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Effects of photodynamic laser and violet-blue led irradiation on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide attached to moderately rough titanium surface: in vitro study

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Abstract

Effective decontamination of biofilm and bacterial toxins from the surface of dental implants is a yet unresolved issue. This study investigates the in vitro efficacy of photodynamic treatment (PDT) with methylene blue (MB) photoactivated with λ 635 nm diode laser and of λ 405 nm violet-blue LED phototreatment for the reduction of bacterial biofilm and lipopolysaccharide (LPS) adherent to titanium surface mimicking the bone-implant interface. Staphylococcus aureus biofilm grown on titanium discs with a moderately rough surface was subjected to either PDT (0.1% MB and λ 635 nm diode laser) or λ 405 nm LED phototreatment for 1 and 5 min. Bactericidal effect was evaluated by vital staining and residual colony-forming unit count. Biofilm and titanium surface morphology were analyzed by scanning electron microscopy (SEM). In parallel experiments, discs coated with Escherichia coli LPS were treated as above before seeding with RAW 264.7 macrophages to quantify LPS-driven inflammatory cell activation by measuring the enhanced generation of nitric oxide (NO). Both PDT and LED phototreatment induced a statistically significant (p < 0.05 or higher) reduction of viable bacteria, up to −99 and −98% (5 min), respectively. Moreover, besides bactericidal effect, PDT and LED phototreatment also inhibited LPS bioactivity, assayed as nitrite formation, up to −42%, thereby blunting host inflammatory response. Non-invasive phototherapy emerges as an attractive alternative in the treatment of peri-implantitis to reduce bacteria and LPS adherent to titanium implant surface without causing damage of surface microstructure. Its efficacy in the clinical setting remains to be investigated.

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References

  1. Albrektsson T, Canullo L, Cochran D, De Bruyn H (2016) “Peri-implantitis”: a complication of a foreign body or a man-made “disease”. Facts and fiction. Clin Implant Dent Relat Res 18:840–849

    Article  PubMed  Google Scholar 

  2. Zitzmann NU, Berglundh T (2008) Definition and prevalence of peri-implant diseases. J Clin Periodontol 35:286–291

    Article  PubMed  Google Scholar 

  3. Tomasi C, Derks J (2012) Clinical research of peri-implant diseases: quality of reporting, case definitions and methods to study incidence, prevalence and risk factors of peri-implant diseases. J Clin Periodontol 12:207–223

    Article  Google Scholar 

  4. Renvert S, Quirynen M (2015) Risk indicators for peri-implantitis. A narrative review. Clin Oral Implant Res 11:15–44

    Article  Google Scholar 

  5. Bi Y, Seabold J, Kaar S, Ragab A, Goldberg V, Anderson J, Greenfield E (2001) Adherent endotoxin on orthopedic wear particles stimulates cytokine production and osteoclast differentiation. J Bone Miner Res 16:2082–2091

    Article  CAS  PubMed  Google Scholar 

  6. Wataha J, Hanes P, Lockwood P (2001) Effect of lipopolysaccharide contamination on the attachment of osteoblast-like cells to titanium and titanium alloy in vitro. J Oral Implantol 27:174–179

    Article  PubMed  Google Scholar 

  7. Morra M, Cassinelli C, Bollati D, Cascardo G, Bellanda M (2015) Adherent endotoxin on dental implant surfaces: a reappraisal. J Oral Implantol 41:10–16

    Article  PubMed  Google Scholar 

  8. Persson GR, Renvert S (2014) Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res 16:783–793

    Article  PubMed  Google Scholar 

  9. Harris LG, Richards RG (2004) Staphylococcus aureus adhesion to different treated titanium surfaces. J Mater Sci Mater Med 15:311–314

    Article  CAS  PubMed  Google Scholar 

  10. Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implant Res 17:68–81

    Article  Google Scholar 

  11. Al-Ahmad A, Wiedmann-Al-Ahmad M, Fackler A, Follo M, Hellwig E, Bächle M, Hannig C, Han JS, Wolkewitz M, Kohal R (2013) In vivo study of the initial bacterial adhesion on different implant materials. Arch Oral Biol 58:1139–1147

    Article  CAS  PubMed  Google Scholar 

  12. Ferreira Ribeiro C, Cogo-Müller K, Franco GC, Silva-Concílio LR, Sampaio Campos M, de Mello RS, Claro Neves AC (2016) Initial oral biofilm formation on titanium implants with different surface treatments: an in vivo study. Arch Oral Biol 69:33–39

    Article  PubMed  Google Scholar 

  13. Karring ES, Stavropoulos A, Ellegaard B, Karring T (2005) Treatment of peri-implantitis by the Vector system. Clin Oral Implant Res 16:288–293

    Article  Google Scholar 

  14. Renvert S, Lessem J, Dahlen G, Lindahl C, Svensson M (2006) Topical minocycline microspheres versus topical chlorhexidine gel as an adjunct to mechanical debridement of incipient peri-implant infections: a randomized clinical trial. J Clin Periodontol 33:362–369

    Article  CAS  PubMed  Google Scholar 

  15. Al-Hashedi AA, Laurenti M, Benhamou V, Tamimi F (2016) Decontamination of titanium implants using physical methods. Clin Oral Implant Res. doi:10.1111/clr.12914

    Google Scholar 

  16. Dortbudak O, Haas R, Bernhart T, Mailath-Pokorny G (2001) Lethal photosensitization for decontamination of implant surfaces in the treatment of peri-implantitis. Clin Oral Implant Res 12:104–108

    Article  CAS  Google Scholar 

  17. Chan Y, Lai CH (2003) Bactericidal effects of different laser wavelengths on periodontopathic germs in photodynamic therapy. Lasers Med Sci 18:51–55

    Article  PubMed  Google Scholar 

  18. Wainwright M (2005) The development of phenothiazinium photosensitisers. Photodiagnosis Photodyn Ther 2:263–272

    Article  CAS  PubMed  Google Scholar 

  19. Castano AP, Demidova TN, Hamblin MR (2004) Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization. Photodiagnosis Photodyn Ther 1:279–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Maclean M, MacGregor SJ, Anderson JG, Woolsey GA (2009) Inactivation of bacterial pathogens following exposure to light from a 405nm LED array. Appl Environ Microbiol 75:1932–1937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fontana CR, Song X, Polymeri A, Goodson JM, Wang X, Soukos NS (2015) The effect of blue light on periodontal biofilm growth in vitro. Lasers Med Sci 30:2077–2086

    Article  PubMed  Google Scholar 

  22. Soukos NS, Som S, Abernethy AD, Ruggiero K, Dunham J, Lee C, Doukas AG, Goodson JM (2005) Phototargeting oral black-pigmented bacteria. Antimicrob Agents Chemother 49:1391–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kurz J, Eberle F, Graumann T, Kaschel ME, Sähr A, Neumann F, Dalpke AH, Erdinger L (2011) Inactivation of LPS and RNase A on photocatalytically active surfaces. Chemosphere 84:1188–1193

    Article  CAS  PubMed  Google Scholar 

  24. Bornstein E (2004) Near-infrared dental diode lasers. Scientific and photobiologic principles and applications. Dent Today 23:102–108

    PubMed  Google Scholar 

  25. Harrison JJ, Stremick CA, Turner RJ, Allan ND, Olson ME, Ceri H (2010) Microtiter susceptibility testing of microbes growing on peg lids: a miniaturized biofilm model for high-throughput screening. Nat Protoc 5:1236–1254

    Article  CAS  PubMed  Google Scholar 

  26. Giannelli M, Bani D, Tani A, Pini A, Margheri M, Zecchi-Orlandini S, Tonelli P, Formigli L (2009) In vitro evaluation of the effects of low-intensity Nd:YAG laser irradiation on the inflammatory reaction elicited by bacterial lipopolysaccharide adherent to titanium dental implants. J Periodontol 80:977–984

    Article  CAS  PubMed  Google Scholar 

  27. Giannelli M, Pini A, Formigli L, Bani D (2011) Comparative in vitro study among the effects of different laser and LED irradiation protocols and conventional chlorhexidine treatment for deactivation of bacterial lipopolysaccharide adherent to titanium surface. Photomed Laser Surg 29:573–580

    Article  CAS  PubMed  Google Scholar 

  28. Giannelli M, Landini G, Materassi F, Chellini F, Antonelli A, Tani A, Zecchi-Orlandini S, Rossolini GM, Bani D (2016) The effects of diode laser on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide adherent to titanium oxide surface of dental implants. An in vitro study Lasers Med Sci. doi:10.1007/s10103-016-2025-5

    Google Scholar 

  29. Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142

    CAS  PubMed  Google Scholar 

  30. Masini E, Nistri S, Vannacci A, Bani Sacchi T, Novelli A, Bani D (2004) Relaxin inhibits the activation of human neutrophils: involvement of the nitric oxide pathway. Endocrinology 145:1106–1112

    Article  CAS  PubMed  Google Scholar 

  31. Leonhardt A, Bergström C, Lekholm U (2003) Microbiologic diagnostics at titanium implants. Clin Implant Dent Relat Res 5:226–232

    Article  PubMed  Google Scholar 

  32. Pereira CA, Romeiro RL, Costa ACBP, Machado AKS, Junqueira JC, Jorge AOC (2011) Susceptibility of Candida albicans, Staphylococcus aureus, and Streptococcus mutans biofilms to photodynamic inactivation: an in vitro study. Lasers Med Sci 26:341–348

    Article  PubMed  Google Scholar 

  33. Rosa LP, da Silva FC, Nader SA, Meira GA, Viana MS (2015) Antimicrobial photodynamic inactivation of Staphylococcus aureus biofilms in bone specimens using methylene blue, toluidine blue ortho and malachite green: an in vitro study. Arch Oral Biol 60:675–680

    Article  CAS  PubMed  Google Scholar 

  34. Mombelli A (2002) Microbiology and antimicrobial therapy of peri-implantitis. Periodontol 2000(28):177–189

    Article  Google Scholar 

  35. Usacheva MN, Teichert MC, Biel MA (2003) The interaction of lipopolysaccharides with phenothiazine dyes. Lasers Surg Med 33:311–319

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr. Peter Schüpbach, from Schüpbach Ltd. (Thalwil, Switzerland), for conducting the SEM investigation and Dr. Waldemar Hoffmann, Nobel Biocare Services AG (Kloten, Switzerland), for reviewing the manuscript. Moreover, Nobel Biocare Services AG (Kloten, Switzerland) is acknowledged for supporting this study (Grant 2014–1250) and for the generous gift of the titanium discs needed for the experiments.

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Authors and Affiliations

  1. Odontostomatologic Laser Therapy Center, Via dell’ Olivuzzo 162, 50143, Florence, Italy

    Marco Giannelli & Fabrizio Materassi

  2. Department of Medical Biotechnologies, Santa Maria alle Scotte University Hospital, University of Siena, Viale Bracci, Siena, Italy

    Giulia Landini, Alberto Antonelli & Gian Maria Rossolini

  3. Department of Experimental and Clinical Medicine—Section of Anatomy and Histology, Largo Brambilla 3, University of Florence, 50134, Florence, Italy

    Flaminia Chellini, Alessia Tani, Daniele Nosi, Sandra Zecchi-Orlandini & Daniele Bani

  4. Department of Experimental and Clinical Medicine, Section of Critical Care and Specialistic Medicine, University of Florence, Florence, Italy

    Alberto Antonelli & Gian Maria Rossolini

  5. Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Via San Damiano, 50134, Florence, Italy

    Gian Maria Rossolini

Authors
  1. Marco Giannelli
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  2. Giulia Landini
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  3. Fabrizio Materassi
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  4. Flaminia Chellini
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  8. Sandra Zecchi-Orlandini
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  9. Gian Maria Rossolini
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  10. Daniele Bani
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Correspondence to Marco Giannelli.

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The authors declare that they have no conflict of interest concerning the contents of this study and that Nobel Biocare Services AG did not influence in any way the analysis or interpretation of the experimental data.

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Giannelli, M., Landini, G., Materassi, F. et al. Effects of photodynamic laser and violet-blue led irradiation on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide attached to moderately rough titanium surface: in vitro study. Lasers Med Sci 32, 857–864 (2017). https://doi.org/10.1007/s10103-017-2185-y

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  • DOI: https://doi.org/10.1007/s10103-017-2185-y

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