Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
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A periodontitis-associated multispecies model of an oral biofilm

  • Park, Jong Hwa (Department of Periodontology, Research Institute of Oral Sciences, Gangneung-Wonju National University College of Dentistry) ;
  • Lee, Jae-Kwan (Department of Periodontology, Research Institute of Oral Sciences, Gangneung-Wonju National University College of Dentistry) ;
  • Um, Heung-Sik (Department of Periodontology, Research Institute of Oral Sciences, Gangneung-Wonju National University College of Dentistry) ;
  • Chang, Beom-Seok (Department of Periodontology, Research Institute of Oral Sciences, Gangneung-Wonju National University College of Dentistry) ;
  • Lee, Si-Young (Department of Microbiology and Immunology, Research Institute of Oral Sciences, Gangneung-Wonju National University College of Dentistry)
  • Received : 2014.02.25
  • Accepted : 2014.03.20
  • Published : 2014.04.30
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Abstract

Purpose: While single-species biofilms have been studied extensively, we know notably little regarding multispecies biofilms and their interactions. The purpose of this study was to develop and evaluate an in vitro multispecies dental biofilm model that aimed to mimic the environment of chronic periodontitis. Methods: Streptococcus gordonii KN1, Fusobacterium nucleatum ATCC23726, Aggregatibacter actinomycetemcomitans ATCC33384, and Porphyromonas gingivalis ATCC33277 were used for this experiment. The biofilms were grown on 12-well plates with a round glass slip (12 mm in diameter) with a supply of fresh medium. Four different single-species biofilms and multispecies biofilms with the four bacterial strains listed above were prepared. The biofilms were examined with a confocal laser scanning microscope (CLSM) and scanning electron microscopy (SEM). The minimum inhibitory concentrations (MIC) for four different planktonic single-species and multispecies bacteria were determined. The MICs of doxycycline and chlorhexidine for four different single-species biofilms and a multispecies biofilm were also determined. Results: The CLSM and SEM examination revealed that the growth pattern of the multispecies biofilm was similar to those of single-species biofilms. However, the multispecies biofilm became thicker than the single-species biofilms, and networks between bacteria were formed. The MICs of doxycycline and chlorhexidine were higher in the biofilm state than in the planktonic bacteria. The MIC of doxycycline for the multispecies biofilm was higher than were those for the single-species biofilms of P. gingivalis, F. nucleatum, or A. actinomycetemcomitans. The MIC of chlorhexidine for the multispecies biofilm was higher than were those for the single-species biofilms of P. gingivalis or F. nucleatum. Conclusions: To mimic the natural dental biofilm, a multispecies biofilm composed of four bacterial species was grown. The 24-hour multispecies biofilm may be useful as a laboratory dental biofilm model system.

Keywords

References

  1. Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontol 2000 2002;28:12-55. https://doi.org/10.1034/j.1600-0757.2002.280102.x
  2. Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005;38:72-122. https://doi.org/10.1111/j.1600-0757.2005.00113.x
  3. Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 2010;8:471-80. https://doi.org/10.1038/nrmicro2381
  4. James GA, Korber DR, Caldwell DE, Costerton JW. Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J Bacteriol 1995;177:907-15. https://doi.org/10.1128/jb.177.4.907-915.1995
  5. Kolenbrander PE, Palmer RJ Jr, Rickard AH, Jakubovics NS, Chalmers NI, Diaz PI. Bacterial interactions and successions during plaque development. Periodontol 2000 2006;42:47-79. https://doi.org/10.1111/j.1600-0757.2006.00187.x
  6. Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol 2005;13:34-40. https://doi.org/10.1016/j.tim.2004.11.010
  7. Wilson M. Susceptibility of oral bacterial biofilms to antimicrobial agents. J Med Microbiol 1996;44:79-87. https://doi.org/10.1099/00222615-44-2-79
  8. Sissons CH. Artificial dental plaque biofilm model systems. Adv Dent Res 1997;11:110-26. https://doi.org/10.1177/08959374970110010201
  9. Schlafer S, Raarup MK, Meyer RL, Sutherland DS, Dige I, Nyengaard JR, et al. pH landscapes in a novel five-species model of early dental biofilm. PLoS One 2011;6:e25299. https://doi.org/10.1371/journal.pone.0025299
  10. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ Jr. Communication among oral bacteria. Microbiol Mol Biol Rev 2002;66:486-505. https://doi.org/10.1128/MMBR.66.3.486-505.2002
  11. Sader HS, Flamm RK, Jones RN. Antimicrobial activity of daptomycin tested against Gram-positive pathogens collected in Europe, Latin America, and selected countries in the Asia-Pacific Region (2011). Diagn Microbiol Infect Dis 2013;75:417-22. https://doi.org/10.1016/j.diagmicrobio.2013.01.001
  12. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 2000;27:648-57. https://doi.org/10.1034/j.1600-051x.2000.027009648.x
  13. Prates RA, Yamada AM Jr, Suzuki LC, Eiko Hashimoto MC, Cai S, Gouw-Soares S, et al. Bactericidal effect of malachite green and red laser on Actinobacillus actinomycetemcomitans. J Photochem Photobiol B 2007;86:70-6. https://doi.org/10.1016/j.jphotobiol.2006.07.010
  14. Wright TL, Ellen RP, Lacroix JM, Sinnadurai S, Mittelman MW. Effects of metronidazole on Porphyromonas gingivalis biofilms. J Periodontal Res 1997;32:473-7. https://doi.org/10.1111/j.1600-0765.1997.tb00560.x
  15. Sanchez MC, Llama-Palacios A, Blanc V, Leon R, Herrera D, Sanz M. Structure, viability and bacterial kinetics of an in vitro biofilm model using six bacteria from the subgingival microbiota. J Periodontal Res 2011;46:252-60. https://doi.org/10.1111/j.1600-0765.2010.01341.x
  16. Periasamy S, Kolenbrander PE. Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 2009;191:6804-11. https://doi.org/10.1128/JB.01006-09
  17. Walker C, Sedlacek MJ. An in vitro biofilm model of subgingival plaque. Oral Microbiol Immunol 2007;22:152-61. https://doi.org/10.1111/j.1399-302X.2007.00336.x
  18. Prescott JF, Baggot JD. Antimicrobial susceptibility testing and antimicrobial drug dosage. J Am Vet Med Assoc 1985;187:363-8.
  19. Song HH, Lee JK, Um HS, Chang BS, Lee SY, Lee MK. Phototoxic effect of blue light on the planktonic and biofilm state of anaerobic periodontal pathogens. J Periodontal Implant Sci 2013;43:72-8. https://doi.org/10.5051/jpis.2013.43.2.72

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