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Odontology

, Volume 104, Issue 3, pp 310–317 | Cite as

Effects of surface reaction-type pre-reacted glass ionomer on oral biofilm formation of Streptococcus gordonii

  • Kisaki Shimazu
  • Riyo Oguchi
  • Yukihiro Takahashi
  • Kiyoshi Konishi
  • Hiroyuki Karibe
Original Article

Abstract

Streptococcus gordonii, a bacterium involved in the initial colonization of tooth surfaces, contributes to dental biofilm formation and is an important cause of infective endocarditis. This study aimed to investigate the influence of surface reaction-type pre-reacted glass ionomer (S-PRG) filler on oral bacterial growth and aggregation of S. gordonii. The effect of various concentrations of S-PRG eluate on the growth and the biofilm formation of S. gordonii and other oral microorganisms (Streptococcus mutans, Streptococcus oralis, Lactobacillus acidophilus, and Candida albicans) was assessed. In addition, the effect of S-PRG eluate on coaggregation of S. gordonii with both S. oralis and Fusobacterium nucleatum was assessed. The effect of S-PRG eluate treatment on autoaggregation of S. gordonii was also evaluated. Our results indicate that S-PRG eluate treatment reduced both for the growth and for biofilm of all organisms in a dose-dependent manner. Coaggregation of S. gordonii with both S. oralis and F. nucleatum was inhibited by S-PRG eluate, whereas autoaggregation of S. gordonii increased at certain concentrations of S-PRG eluate. These results indicate that the S-PRG filler possesses antimicrobial activity that is mediated by inhibiting growth and biofilm of oral microorganisms, and by suppressing coaggregation of S. gordonii. In addition, these findings indicate that coaggregation of S. gordonii with other bacteria is inhibited by increased autoaggregation of S. gordonii.

Keywords

S-PRG filler Streptococcus gordonii Bacterial growth Coaggregation Biofilm 

Notes

Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research No. 26861845 from Japan Society for the Promotion of Science.

Compliance with ethical standards

Conflict of interest

The S-PRG filler was provided by Shofu Inc. (Kyoto, Japan); however, the sponsor of the study had no role in the study design, conduct of the study, data collection, data interpretation, or preparation of the report.

References

  1. 1.
    Gibbons RJ. Adherent interactions which may affect microbial ecology in the mouth. J Dent Res. 1984;63:378–85.CrossRefPubMedGoogle Scholar
  2. 2.
    Whittaker CJ, Clemans DL, Kolenbrander PE. Insertional inactivation of an intrageneric coaggregation-relevant adhesin locus from Streptococcus gordonii DL1 (Challis). Infect Immun. 1996;64:4137–42.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Cisar JO, Sandberg AL, Abeygunawardana C, Reddy GP, Bush CA. Lectin recognition of host-like saccharide motifs in streptococcal cell wall polysaccharides. Glycobiology. 1995;5:655–62.CrossRefPubMedGoogle Scholar
  4. 4.
    Palmer RJ Jr, Gordon SM, Cisar JO, Kolenbrander PE. Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J Bacteriol. 2003;185:3400–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Lamont RJ, Hersey SG, Rosan B. Characterization of the adherence of Porphyromonas gingivalis to oral streptococci. Oral Microbiol Immunol. 1992;7:193–7.CrossRefPubMedGoogle Scholar
  6. 6.
    Park Y, Simionato MR, Sekiya K, Murakami Y, James D, Chen W, Hackett M, Yoshimura F, Demuth DR, Lamont RJ. Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect Immun. 2005;73:3983–9.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Love RM, McMillan MD, Park Y, Jenkinson HF. Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin. Infect Immun. 2000;68:1359–65.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kolenbrander PE. Intergeneric coaggregation among human oral bacteria and ecology of dental plaque. Annu Rev Microbiol. 1988;42:627–56.CrossRefPubMedGoogle Scholar
  9. 9.
    Tanzer JM, Baranowski LK, Rogers JD, Haase EM, Scannapieco FA. Oral colonization and cariogenicity of Streptococcus gordonii in specific pathogen-free TAN: SPFOM (OM) BR rats consuming starch or sucrose diets. Arch Oral Biol. 2001;46:323–33.CrossRefPubMedGoogle Scholar
  10. 10.
    Baddour LM. Virulence factors among Gram-positive bacteria in experimental endocarditis. Infect Immun. 1994;62:2143–8.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Stinson MW, Alder S, Kumar S. Invasion and killing of human endothelial cells by viridans group streptococci. Infect Immun. 2003;71:2365–72.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Takahashi Y, Takashima E, Shimazu K, Yagishita H, Aoba T, Konishi K. Contribution of sialic acid-binding adhesin to pathogenesis of experimental endocarditis caused by Streptococcus gordonii DL1. Infect Immun. 2006;74:740–3.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Pupo YM, Farago PV, Nadal JM, Simao LC, Esmerino LA, Gomes OM, Gomes JC. Effect of a novel quaternary ammonium methacrylate polymer (QAMP) on adhesion and antibacterial properties of dental adhesives. Int J Mol Sci. 2014;15:8998–9015.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Xu HH, Moreau JL, Sun L, Chow LC. Nanocomposite containing amorphous calcium phosphate nanoparticles for caries inhibition. Dent Mater. 2011;27:762–9.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Cui C, Zhou XN, Chen WM. Self-etching adhesives: possible new pulp capping agents to vital pulp therapy. Front Med. 2011;5:77–9.CrossRefPubMedGoogle Scholar
  16. 16.
    Saku S, Kotake H, Scougall-Vilchis RJ, Ohashi S, Hotta M, Horiuchi S, Hamada K, Asaoka K, Tanaka E, Yamamoto K. Antibacterial activity of composite resin with glass-ionomer filler particles. Dent Mater J. 2010;29:193–8.CrossRefPubMedGoogle Scholar
  17. 17.
    Shimazu K, Ogata K, Karibe H. Evaluation of the ion-releasing and recharging abilities of a resin-based fissure sealant containing S-PRG filler. Dent Mater J. 2011;30:923–7.CrossRefPubMedGoogle Scholar
  18. 18.
    Han L, Cv E, Li M, Niwano K, Ab N, Okamoto A, Honda N, Iwaku M. Effect of fluoride mouth rinse on fluoride releasing and recharging from aesthetic dental materials. Dent Mater J. 2002;21:285–95.CrossRefPubMedGoogle Scholar
  19. 19.
    Itota T, Carrick TE, Yoshiyama M, McCabe JF. Fluoride release and recharge in giomer, compomer and resin composite. Dent Mater. 2004;20:789–95.CrossRefPubMedGoogle Scholar
  20. 20.
    Kamijo K, Mukai Y, Tominaga T, Iwaya I, Fujino F, Hirata Y, Teranaka T. Fluoride release and recharge characteristics of denture base resins containing surface pre-reacted glass-ionomer filler. Dent Mater J. 2009;28:227–33.CrossRefPubMedGoogle Scholar
  21. 21.
    Han L, Okamoto A, Fukushima M, Okiji T. Evaluation of a new fluoride-releasing one-step adhesive. Dent Mater J. 2006;25:509–15.CrossRefPubMedGoogle Scholar
  22. 22.
    Itota T, Carrick TE, Rusby S, Al-Naimi OT, Yoshiyama M, McCabe JF. Determination of fluoride ions released from resin-based dental materials using ion-selective electrode and ion chromatograph. J Dent. 2004;32:117–22.CrossRefPubMedGoogle Scholar
  23. 23.
    Mukai Y, Kamijo K, Fujino F, Hirata Y, Teranaka T, ten Cate JM. Effect of denture base-resin with prereacted glass-ionomer filler on dentin demineralization. Eur J Oral Sci. 2009;117:750–4.CrossRefPubMedGoogle Scholar
  24. 24.
    Mukai Y, Tomiyama K, Shiiya T, Kamijo K, Fujino F, Teranaka T. Formation of inhibition layers with a newly developed fluoride-releasing all-in-one adhesive. Dent Mater J. 2005;24:172–7.CrossRefPubMedGoogle Scholar
  25. 25.
    Shimazu K, Ogata K, Karibe H. Caries-preventive effect of fissure sealant containing surface reaction-type pre-reacted glass ionomer filler and bonded by self-etching primer. J Clin Pediatr Dent. 2012;36:343–7.CrossRefPubMedGoogle Scholar
  26. 26.
    Fujimoto Y, Iwasa M, Murayama R, Miyazaki M, Nagafuji A, Nakatsuka T. Detection of ions released from S-PRG fillers and their modulation effect. Dent Mater J. 2010;29:392–7.CrossRefPubMedGoogle Scholar
  27. 27.
    Yoneda M, Suzuki N, Masuo Y, Fujimoto A, Iha K, Yamada K, Iwamoto T, Hirofuji T. Effect of S-PRG eluate on biofilm formation and enzyme activity of oral bacteria. Int J Dent. 2012;2012:1–6.CrossRefGoogle Scholar
  28. 28.
    Suzuki N, Yoneda M, Haruna K, Masuo Y, Nishihara T, Nakanishi K, Yamada K, Fujimoto A, Hirofuji T. Effects of S-PRG eluate on oral biofilm and oral malodor. Arch Oral Biol. 2014;59:407–13.CrossRefPubMedGoogle Scholar
  29. 29.
    Liljemark WF, Bloomquist C. Human oral microbial ecology and dental caries and periodontal diseases. Crit Rev Oral Biol Med. 1996;7:180–98.CrossRefPubMedGoogle Scholar
  30. 30.
    Tahmourespour A, Kermanshahi RK. The effect of a probiotic strain (Lactobacillus acidophilus) on the plaque formation of oral streptococci. Bosn J Basic Med Sci. 2011;11:37–40.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Corcuera MT, Gomez-Lus ML, Gomez-Aguado F, Maestre JR, Ramos Mdel C, Alonso MJ, Prieto J. Morphological plasticity of Streptococcus oralis isolates for biofilm production, invasiveness, and architectural patterns. Arch Oral Biol. 2013;58:1584–93.CrossRefPubMedGoogle Scholar
  32. 32.
    Douglas CW, Heath J, Hampton KK, Preston FE. Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol. 1993;39:179–82.CrossRefPubMedGoogle Scholar
  33. 33.
    Felk A, Kretschmar M, Albrecht A, Schaller M, Beinhauer S, Nichterlein T, Sanglard D, Korting HC, Schäfer W, Hube B. Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect Immun. 2002;70:3689–700.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. Nonfilamentous C. albicans mutants are avirulent. Cell. 1997;90:939–49.CrossRefPubMedGoogle Scholar
  35. 35.
    Loo CY, Corliss DA, Ganeshkumar N. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol. 2000;182:1374–82.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Cisar JO, Kolenbrander PE, McIntire FC. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun. 1979;24:742–52.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Kolenbrander PE, Andersen RN, Holdeman LV. Coaggregation of oral Bacteroides species with other bacteria: central role in coaggregation bridges and competitions. Infect Immun. 1985;48:741–6.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Palmer RJ Jr, Gordon SM, Cisar JO, Kolenbrander PE. Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J Bacteriol. 2003;185:3400–9.CrossRefPubMedGoogle Scholar
  39. 39.
    Takemoto T, Hino T, Yoshida M, Nakanishi K, Shirakawa M, Okamoto H. Characteristics of multimodal co-aggregation between Fusobacterium nucleatum and streptococci. J Periodontal Res. 1995;30:252–7.CrossRefPubMedGoogle Scholar
  40. 40.
    Kinder SA, Holt SC. Characterization of coaggregation between Bacteroides gingivalis T22 and Fusobacterium nucleatum T18. Infect Immun. 1989;57:3425–33.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Han L, Takenaka S, Okiji T. Evaluation of selected properties of a prototype S-PRG filler containing root canal sealer. Jpn J Conserv Dent. 2007;50:713–20.Google Scholar
  42. 42.
    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.CrossRefPubMedGoogle Scholar
  43. 43.
    Egland PG, Du LD, Kolenbrander PE. Identification of independent Streptococcus gordonii SspA and SspB functions in coaggregation with Actinomyces naeslundii. Infect Immun. 2001;69:7512–6.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Jakubovics NS, Kerrigan SW, Nobbs AH, Stromberg N, van Dolleweerd CJ, Cox DM, Kelly CG, Jenkinson HF. Functions of cell surface-anchored antigen I/II family and Hsa polypeptides in interactions of Streptococcus gordonii with host receptors. Infect Immun. 2005;73:6629–38.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Takahashi Y, Konishi K, Cisar JO, Yoshikawa M. Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun. 2002;70:1209–18.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Nobbs AH, Zhang Y, Khammanivong A, Herzberg MC. Streptococcus gordonii Hsa environmentally constrains competitive binding by Streptococcus sanguinis to saliva-coated hydroxyapatite. J Bacteriol. 2007;189:3106–14.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kinder SA, Holt SC. Coaggregation between bacterial species. Methods Enzymol. 1994;236:254–70.CrossRefPubMedGoogle Scholar
  48. 48.
    Guo L, Wu T, Hu W, He X, Sharma S, Webster P, Gimzewski JK, Zhou X, Lux R, Shi W. Phenotypic characterization of the foldase homologue PrsA in Streptococcus mutans. Mol Oral Microbiol. 2013;28:154–65.CrossRefPubMedGoogle Scholar

Copyright information

© The Society of The Nippon Dental University 2015

Authors and Affiliations

  • Kisaki Shimazu
    • 1
  • Riyo Oguchi
    • 1
  • Yukihiro Takahashi
    • 2
  • Kiyoshi Konishi
    • 2
  • Hiroyuki Karibe
    • 1
  1. 1.Department of Pediatric DentistryThe Nippon Dental University School of Life Dentistry at TokyoTokyoJapan
  2. 2.Department of MicrobiologyThe Nippon Dental University School of Life Dentistry at TokyoTokyoJapan

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