Skip to main content

Advertisement

Log in

The effect of a single episode of antimicrobial photodynamic therapy in the treatment of experimental periodontitis. Microbiological profile and cytokine pattern in the dog mandible

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

The purpose of this study was to evaluate the effect of a single application of antimicrobial photodynamic therapy (aPDT) on microbiological profile and cytokine pattern in dogs. Periodontal disease was induced by placing 3.0 silk ligatures around the mandibular pre-molars bilaterally during 8 weeks. The dogs were randomly treated with aPDT using a dye/laser system, scaling and root planning (SRP), or with the association of treatments (SRP + aPDT). Plaque samples were collected at baseline, 1, 3, and 4 weeks, and the mean counts of 40 species were determined using DNA-DNA hybridization. Gingival biopsies were removed and the expression of tumor necrosis factor alpha (TNF-α), receptor activator of NF-kB ligand (RANKL), osteoprotegerin (OPG), matrix metalloproteinase (MMP-1), interleukin (IL) 6, IL-10 and total bacterial load by analysis of 16 S rRNA gene were evaluated through real-time PCR. The results shows that the levels of the majority of the species were reduced 1 week post-therapy for all treatments, however, an increase in counts of Prevotella intermedia (p = 0.00), Prevotella. nigrescens (p = 0.00) and Tannerella forsythia (p = 0.00) was observed for aPDT and SRP + aPDT. After 4 weeks, a regrowth of Porphyromonas gingivalis (p = 0.00) and Treponema denticola (p = 0.00), was observed for all treatments. Also, a strikingly reduction of counts on counts of Aggregatibacter actinomycetemcomitans was observed for the aPDT (p = 0.00). For the cytokine pattern, the results were similar for all treatments, and a reduction in the expression of cytokines and bacterial load was observed throughout the study. Our results suggest that SRP, aPDT in a single application, and SRP + aPDT affects different bacterial species and have similar effects on the expression of cytokines evaluated during the treatment of ligature-induced periodontitis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Page RC, Offenbacher S, Schroeder HE, Seymour GJ (2000) Kornman KS (1997) Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 14:216–248

    Article  Google Scholar 

  2. Tanner ACR, Socransky SS, Goodson JM (1984) Microbiota periodontal pockets losing crestal alveolar bone. J Periodontal Res 19:279–291

    Article  PubMed  CAS  Google Scholar 

  3. Petersilka GJ, Ehmke B (2000) Flemming TF (2002) Antimicrobial effects of mechanical debridement. Periodontol 28:56–71

    Article  Google Scholar 

  4. Umeda M, Takeuchi Y, Noguchi K, Huang Y, Koshy G, Ishikawa I (2004) Effects of non-surgical periodontal therapy on the microbiota. Periodontol 36:98–120

    Article  Google Scholar 

  5. Mousquès T, Listgarten M, Phillips R (1980) Effect of scaling and root planning on the composition of the human subgingival microbial flora. J Periodontal Res 15:144–151

    Article  PubMed  Google Scholar 

  6. Haffajee AD, Cugini MA, Dibart S, Smith C, Kent RL, Socransky SS (1997) The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol 24:324–334

    Article  PubMed  CAS  Google Scholar 

  7. Tunkel J, Heinecke A, Flemmig TF (2002) A systematic review of efficacy of machine-driven and manual subgingival debridement in the treatment of chronic periodontitis. J Clin Periodontol 29 Suppl 3:72–81; discussion 90–91

    Google Scholar 

  8. Greenstein G (2000) Nonsurgical periodontal therapy in 2000: a literature review. J Am Dent Assoc 131:1580–1592

    PubMed  CAS  Google Scholar 

  9. Greenstein G (1992) Periodontal response to mechanical non-surgical therapy: A review. J Periodontol 63:118–130

    PubMed  CAS  Google Scholar 

  10. Moore J, Wilson M, Kieser JB (1986) The distribution of bacterial lipopolysaccharide (endotoxin) in relation to periodontally involved root surfaces. J Clin Periodontol 13:748–751

    Article  PubMed  CAS  Google Scholar 

  11. Badersten A, Nilvéus R, Egelberg J (1987) 4-year observations of basic periodontal therapy. J Clin Periodontol 14:438–444

    Article  PubMed  CAS  Google Scholar 

  12. Ramfjord SP, Caffesse RG, Morrison EC et al (1987) 4 modalities of periodontal treatment compared over 5 years. J Clin Periodontol 14:445–452

    Article  PubMed  CAS  Google Scholar 

  13. Giannobile WV (2008) Host-response therapeutics for periodontal diseases. J Periodontol 79:1592–1600

    Article  PubMed  CAS  Google Scholar 

  14. Von Tappeiner HJA (1904) On the effect of photodynamic (fluorescent) substances on protozoa and enzymes (in German). Deutsch Arch Klin Med 39:427–487

    Google Scholar 

  15. Sharman WM, Allen CM, van Lier JE (1999) Photodynamic therapeutics: basic principles and clinical applications. Drug Discov Today 4:507–517

    Article  PubMed  CAS  Google Scholar 

  16. Dougherty TJ, Gomer CJ, Henderson BW et al (1998) Photodynamic therapy. J Natl Cancer Inst 90:889–905

    Article  PubMed  CAS  Google Scholar 

  17. Shibutani T, Murahashi Y, Tsukada E, Iwayama Y, Heersche JN (1997) Experimentally induced periodontitis in beagle dogs causes rapid increases in osteoclastic resorption of alveolar bone. J Periodontol 68:385–391

    PubMed  CAS  Google Scholar 

  18. Socransky SS, Smith C, Martin L, Paster BJ, Dewhirst FE, Levin AE (1994) “Checkerboard” DNA-DNA hybridization. Biotechniques 17:788–792

    PubMed  CAS  Google Scholar 

  19. Socransky SS, Haffajee AD, Smith C et al (2004) The use of checkerboard DNA–DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 19:352–362

    Article  PubMed  CAS  Google Scholar 

  20. Garlet GP, Martins W Jr, Ferreira BR, Milanezi CM, Silva JS (2003) Patterns of chemokines and chemokine receptors expression in different forms of human periodontal disease. J Periodontal Res 38:210–217

    Article  PubMed  CAS  Google Scholar 

  21. Menezes R, Garlet TP, Trombone AP et al (2008) The potential role of suppressors of cytokine signaling in the attenuation of inflammatory reaction and alveolar bone loss associated with apical periodontitis. J Endod 34:1480–1484

    Article  PubMed  Google Scholar 

  22. Trombone AP, Cardoso CR, Repeke CE et al (2009) Tumor necrosis factor-alpha -308 G/A single nucleotide polymorphism and red-complex periodontopathogens are independently associated with increased levels of tumor necrosis factor-alpha in diseased periodontal tissues. J Periodontal Res 44:598–608

    Article  PubMed  CAS  Google Scholar 

  23. Kömerik N, Nakanishi H, Mac Robert AJ, Henderson B, Speight P, Wilson M (2003) In vivo killing of Porphyromonas gingivalis by toluidine blue-mediated photosensitization in an animal model. Antimicrob Agents Chemother 47:932–940

    Article  PubMed  Google Scholar 

  24. Takamatsu N, Yano K, He T, Umeda M, Ishikawa I (1999) Effect of initial periodontal therapy on the frequency of detecting Bacteroides forsythus, Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans. J Periodontol 70:574–580

    Article  PubMed  CAS  Google Scholar 

  25. Renvert S, Wikstrom M, Dahlen G, Slots J, Egelberg J (1990) Effect of root debridement on the elimination of Actinobacillus actinomycetemcomitans and Bacteroides gingivalis from periodontal pockets. J Clin Periodontol 17:345–350

    Article  PubMed  CAS  Google Scholar 

  26. Faveri M, Figueiredo LC, Duarte PM, Mestnik MJ, Mayer MP, Feres M (2009) Microbiological profile of untreated subjects with localized aggressive periodontitis. J Clin Periodontol 36:739–749

    Article  PubMed  CAS  Google Scholar 

  27. Slots J, Genco RJ (1984) Black-pigmented Bacteroides species, Capnocytophaga species and Actinobacillus actinomycetemcomitans human periodontal disease virulence factors colonization survival tissue destruction. J Dent Res 63:412–421

    Article  PubMed  CAS  Google Scholar 

  28. Haffajee AD (2000) Socransky SS (1994) Microbial etiological agents of destructive periodontal diseases. Periodontol 5:78–111

    Article  Google Scholar 

  29. Graves D (2008) Cytokines that promote periodontal tissue destruction. J Periodontol 79(8 Suppl):1585–1591

    Article  PubMed  CAS  Google Scholar 

  30. Silva TA, Garlet GP, Fukada SY, Silva JS, Cunha FQ (2007) Chemokines in oral inflammatory diseases: apical periodontitis and periodontal disease. J Dent Res 86:306–319

    Article  PubMed  CAS  Google Scholar 

  31. Wilson M (2004) Lethal photosensitisation of oral bacteria and its potential application in the photodynamic therapy of oral infections. Photochem Photobiol Sci 3:412–418

    Article  PubMed  CAS  Google Scholar 

  32. de Oliveira RR, Schwartz-Filho HO, Novaes AB Jr, Taba M Jr (2007) Antimicrobial photodynamic therapy in the non-surgical treatment of aggressive periodontitis: a preliminary randomized controlled clinical study. J Periodontol 78:965–973

    Article  PubMed  Google Scholar 

  33. de Oliveira RR, Schwartz-Filho HO, Novaes AB et al (2009) Antimicrobial photodynamic therapy in the non-surgical treatment of aggressive periodontitis: cytokine profile in gingival crevicular fluid, preliminary results. J Periodontol 80:98–105

    Article  PubMed  Google Scholar 

  34. Wasserman B, Hirschfeld I (1998) The relationship of initial clinical parameters to the long-term response in 112 cases of periodontal disease. J Clin Periodontol 15:38–42

    Article  Google Scholar 

  35. Wilson M (1994) Bactericidal effect of laser light and its potential use in the treatment of plaque-related diseases. Int Dent J 44:181–189

    PubMed  CAS  Google Scholar 

  36. Sarkar S, Wilson M (1993) Lethal photosensitization of bacteria in subgingival plaque from patients with chronic periodontitis. J Periodont Res 28:204–210

    Article  PubMed  CAS  Google Scholar 

  37. Zanin IC, Goncalves RB, Junior AB, Hope CK, Pratten J (2005) Susceptibility of Streptococcus mutans biofilms to photodynamic therapy: an in vitro study. J Antimicrob Chemother 56:324–330

    Article  PubMed  CAS  Google Scholar 

  38. Bhatti M, MacRobert A, Meghji S, Henderson B, Wilson M (1997) Effect of dosimetric and physiological factors on the lethal photosensitization of Porphyromonas gingivalis in vitro. Photochem Photobiol 65:1026–1031

    Article  PubMed  CAS  Google Scholar 

  39. Chan Y, Lai CH (2003) Bactericidal effects of different laser wavelengths on periodontopathic germs in photodynamic therapy. Lasers Med Sci 18:51–56

    Article  PubMed  Google Scholar 

  40. Haas R, Dörtbudak O, Mensdorff-Pouilly N, Mailath G (1997) Elimination of bacteria on different implant surfaces through photosensitization and soft laser. An in vitro study. Clin Oral Implants Res 8:249–254

    Article  PubMed  CAS  Google Scholar 

  41. Usacheva M, Teichert MC, Biel MA (2001) Comparison of the methylene blue and toluidine blue photobactericidal efficacy against Gram-positive and Gram-negative microorganisms. Lasers Surg Med 29:165–173

    Article  PubMed  CAS  Google Scholar 

  42. Nussbaum E, Lilge L, Mazzulli T (2002) Effects of 630, 660, 810 and 905 nm laser irradiation delivering radiant exposure of 1–50 J/cm2 on three species of bacteria in vitro. J Clin Laser Med Surg 20:325–333

    Article  PubMed  Google Scholar 

  43. Haas R, Baron M, Dortbudak O, Watzek G (2000) Lethal photosensitization, autogenous bone, and e-PTFE membrane for the treatment of peri-implantitis: preliminary results. Int J Oral Maxillofac Implants 15:374–382

    PubMed  CAS  Google Scholar 

  44. Kömerik N, Curnow A, MacRobert AJ, Hopper C, Speight PM, Wilson M (2002) Fluorescence biodistribution and photosensitizing activity of toluidine blue O on rat buccal mucosa. Lasers Med Sci 17:86–92

    Article  PubMed  Google Scholar 

  45. Hayek RR, Araujo NS, Gioso MA et al (2005) Comparative study between the effects of photodynamic therapy and conventional therapy on microbial reduction in ligature-induced peri-implantitis in dogs. J Periodontol 76:1275–1281

    Article  PubMed  Google Scholar 

  46. Shibli JA, Martins MC, Theodoro LH, Lotufo RF, Garcia VG, Marcantonio E Jr (2003) Lethal photosensitization in microbiological treatment of ligature-induced periimplantitis: a preliminary study in dogs. J Oral Sci 45:17–23

    PubMed  Google Scholar 

  47. Qin YL, Luan XL, Bi LJ, Sheng Q, Zhou CN, Zhang ZG (2008) Comparison of toluidine blue-mediated photodynamic therapy and conventional scaling treatment for periodontitis in rats. J Periodontol Res 43:162–167

    Article  CAS  Google Scholar 

  48. Andersen R, Loebel N, Hammond D, Wilson M (2007) Treatment of periodontal disease by photodisinfection compared to scaling and root planing. J Clin Dent 18:34–38

    PubMed  Google Scholar 

  49. Sigusch BW, Pfitzner A, Albrecht V, Glockmann E (2005) Efficacy of photodynamic therapy on inflammatory signs and two selected periodontopathogenic species in a beagle dog model. J Periodontol 76:1100–1105

    Article  PubMed  CAS  Google Scholar 

  50. Fernandes LA, de Almeida JM, Theodoro LH et al (2009) Treatment of experimental periodontal disease by photodynamic therapy in immunosuppressed rats. J Clin Periodontol 36:219–228

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The diode laser, photosensitizer, and fiber optic applicator used in this study were donated by Helbo Photodynamic Systems, Grieskirchen, Austria. This study was in part supported by FAPESP (Grant # 2005/05600774-3 and 2005/60775-0). The authors report no conflicts of interest related to this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arthur Belém Novaes Jr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Oliveira, R.R., Novaes, A.B., Garlet, G.P. et al. The effect of a single episode of antimicrobial photodynamic therapy in the treatment of experimental periodontitis. Microbiological profile and cytokine pattern in the dog mandible. Lasers Med Sci 26, 359–367 (2011). https://doi.org/10.1007/s10103-010-0864-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-010-0864-z

Keywords

Navigation