenomic approach. FEMS Microbiol. Lett. 258, 257–262.

    Article  PubMed  CAS  Google Scholar 

  • Fluit, A.C., M.R. Visser, and F.J. Schmitz. 2001. Molecular detection of antimicrobial resistance. Clin. Microbiol. Rev. 14, 836–871.

    Article  PubMed  CAS  Google Scholar 

  • Handelsman, J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68, 669–685.

    Article  PubMed  CAS  Google Scholar 

  • Iwahara, K., T. Kuriyama, S. Shimura, D.W. Williams, M. Yanagisawa, K. Nakagawa, and T. Karasawa. 2006. Detection of cfxA and cfxA2, the beta-lactamase genes of Prevotella spp., in clinical samples from dentoalveolar infection by real-time PCR. J. Clin. Microbiol. 44, 172–176.

    Article  PubMed  CAS  Google Scholar 

  • Kroes, I., P.W. Lepp, and D.A. Relman. 1999. Bacterial diversity within the human subgingival crevice. Proc. Natl. Acad. Sci. USA 96, 14547–14552.

    Article  PubMed  CAS  Google Scholar 

  • Levy, S.B. 1997. Antibiotic resistance: an ecological imbalance, pp. 1–14. In D.J.a.G.J. Chadwick (ed.), Antibiotic Resistance: Origins, Evolution, Selection and Spread, CIBA Foundation Symposium 207, Wiley, Chichester, UK.

    Google Scholar 

  • Livak, K.J. and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.

    Article  PubMed  CAS  Google Scholar 

  • Maeda, H., C. Fujimoto, Y. Haruki, T. Maeda, S. Kokeguchi, M. Petelin, H. Arai, I. Tanimoto, F. Nishimura, and S. Takashiba. 2003. Quantitative real-time PCR using TaqMan and SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol. Med. Microbiol. 39, 81–86.

    Article  PubMed  CAS  Google Scholar 

  • Marsh, P.D. 2003. Are dental diseases examples of ecological catastrophes?. Microbiology 149, 279–294.

    Article  PubMed  CAS  Google Scholar 

  • Marsh, P.D. 2004. Dental plaque as a microbial biofilm. Caries Res. 38, 204–211.

    Article  PubMed  CAS  Google Scholar 

  • Marsh, P.D. 2005. Dental plaque: biological significance of a biofilm and community life-style J. Clin. Periodontol. 32Suppl 6, 7–15.

    Article  PubMed  CAS  Google Scholar 

  • Mazel, D. and J. Davies. 1999. Antibiotic resistance in microbes Cell Mol. Life Sci. 56, 742–754.

    Article  PubMed  CAS  Google Scholar 

  • Medeiros, A.A. 1997. beta-Lactamases: quality and resistance. Clin. Microbiol. Infect. 3Suppl 4, S2–S9.

    PubMed  Google Scholar 

  • Mercer, D.K., K.P. Scott, C.M. Melville, L.A. Glover, and H.J. Flint. 2001. Transformation of an oral bacterium via chromosomal integration of free DNA in the presence of human saliva FEMS Microbiol. Lett. 200, 163–167.

    CAS  Google Scholar 

  • Moore, W.E. and L.V. Moore. 1994. The bacteria of periodontal diseases. Periodontol 2000 5, 66–77.

    Article  CAS  Google Scholar 

  • Okamoto, M., K. Takano, and N. Maeda. 2001. Distribution of the tetracycline resistance determinant tetQ gene in oral isolates of black-pigmented anaerobes in Japan. Oral Microbiol. Immunol. 16, 224–228.

    Article  PubMed  CAS  Google Scholar 

  • Paster, B.J., S.K. Boches, J.L. Galvin, R.E. Ericson, C.N. Lau, V.A. Levanos, A. Sahasrabudhe, and F.E. Dewhirst. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770–3783.

    Article  PubMed  CAS  Google Scholar 

  • Paster, B.J., I. Olsen, J.A. Aas, and F.E. Dewhirst. 2006. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42, 80–87.

    Article  Google Scholar 

  • Pintado, C., C. Salvador, R. Rotger, and C. Nombela. 1985. Multiresistance plasmid from commensal Neisseria strains. Antimicrob. Agents Chemother. 27, 120–124.

    PubMed  CAS  Google Scholar 

  • Roberts, M.C. 1998. Antibiotic resistance in oral/respiratory bacteria. Crit. Rev. Oral Biol. Med. 9, 522–540.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, A.P., G. Cheah, D. Ready, J. Pratten, M. Wilson, and P. Mullany. 2001. Transfer of TN916-like elements in microcosm dental plaques. Antimicrob. Agents Chemother. 45, 2943–2946.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, A.P. and P. Mullany. 2006. Genetic basis of horizontal gene transfer among oral bacteria. Periodontol. 2000 42, 36–46.

    Article  Google Scholar 

  • Roberts, A.P., J. Pratten, M. Wilson, and P. Mullany. 1999. Transfer of a conjugative transposon, Tn5397 in a model oral biofilm. FEMS Microbiol. Lett. 177, 63–66.

    Article  PubMed  CAS  Google Scholar 

  • Seville, L.A., A.J. Patterson, K.P. Scott, P. Mullany, M.A. Quail, J. Parkhill, D. Ready, M. Wilson, D. Spratt, and A.P. Roberts. 2009. Distribution of tetracycline and erythromycin resistance genes among human oral and fecal metagenomic DNA. Microb. Drug Resist. 15, 159–166.

    Article  PubMed  CAS  Google Scholar 

  • Socransky, S.S. and A.D. Haffajee. 1994. Evidence of bacterial etiology: a historical perspective. Periodontol. 2000. 5, 7–25.

    Article  Google Scholar 

  • Socransky, S.S. and A.D. Haffajee. 2002. Dental biofilms: difficult therapeutic targets. Periodontol. 2000 28, 12–55.

    Article  Google Scholar 

  • Socransky, S.S., A.D. Haffajee, M.A. Cugini, C. Smith, and R.L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25, 134–144.

    Article  PubMed  CAS  Google Scholar 

  • Sommer, M.O., G. Dantas, and G.M. Church. 2009. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325, 1128–1131.

    Article  PubMed  CAS  Google Scholar 

  • Van Winkelhoff, A.J., T.E. Rams, and J. Slots. 1996. Systemic antibiotic therapy in periodontics. Periodontol. 2000 10, 45–78.

    Article  Google Scholar 

  • Wang, B.Y., B. Chi, and H.K. Kuramitsu. 2002. Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms. Oral Microbiol. Immunol. 17, 108–112.

    Article  PubMed  CAS  Google Scholar 

  • Yoo, J.Y., H.C. Kim, W. Zhu, S.M. Kim, M. Sabet, M. Handfield, J. Hillman, A. Progulske-Fox, and S.W. Lee. 2007. Identification of Tannerella forsythia antigens specifically expressed in patients with periodontal disease. FEMS Microbiol. Lett. 275, 344–352.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Seok-Woo S. Lee.

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Kim, SM., Kim, H.C. & Lee, SW.S. Characterization of antibiotic resistance determinants in oral biofilms. J Microbiol. 49, 595–602 (2011). https://doi.org/10.1007/s12275-011-0519-1

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