Skip to main content

Advertisement

SpringerLink
Log in

Effect of S53P4 bone substitute on staphylococcal adhesion and biofilm formation on other implant materials in normal and hypoxic conditions

  • Biocompatibility Studies
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

To study the effect of bioactive glass bone substitute granules (S53P4) on bacterial adhesion and biofilm formation on other simultaneously used implant materials and the role of the hypoxic conditions to the adhesion. Bacterial and biofilm formation were studied on materials used both in middle ear prostheses and in fracture fixtures (titanium, polytetrafluoroethylene, polydimethylsiloxane and bioactive glass plates) in the presence or absence of S53P4 granules. The experiments were done either in normal atmosphere or in hypoxia simulating atmospheric conditions of middle ear, mastoid cavity and sinuses. We used two collection strains of Staphylococcus aureus and Staphylococcus epidermidis. In the presence of bioglass and hypoxic conditions the adhesion of the planktonic bacterial cells was decreased for most of the materials. The biofilm formation was decreased for S. epidermidis on titanium and polydimethylsiloxane in both atmospheric conditions and on bioglass plates in normoxia. For S. aureus the biofilm formation was decreased on bioglass plates and polytetrafluoroethylene in normoxia. Hypoxia produces a decrease in the biofilm formation only for S. aureus on polytetrafluoroethylene and for S. epidermidis on bioglass plates. However, in none of the cases bioactive glass increased the bacterial or biofilm adhesion. The presence of bioglass in normoxic and hypoxic conditions prevents the bacterial and biofilm adhesion on surfaces of several typical prosthesis materials in vitro. This may lead to diminishing postoperative infections, however, further in vivo studies are needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Andriole VT, Nagel DA, Southwick WO. A paradigm for human chronic osteomyelitis. J Bone Joint Surg Am. 1973;55(7):1511–5.

    Google Scholar 

  2. Rochford ET, Richards RG, Moriarty TF. Influence of material on the development of device-associated infections. Clin Microbiol Infect. 2012;18(12):1162–7.

    Article  Google Scholar 

  3. Guggenbichler JP, Assadian O, Boeswald M, Kramer A. Incidence and clinical implication of nosocomial infections associated with implantable biomaterials—catheters, ventilator-associated pneumonia, urinary tract infections. GMS Krankenhhyg Interdiszip. 2011;6(1):Doc18.

  4. Elek SD, Conen PE. The virulence of Staphylococcus pyogenes for man; a study of the problems of wound infection. Br J Exp Pathol. 1957;38(6):573–86.

    Google Scholar 

  5. Deysine M. Infections associated with surgical implants. N Engl J Med. 2004;351(2):193–5.

    Article  Google Scholar 

  6. Katsikogianni M, Missirlis YF. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cell Mater. 2004;8:37–57.

    Google Scholar 

  7. Perez-Tanoira R, Perez-Jorge C, Endrino JL, Gomez-Barrena E, Horwat D, Pierson JF, et al. Bacterial adhesion on biomedical surfaces covered by micrometric silver Islands. J Biomed Mater Res Part A. 2012;100(6):1521–8.

    Article  Google Scholar 

  8. Stoor P, Pulkkinen J, Grenman R. Bioactive glass S53P4 in the filling of cavities in the mastoid cell area in surgery for chronic otitis media. Ann Otol Rhinol Laryngol. 2010;119(6):377–82.

    Google Scholar 

  9. Stoor P, Soderling E, Grenman R. Bioactive glass S53P4 in repair of septal perforations and its interactions with the respiratory infection-associated microorganisms Haemophilus influenzae and Streptococcus pneumoniae. J Biomed Mater Res. 2001;58(1):113–20.

    Article  Google Scholar 

  10. Stoor P, Soderling E, Grenman R. Interactions between the bioactive glass S53P4 and the atrophic rhinitis-associated microorganism Klebsiella ozaenae. J Biomed Mater Res. 1999;48(6):869–74.

    Article  Google Scholar 

  11. Yung M, Tassone P, Moumoulidis I, Vivekanandan S. Surgical management of troublesome mastoid cavities. J Laryngol Otol. 2011;125(3):221–6.

    Article  Google Scholar 

  12. Peltola M, Aitasalo K, Suonpaa J, Varpula M, Yli-Urpo A. Bioactive glass S53P4 in frontal sinus obliteration: a long-term clinical experience. Head Neck. 2006;28(9):834–41.

    Article  Google Scholar 

  13. Munukka E, Leppäranta O, Korkeamäki M, Vaahtio M, Peltola T, Zhang D, et al. Bactericidal effects of bioactive glasses on clinically important aerobic bacteria. J Mater Sci Mater Med. 2008;19:27–32.

    Article  Google Scholar 

  14. Jones JR. Review of bioactive glass: from Hench to hybrids. Acta Biomater. 2013;9(1):4457–86.

    Article  Google Scholar 

  15. Leppäranta O, Vaahtio M, Peltola T, Zhang D, Hupa L, Hupa M, et al. Antibacterial effect of bioactive glasses on clinically important anaerobic bacteria in vitro. J Mater Sci Mater Med. 2008;19:547–51.

    Article  Google Scholar 

  16. Hench LLPH. Direct chemical bond of bioactive glass-ceramic materials to bone and muscle. J Biomed Mater Res. 1973;7(3):25–42.

    Article  Google Scholar 

  17. Cui X, Zhao C, Gu Y, Li L, Wang H, Huang W, et al. A novel injectable borate bioactive glass cement for local delivery of vancomycin to cure osteomyelitis and regenerate bone. J Mater Sci Mater Med. 2014;25(3):733–45.

    Article  Google Scholar 

  18. Coraca-Huber DC, Fille M, Hausdorfer J, Putzer D, Nogler M. Efficacy of antibacterial bioactive glass S53P4 against S. aureus biofilms grown on titanium discs in vitro. J Orthop Res. 2014;32(1):175–7.

    Article  Google Scholar 

  19. Drago L, Romano D, De Vecchi E, Vassena C, Logoluso N, Mattina R, et al. Bioactive glass BAG-S53P4 for the adjunctive treatment of chronic osteomyelitis of the long bones: an in vitro and prospective clinical study. BMC Infect Dis. 2013;13:584.

    Article  Google Scholar 

  20. Stoor P, Soderling E, Salonen JI. Antibacterial effects of a bioactive glass paste on oral microorganisms. Acta Odontol Scand. 1998;56(3):161–5.

    Article  Google Scholar 

  21. Drago L, Vassena C, Fenu S, De Vecchi E, Signori V, De Francesco R, et al. In vitro antibiofilm activity of bioactive glass S53P4. Future Microbiol. 2014;9(5):593–601.

    Article  Google Scholar 

  22. Luntz M, Levi D, Sade J, Herman M. Relationship between the gas composition of the middle ear and the venous blood at steady state. Laryngoscope. 1995;105(5 Pt 1):510–2.

    Article  Google Scholar 

  23. Hergils L, Magnuson B. Human middle ear gas composition studied by mass spectrometry. Acta Otolaryngol. 1990;110(1–2):92–9.

    Article  Google Scholar 

  24. Kinnari TJ, Soininen A, Esteban J, Zamora N, Alakoski E, Kouri VP, et al. Adhesion of staphylococcal and Caco-2 cells on diamond-like carbon polymer hybrid coating. J Biomed Mater Res Part A. 2008;86(3):760–8.

    Article  Google Scholar 

  25. Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, Penades JR, et al. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol. 2003;48(4):1075–87.

    Article  Google Scholar 

  26. Boulos L, Prevost M, Barbeau B, Coallier J, Desjardins R. LIVE/DEAD BacLight : application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J Microbiol Methods. 1999;37(1):77–86.

    Article  Google Scholar 

  27. Buckingham-Meyer K, Goeres DM, Hamilton MA. Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods. 2007;70(2):236–44.

    Article  Google Scholar 

  28. Esteban J, Gomez-Barrena E, Cordero J, Martin-de-Hijas NZ, Kinnari TJ, Fernandez-Roblas R. Evaluation of quantitative analysis of cultures from sonicated retrieved orthopedic implants in diagnosis of orthopedic infection. J Clin Microbiol. 2008;46(2):488–92.

    Article  Google Scholar 

  29. Kobayashi N, Bauer TW, Tuohy MJ, Fujishiro T, Procop GW. Brief ultrasonication improves detection of biofilm-formative bacteria around a metal implant. Clin Orthop Relat Res. 2007;457:210–3.

    Google Scholar 

  30. Herigstad B, Hamilton M, Heersink J. How to optimize the drop plate method for enumerating bacteria. J Microbiol Methods. 2001;44(2):121–9.

    Article  Google Scholar 

  31. Schaible B, Taylor CT, Schaffer K. Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition of multidrug efflux pumps. Antimicrob Agents Chemother. 2012;56(4):2114–8.

    Article  Google Scholar 

  32. Hu S, Chang J, Liu M, Ning C. Study on antibacterial effect of 45S5 Bioglass. J Mater Sci Mater Med. 2009;20(1):281–6.

    Article  Google Scholar 

  33. Rivadeneira J, Carina Audisio M, Boccaccini AR, Gorustovich AA. In vitro antistaphylococcal effects of a novel 45S5 bioglass/agar-gelatin biocomposite films. J Appl Microbiol. 2013;115(2):604–12.

    Article  Google Scholar 

  34. Kwok P, Fisch U, Strutz J, Jacob P. Comparative electron microscopic study of the surface structure of gold, Teflon, and titanium stapes prostheses. Otol Neurotol. 2001;22(5):608–13.

    Article  Google Scholar 

  35. Cramton SE, Ulrich M, Gotz F, Doring G. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun. 2001;69(6):4079–85.

    Article  Google Scholar 

  36. Borzabadi-Farahani A, Borzabadi E, Lynch E. Nanoparticles in orthodontics, a review of antimicrobial and anti-caries applications. Acta Odontol Scand. 2014;72(6):413–7.

    Article  Google Scholar 

Download references

Acknowledgments

This project was financially supported by the Finska Läkaresällskapet and the special subsidiary fund of the Helsinki University Central Hospital.

Author information

Authors and Affiliations

  1. Otorhinolaryngology-Head and Neck Surgery, University of Helsinki and Helsinki University Hospital, Haartmaninkatu 4 E, 00029, Helsinki, Finland

    R. Pérez-Tanoira, M. García-Pedrazuela, T. Hyyrynen, A. Aarnisalo & T. J. Kinnari

  2. Department of Clinical Microbiology, IIS-Fundación Jiménez Díaz, Madrid, Spain

    R. Pérez-Tanoira & M. García-Pedrazuela

  3. ORTON Research Institute, Helsinki, Finland

    A. Soininen, V.-M. Tiainen & Y. T. Konttinen

  4. ORTON Orthopedic Hospital, Helsinki, Finland

    A. Soininen, V.-M. Tiainen & Y. T. Konttinen

  5. Department of Bacteriology and Immunology, Haartman Institute, University of Helsinki, Helsinki, Finland

    Mikko T. Nieminen

  6. Oral and Maxillofacial Diseases, University of Helsinki and Helsinki University Hospital, Helsinki, Finland

    Mikko T. Nieminen

  7. Department of Medicine, Institute of Clinical Medicine, Biomedicum, Helsinki, Finland

    Y. T. Konttinen

  8. COXA Hospital for Joint Replacement, Tampere, Finland

    Y. T. Konttinen

Authors
  1. R. Pérez-Tanoira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. García-Pedrazuela
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Hyyrynen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Soininen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Aarnisalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mikko T. Nieminen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. V.-M. Tiainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Y. T. Konttinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T. J. Kinnari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Pérez-Tanoira.

Ethics declarations

Conflict of interest

None to declare.

Additional information

R. Pérez-Tanoira and M. García-Pedrazuela are two first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Tanoira, R., García-Pedrazuela, M., Hyyrynen, T. et al. Effect of S53P4 bone substitute on staphylococcal adhesion and biofilm formation on other implant materials in normal and hypoxic conditions. J Mater Sci: Mater Med 26, 239 (2015). https://doi.org/10.1007/s10856-015-5569-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-015-5569-1

Keywords

Search

Navigation