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Antimicrobial photodynamic therapy minimizes the deleterious effect of nicotine in female rats with induced periodontitis

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Abstract

The aim of this study was to compare the use of antimicrobial photodynamic therapy (aPDT) as an adjunct to scaling and root planing (SRP) in the treatment of experimentally induced periodontitis in female rats that were systemically treated with or without nicotine. Female rats (n = 180) were divided into two groups: vehicle administration (Veh) and nicotine administration (Nic). Mini-pumps containing either vehicle or nicotine were implanted in the rats 30 days before the induction of experimental periodontitis (EP). EP was induced by placing a cotton ligature around the left mandibular first molar. After 7 days, the ligature was removed, and the rats were randomly divided into three treatment subgroups: SRP (only SRP), DL (SRP plus diode laser), and aPDT (SRP plus aPDT). The aPDT consisted of phenothiazine photosensitizer deposition followed by diode laser irradiation. Ten rats from each subgroup were euthanized at 7, 15, and 30 days after treatment. Alveolar bone loss (ABL) in the furcation region was evaluated using histological, histometric, and immunohistochemical analyses. The rats that were treated with nicotine showed more ABL compared to those treated with vehicle. In both the Veh and Nic groups, SRP plus aPDT treatment resulted in reduced ABL, smaller numbers of both TRAP- and RANKL-positive cells, and higher numbers of PCNA-positive cells compared to SRP treatment alone. aPDT was an effective adjunctive therapy for the treatment of periodontitis in female rats regardless of whether they received nicotine.

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References

  1. Johannsen A, Susin C, Gustafsson A (2014) Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 64:111–126

    Article  Google Scholar 

  2. Hebert R (2003) What’s new in nicotine & tobacco research? Nicotine Tob Res 5:427–433

    Article  PubMed  Google Scholar 

  3. Benowitz NL, Lessov-Schlaggar CN, Swan GE, Jacob P (2006) 3rd. Female sex and oral contraceptive use accelerate nicotine metabolism. Clin Pharmacol Ther 79:480–488

    Article  PubMed  CAS  Google Scholar 

  4. Johnstone E, Benowitz N, Cargill A et al (2006) Determinants of the rate of nicotine metabolism and effects on smoking behavior. Clin Pharmacol Ther 80:319–330

    Article  PubMed  CAS  Google Scholar 

  5. Higashi E, Fukami T, Itoh M et al (2007) Human CYP2A6 is induced by estrogen via estrogen receptor. Drug Metab Dispos 35:1935–1941

    Article  PubMed  CAS  Google Scholar 

  6. Nakajima M, Yamamoto T, Nunoya K et al (1996) Role of human cytochrome P4502A6 in C-oxidation of nicotine. Drug Metab Dispos 24:1212–1217

    PubMed  CAS  Google Scholar 

  7. Jensen J, Christiansen C, Rødbro P (1985) Cigarette smoking, serum estrogens, and bone loss during hormone-replacement therapy early after menopause. N Engl J Med 17(313):973–975

    Article  Google Scholar 

  8. Mueck AO, Seeger H (2005) Smoking, estradiol metabolism and hormone replacement therapy. Curr Med Chem Cardiovasc Hematol Agents 3:45–54

    Article  PubMed  CAS  Google Scholar 

  9. Ma L, Zwahlen RA, Zheng LW, Sham MH (2011) Influence of nicotine on the biological activity of rabbit osteoblasts. Clin Oral Implants Res 22:338–342

    Article  PubMed  Google Scholar 

  10. Kim SJ, Kim HJ, Lee SJ, Park YJ, Lee J, You HK (2006) Effects of nicotine on proliferation and osteoblast differentiation in human alveolar bone marrow-derived mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai) 38:874–882

    Article  Google Scholar 

  11. Henemyre CL, Scales DK, Hokett SD et al (2003) Nicotine stimulates osteoclast resorption in a porcine marrow cell model. J Periodontol 74:1440–1446

    Article  PubMed  CAS  Google Scholar 

  12. Tanaka H, Tanabe N, Shoji M et al (2006) Nicotine and lipopolysaccharide stimulate the formation of osteoclast-like cells by increasing macrophage colony-stimulating factor and prostaglandin E2 production by osteoblasts. Life Sci 78:1733–1740

    Article  PubMed  CAS  Google Scholar 

  13. Jimi E, Shuto T, Koga T (1995) Macrophage colony-stimulating factor and interleukin-1a maintain the survival of osteoclast-like cells. Endocrinology 136:808–811

    PubMed  CAS  Google Scholar 

  14. Lee SK, Chung JH, Choi SC et al (2013) Sodium hydrogen sulfide inhibits nicotine and lipopolysaccharide-induced osteoclastic differentiation and reversed osteoblastic differentiation in human periodontal ligament cells. J Cell Biochem 114:1183–1193

    Article  PubMed  CAS  Google Scholar 

  15. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D (2004) The molecular triad OPG/RANK/RANKL:Involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 15:457–475

    Article  PubMed  CAS  Google Scholar 

  16. Wu LZ, Duan DM, Liu YF, Ge X, Zhou ZF, Wang XJ (2013) Nicotine favors osteoclastogenesis in human periodontal ligament cells co-cultured with CD4(+) T cells by upregulating IL-1β. Int J Mol Med 31:938–942

    PubMed  CAS  Google Scholar 

  17. Lee HJ, Pi SH, Kim Y et al (2009) Effects of nicotine on antioxidant defense enzymes and RANKL expression in human periodontal ligament cells. J Periodontol 80:1281–1288

    Article  PubMed  CAS  Google Scholar 

  18. Sorkhdini P, Moslemi N, Jamshidi S, Jamali R, Amirzargar AA, Fekrazad R (2013) Effect of hydrosoluble chlorine-mediated antimicrobial photodynamic therapy on clinical parameters and cytokine profile in ligature-induced periodontitis in dogs. J Periodontol 84:793–800

    Article  PubMed  CAS  Google Scholar 

  19. Oda S, Nitta H, Setoguchi T, Izumi Y, Ishikawa I (2004) Current concepts and advances in manual and power-driven instrumentation. Periodontol 36:45–58

    Article  Google Scholar 

  20. Braham P, Herron C, Street C, Darveau R (2009) Antimicrobial photodynamic therapy may promote periodontal healing through multiple mechanisms. J Periodontol 80:1790–1798

    Article  PubMed  CAS  Google Scholar 

  21. Garcia VG, Fernandes LA, Macarini VC et al (2011) Treatment of experimental periodontal disease with antimicrobial photodynamic therapy in nicotine-modified rats. J Clin Periodontol 38:1106–1114

    Article  PubMed  CAS  Google Scholar 

  22. Garcia VG, Gualberto Júnior EC, Fernandes LA et al (2013) Adjunctive antimicrobial photodynamic treatment of experimentally induced periodontitis in rats with ovariectomy. J Periodontol 84:556–565

    Article  PubMed  CAS  Google Scholar 

  23. Yamano S, Berley JA, Kuo WP et al (2010) Effects of nicotine on gene expression and osseointegration in rats. Clin Oral Implants Res 21:1353–1359

    Article  PubMed  Google Scholar 

  24. Garcia VG, Longo M, Gualberto Júnior EC et al (2014) Effect of the concentration of phenothiazine photosensitizers in antimicrobial photodynamic therapy on bone loss and the immune inflammatory response of induced periodontitis in rats. J Periodontal Res 49:584–594

    Article  PubMed  CAS  Google Scholar 

  25. Ström JO, Theodorsson E, Theodorsson A (2008) Order of magnitude differences between methods for maintaining physiological 17beta-oestradiol concentrations in ovariectomized rats. Scand J Clin Lab Invest 68:814–822

    Article  PubMed  Google Scholar 

  26. Raval AP, Hirsch N, Dave KR, Yavagal DR, Bramlett H, Saul I (2011) Nicotine and strogen synergistically exacerbate cerebral ischemic injury. Neuroscience 181:216–225

    Article  PubMed  CAS  Google Scholar 

  27. Bosco AF, Bonfante S, de Almeida JM, Luize DS, Nagata MJ, Garcia VG (2007) A histologic and histometric assessment of the influence of nicotine on alveolar bone loss in rats. J Periodontol 78:527–532

    Article  PubMed  Google Scholar 

  28. Hapidin H, Othman F, Soelaiman IN, Shuid AN, Luke DA, Mohamed N (2007) Negative effects of nicotine on bone-resorbing cytokines and bone histomorphometric parameters in male rats. J Bone Miner Metab 25:93–98

    Article  PubMed  CAS  Google Scholar 

  29. Müller Campanile VS, Giannopoulou C, Campanile G, Cancela JA, Mombelli A (2015) Single or repeated antimicrobial photodynamic therapy as adjunct to ultrasonic debridement in residual periodontal pockets: clinical, microbiological, and local biological effects. Lasers Med Sci 30:27–34

    Article  PubMed  PubMed Central  Google Scholar 

  30. Tardivo JP, Del Giglio A, de Oliveira CS et al (2005) Methylene blue in photodynamic therapy: from basic mechanisms to clinical applications. Photodiagnosis Photododyn Ther 2:175–191

    Article  CAS  Google Scholar 

  31. Ochsner M (1997) Photophysical and photobiological processes in the photodynamic therapy of tumors. J Photochem Photobiol B 39:1–18

    Article  PubMed  CAS  Google Scholar 

  32. Kömerik N, Nakanishi H, MacRobert 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  PubMed Central  Google Scholar 

  33. Wainwright M (1998) Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42:13–28

    Article  PubMed  CAS  Google Scholar 

  34. 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 

  35. Komerik N, Wilson M, Poole S (2000) The effect of photodynamic action on two virulence factors of gram-negative bacteria. Photochem Photobiol 72:676–680

    Article  PubMed  CAS  Google Scholar 

  36. Asagiri M, Takayanagi H (2007) The molecular understanding of osteoclast differentiation. Bone 40:251–264

    Article  PubMed  CAS  Google Scholar 

  37. Cochran DL (2008) Inflammation and bone loss in periodontal disease. J Periodontol 79:1569–1576

    Article  PubMed  CAS  Google Scholar 

  38. Graves DT, Cochran D (2003) The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J Periodontol 74:391–401

    Article  PubMed  CAS  Google Scholar 

  39. Lerner UH (2006) Inflammation-induced bone remodeling in periodontal disease and the influence of postmenopausal osteoporosis. J Dent Res 85:596–607

    Article  PubMed  CAS  Google Scholar 

  40. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423:337–342

    Article  PubMed  CAS  Google Scholar 

  41. Séguier S, Souza SL, Sverzut AC et al (2010) Impact of photodynamic therapy on inflammatory cells during human chronic periodontitis. J Photochem Photobiol B 101:348–354

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the São Paulo Research Foundation (FAPESP), São Paulo, SP, Brazil (FAPESP processes no. 2011/00936-0 and no. 2010/15094-2). The authors are grateful to Prof. Dr. Guilherme de Paula Nogueira (Faculty of Veterinary Medicine, UNESP, Araçatuba, SP, Brazil) for his guidance in the use of radioimmunoassay. The authors report no conflicts of interest related to this study.

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Authors and Affiliations

  1. Group for the Research and Study of Laser in Dentistry, Department of Surgery and Integrated Clinic, Division of Periodontics, São Paulo State University (UNESP), Araçatuba, São Paulo, Brazil

    Erivan Clementino Gualberto Jr., Letícia Helena Theodoro, Mariellén Longo, Vivian Cristina Noronha Novaes, Maria José Hitomi Nagata & Valdir Gouveia Garcia

  2. Department of Basic Science, São Paulo State University (UNESP), Araçatuba, São Paulo, Brazil

    Edilson Ervolino

  3. Dental School of Barretos, University Center of the Educational Foundation of Barretos, Barretos, SP, Brazil

    Valdir Gouveia Garcia

  4. Faculdade de Odontologia de Araçatuba-UNESP, Rua José Bonifácio, 1193, 16015-050, Araçatuba, SP, Brazil

    Valdir Gouveia Garcia

Authors
  1. Erivan Clementino Gualberto Jr.
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  2. Letícia Helena Theodoro
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  3. Mariellén Longo
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  4. Vivian Cristina Noronha Novaes
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  5. Maria José Hitomi Nagata
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  6. Edilson Ervolino
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  7. Valdir Gouveia Garcia
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Corresponding author

Correspondence to Valdir Gouveia Garcia.

Ethics declarations

All protocols were approved by the Institutional Review Board of Araçatuba Dental School, São Paulo State University, Araçatuba, São Paulo, Brazil (no. 2010/005074).

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Gualberto, E.C., Theodoro, L.H., Longo, M. et al. Antimicrobial photodynamic therapy minimizes the deleterious effect of nicotine in female rats with induced periodontitis. Lasers Med Sci 31, 83–94 (2016). https://doi.org/10.1007/s10103-015-1820-8

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  • DOI: https://doi.org/10.1007/s10103-015-1820-8

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