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Journal of Materials Science: Materials in Medicine

, Volume 24, Issue 12, pp 2775–2785 | Cite as

In vitro antimicrobial properties of silver–polysaccharide coatings on porous fiber-reinforced composites for bone implants

  • Sara NgangaEmail author
  • Andrea Travan
  • Eleonora Marsich
  • Ivan Donati
  • Eva Söderling
  • Niko Moritz
  • Sergio Paoletti
  • Pekka K. Vallittu
Article

Abstract

Biostable fiber-reinforced composite (FRC) implants prepared from bisphenol-A-dimethacrylate and triethyleneglycoldimethacrylate resin reinforced with E-glass fibers have been successfully used in cranial reconstructions in 15 patients. Recently, porous FRC structures were suggested as potential implant materials. Compared with smooth surface, porous surface allows implant incorporation via bone ingrowth, but is also a subject to bacterial attachment. Non-cytotoxic silver–polysaccharide nanocomposite coatings may provide a way to decrease the risk of bacterial contamination of porous FRC structures. This study is focused on the in vitro characterization of the effect porosity on the antimicrobial efficiency of the coatings against Staphylococcus aureus and Pseudomonas aeruginosa by a series of microbiological tests (initial adhesion, antimicrobial efficacy, and biofilm formation). Characterization included confocal laser scanning microscopy and scanning electron microscopy. The effect of porosity on the initial attachment of S. aureus was pronounced, but in the case of P. aeruginosa the effect was negligible. There were no significant effects of the coatings on the initial bacterial attachment. In the antimicrobial efficacy test, the coatings were potent against both strains regardless of the sample morphology. In the biofilm tests, there were no clear effects either of morphology or of the coating. Further coating development is foreseen to achieve a longer-term antimicrobial effect to inhibiting bacterial implant colonization.

Keywords

Silver Nanoparticles DMAEMA Antimicrobial Efficacy Initial Adhesion Confocal Laser Scanning Microscopy Image 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study was performed in cooperation of the Department of Biomaterials Science at the University of Turku (Finland) (www.biomaterials.utu.fi) and the Department of Life Sciences at the University of Trieste (Italy). The authors gratefully acknowledge the Finnish National Doctoral Programme of Musculo-Skeletal Disorders and Biomaterials (TBDP) and the Academy of Finland (BioCity Turku Biomaterials Research Programme) for their financial support. They would also like to thank Gabriele Baj, PhD (University of Trieste) for kind assistance in confocal imaging and Oona Hällfors (University of Turku) for technical assistance with microbiological studies. This study was also supported by the Friuli Venezia Giulia Region (LR 26/2005, art. 23: “R3A2 network”).

References

  1. 1.
    Vallittu PK. Flexural properties of acrylic resin polymers reinforced with unidirectional and woven glass fibers. J Prosthet Dent. 1999;81:318–26.CrossRefGoogle Scholar
  2. 2.
    Vallittu PK, Sevelius C. Resin-bonded, glass fiber-reinforced composite fixed partial dentures: a clinical study. J Prosthet Dent. 2000;84:413–8.CrossRefGoogle Scholar
  3. 3.
    Tuusa S, Peltola M, Tirri T, Lassila L, Vallittu PK. A review of two animal studies dealing with biological responses to glass-fibre-reinforced composite implants in critical size calvarial bone defects in rabbits. Key Eng Mat. 2007;361–363(20):471–4.Google Scholar
  4. 4.
    Tuusa SM, Peltola MJ, Tirri T, Puska MA, Röyttä M, Aho H, Sandholm J, Lassila LV, Vallittu PK. Reconstruction of critical size calvarial bone defects in rabbits with glass-fiber-reinforced composite with bioactive glass granule coating. J Biomed Mater Res B. 2008;84B:510–9.CrossRefGoogle Scholar
  5. 5.
    Aitasalo K, Rekola J, Piitulainen J, Vallittu PK. Craniofacial bone reconstruction with a novel bioactive composite implant. J Neurol Surg B. 2012;73:A099.CrossRefGoogle Scholar
  6. 6.
    Peltola MJ, Vallittu PK, Vuorinen V, Aho AAJ, Puntala A, Aitasalo KMJ. Novel composite implant in craniofacial bone reconstruction. Eur Arch Otorhinolaryngol. 2012;269:623–8.CrossRefGoogle Scholar
  7. 7.
    Nganga S, Zhang D, Moritz N, Vallittu PK, Hupa L. Multi-layer porous fiber-reinforced composites for implants: in vitro calcium phosphate formation in the presence of bioactive glass. Dent Mater. 2012;28:1134–45.CrossRefGoogle Scholar
  8. 8.
    Nganga S, Ylä-Soininmäki A, Lassila LVJ, Vallittu PK. Interface shear strength and fracture behaviour of porous glass-fibre-reinforced composite implant and bone model material. J Mech Behav Biomed Mater. 2011;4:1797–804.CrossRefGoogle Scholar
  9. 9.
    Schierholz JM, Beuth J. Implant infections: a haven for opportunistic bacteria. J Hosp Infect. 2001;49:87–93.CrossRefGoogle Scholar
  10. 10.
    Hardes J, Ahrens H, Gebert C, Streitbuerger A, Buerger H, Erren M, Gunsel A, Wedemeyer C, Saxler G, Winkelmann W, Gosheger G. Lack of toxicological side-effects in silver-coated megaprostheses in humans. Biomaterials. 2007;28:2869–75.CrossRefGoogle Scholar
  11. 11.
    Jaberi J, Gambrell K, Tiwana P, Madden C, Finn R. Long-term clinical outcome analysis of poly-methyl-methacrylate cranioplasty for large skull defects. J Oral Maxillofac Surg. 2013;71:e81–8.CrossRefGoogle Scholar
  12. 12.
    Chiang HY, Steelman VM, Pottinger JM, Schlueter AJ, Diekema DJ, Greenlee JD, Howard MA 3rd, Herwaldt LA. Clinical significance of positive cranial bone flap cultures and associated risk of surgical site infection after craniotomies or craniectomies. J Neurosurg. 2011;114(6):1746–54.CrossRefGoogle Scholar
  13. 13.
    Travan A, Marsich E, Donati I, Benincasa M, Giazzon M, Felisari L, Paoletti S. Silver–polysaccharide nanocomposite antimicrobial coatings for methacrylic thermosets. Acta Biomater. 2011;7:337–46.CrossRefGoogle Scholar
  14. 14.
    Moseke C, Gbureck U, Elter P, Drechsler P, Zoll A, Thull R, Ewald A. Hard implant coatings with antimicrobial properties. J Mater Sci Mater Med. 2011;22:2711–20.CrossRefGoogle Scholar
  15. 15.
    De La Brutel RA, Dossche KM, Birnbaum DE, Hacker R. First clinical experience with a mechanical valve with silver coating. J Heart Valve Dis. 2000;9:123–9.Google Scholar
  16. 16.
    Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ. The bactericidal effect of silver nanoparticles. Nanotechnology. 2005;16:2346–53.CrossRefGoogle Scholar
  17. 17.
    Karchmer TB, Giannetta ET, Muto CA, Strain BA, Farr BM. A randomized crossover study of silver-coated urinary catheters in hospitalized patients. Arch Intern Med. 2000;160:3294–8.CrossRefGoogle Scholar
  18. 18.
    Lajcak M, Heidecke V, Haude KH, Rainov NG. Infection rates of external ventricular drains are reduced by the use of silver-impregnated catheters. Acta Neurochir (Wien). 2013;155:875–81.CrossRefGoogle Scholar
  19. 19.
    Pupka A, Skora J, Janczak D, Plonek T, Marczak J, Szydełko T. In situ revascularisation with silver-coated polyester prostheses and arterial homografts in patients with aortic graft infection: a prospective, comparative, single-centre study. Eur J Vasc Endovasc Surg. 2011;41:61–7.CrossRefGoogle Scholar
  20. 20.
    Chen X, Schluesener HJ. Nanosilver: a nanoproduct in medical application. Toxicol Lett. 2008;176:1–12.CrossRefGoogle Scholar
  21. 21.
    Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro. 2005;19:975–83.CrossRefGoogle Scholar
  22. 22.
    Travan A, Donati I, Marsich E, Bellomo F, Achanta S, Toppazzini M, Semeraro S, Scarpa T, Spreafico V, Paoletti S. Surface modification and polysaccharide deposition on BisGMA/TEGDMA thermoset. Biomacromolecules. 2010;11:583–92.CrossRefGoogle Scholar
  23. 23.
    Travan A, Marsich E, Donati I, Foulc MP, Moritz N, Aro HT, Paoletti S. Polysaccharide-coated thermosets for orthopedic applications: from material characterization to in vivo tests. Biomacromolecules. 2012;13:1564–72.CrossRefGoogle Scholar
  24. 24.
    Travan A, Pelillo C, Donati I, Marsich E, Benincasa M, Scarpa T, Semeraro S, Turco G, Gennaro R, Paoletti S. Non-cytotoxic silver nanoparticle-polysaccharide nanocomposites with antimicrobial activity. Biomacromolecules. 2009;10:1429–35.CrossRefGoogle Scholar
  25. 25.
    Marsich E, Travan A, Donati I, Turco G, Kulkova J, Moritz N, Aro HT, Crosera M, Paoletti S. Biological responses of silver-coated thermosets: an in vitro and in vivo study. Acta Biomater. 2013;9:5088–99.CrossRefGoogle Scholar
  26. 26.
    Donati I, Feresini M, Travan A, Marsich E, Lapasin R, Paoletti S. Polysaccharide-based polyanion-polycation-polyanion ternary systems. A preliminary analysis of interpolyelectrolyte interactions in dilute solutions. Biomacromolecules. 2011;12:4044–56.CrossRefGoogle Scholar
  27. 27.
    Tanner J, Vallittu PK, Söderling E. Adherence of Streptococcus mutans to an E-glass fiber-reinforced composite and conventional restorative materials used in prosthetic dentistry. J Biomed Mater Res. 2000;49:250–6.CrossRefGoogle Scholar
  28. 28.
    Life Technologies Corporation. Invitrogen—Protocol for film tracerTM FM® 1-43 green biofilm cell stain. 2009. http://tools.invitrogen.com/content/sfs/manuals/mp10317.pdf. Accessed 23 April 2013.
  29. 29.
    Houot L, Watnick PI. A Novel role for enzyme I of the vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. J Bacteriol. 2008;190:311–20.CrossRefGoogle Scholar
  30. 30.
    Bos R, van der Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microb Rev. 1999;23:179–230.Google Scholar
  31. 31.
    Barton AJ, Sagers RD, Pitt WG. Bacterial adhesion to orthopedic implant polymers. J Biomed Mater Res. 1996;30:403–10.CrossRefGoogle Scholar
  32. 32.
    Jee WS. Integrated bone tissue physiology: anatomy and physiology. In: Cowin SC, editor. Bone mechanics handbook. Boca Raton: CRC Press; 2001. p. 1–33.Google Scholar
  33. 33.
    Dunne WM. Bacterial adhesion: Seen any good biofilms lately? Clin Microbiol Rev. 2002;15:155–66.CrossRefGoogle Scholar
  34. 34.
    Busscher HJ, Rinastiti M, Siswomihardjo W, van der Mei HC. Biofilm formation on dental restorative and implant materials. J Dent Res. 2010;89:657–65.CrossRefGoogle Scholar
  35. 35.
    Tanner J, Vallittu PK, Söderling E. Effect of water storage of E-glass fiber-reinforced composite on adhesion of Streptococcus mutans. Biomaterials. 2001;22:1613–8.CrossRefGoogle Scholar
  36. 36.
    Nganga S, Travan A, Donati I, Crosera M, Paoletti S, Vallittu PK. Degradation of silver–polysaccharide nanocomposite in solution and as coating on fiber reinforced composites by lysozyme and hydrogen peroxide. Biomacromolecules. 2012;13:2605–8.CrossRefGoogle Scholar
  37. 37.
    Stebounova L, Guio E, Grassian V. Silver nanoparticles in simulated biological media: a study of aggregation, sedimentation, and dissolution. J Nanopart Res. 2011;13:233–44.CrossRefGoogle Scholar
  38. 38.
    Stevens KN, Crespo-Biel O, van den Bosch EE, Dias AA, Knetsch ML, Aldenhoff YB, van der Veen FH, Maessen JG, Stobberingh EE, Koole LH. The relationship between the antimicrobial effect of catheter coatings containing silver nanoparticles and the coagulation of contacting blood. Biomaterials. 2009;30:3682–90.CrossRefGoogle Scholar
  39. 39.
    Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.CrossRefGoogle Scholar
  40. 40.
    Benson DE, Burns GL, Mohammad SF. Effects of plasma on adhesion of biofilm forming pseudomonas aeruginosa and staphylococcus epidermidis to fibrin substrate. Trans Am Soc Artif Intern Org. 1996;42:M655–60.CrossRefGoogle Scholar
  41. 41.
    Li D, Zhu M, Xu C, Chen J, Ji B. The effect of Cu2+ or Fe3+ on the noncovalent binding of rutin with bovine serum albumin by spectroscopic analysis. Spectrochim Acta A Mol Biomol Spectrosc. 2011;78(1):74–9.CrossRefGoogle Scholar
  42. 42.
    Lawson M, Hoth K, DeForest C, Bowman C, Anseth K. Inhibition of staphylococcus epidermidis biofilms using polymerizable vancomycin derivatives. Clin Orthop Relat Res. 2010;468:2081–91.CrossRefGoogle Scholar
  43. 43.
    Malaisrie SC, Malekzadeh S, Biedlingmaier JF. In vivo analysis of bacterial biofilm formation on facial plastic bioimplants. Laryngoscope. 1998;108:1733–8.CrossRefGoogle Scholar
  44. 44.
    Donati I, Haug IJ, Scarpa T, Borgogna M, Draget KI, Skjåk- Bræk G, Paoletti S. Synergistic effects in semidilute mixed solutions of alginate and lactose-modified chitosan (chitlac). Biomacromolecules. 2007;8:957–62.CrossRefGoogle Scholar
  45. 45.
    Grunlan JC, Choi JK, Lin A. Antimicrobial behavior of polyelectrolyte multilayer films containing cetrimide and silver. Biomacromolecules. 2005;6:1149–53.CrossRefGoogle Scholar
  46. 46.
    Väkiparta M, Koskinen MK, Vallittu P, Närhi T, Yli-Urpo A. In vitro cytotoxicity of E-glass fiber weave preimpregnated with novel biopolymer. J Mater Sci Mater Med. 2004;15:69–72.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sara Nganga
    • 1
    • 2
    Email author
  • Andrea Travan
    • 3
  • Eleonora Marsich
    • 4
  • Ivan Donati
    • 3
  • Eva Söderling
    • 1
    • 2
  • Niko Moritz
    • 1
    • 2
  • Sergio Paoletti
    • 3
  • Pekka K. Vallittu
    • 1
    • 2
  1. 1.Department of Prosthetic Dentistry and Biomaterials Science, Institute of DentistryUniversity of TurkuTurkuFinland
  2. 2.Biocity Turku Biomaterials Research ProgramTurku Clinical Biomaterial Centre (TCBC)TurkuFinland
  3. 3.Department of Life SciencesUniversity of TriesteTriesteItaly
  4. 4.Medicine, Surgery and Health Sciences DepartmentUniversity of TriesteTriesteItaly

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