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The effects of decontamination methods of dental implant surface on cytokine expression analysis in the reconstructive surgical treatment of peri-implantitis

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Abstract

The aim of this trial was to analyze the effect of implant surface decontamination procedures combined with reconstructive surgical treatment (RST) of peri-implantitis on gene expression levels of selected biomarkers in peri-implant crevicular fluid (PICF). Forty patients diagnosed with peri-implantitis were treated with RST + decontamination of the implant surface using sterile saline and ozone therapy (ozone group) or sterile saline alone (control group). The gene expression levels of interleukin (IL)-6, IL-8, IL-17, vascular endothelial growth factor (VEGF), sclerostin (SOST) and osteoprotegerin (OPG) were evaluated by qPCR analysis at baseline and 6-month follow-up. Changes in cytokine mRNA expression levels were analyzed and compared with clinical/radiographic parameters. Both decontamination methods lead to the downregulations of the selected gene expressions. Ozone group showed significantly higher clinical attachment level (CAL) and radiographic defect fill (DF) values at 6 months compared to the control group (p = 0.026 and p = 0.011). The downregulation of SOST levels was significantly associated with probing depth reduction and radiographic DF (p < 0.05). Implant surface decontamination procedures applied with the RST contribute to a notable reduction in immuno-inflammatory response. The additional use of ozone therapy could have favorable effects in anti-infective regimens of peri-implantitis therapy. SOST, which was found to have significant relationship with both clinical and radiographic outcomes, could be a valuable indicator for the progression of peri-implantitis and may aid the development of new therapeutic strategies for bone gain in the RST of peri-implantitis.

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References

  1. Lindhe J, Meyle J, Periodontology EW. Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol. 2008;35:282–5.

    Article  PubMed  Google Scholar 

  2. Berglundh T, Armitage G, Araujo MG, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;45:286–91.

    Article  Google Scholar 

  3. Tonetti M, Palmer R. Clinical research in implant dentistry: study design, reporting and outcome measurements: consensus report of Working Group 2 of the VIII European Workshop on Periodontology. J Clin Periodontol. 2012;39:73–80.

    Article  PubMed  Google Scholar 

  4. Rakic M, Galindo-Moreno P, Monje A, et al. How frequent does peri-implantitis occur? A systematic review and meta-analysis. Clin Oral Investig. 2018;22:1805–16.

    Article  PubMed  Google Scholar 

  5. Gosau M, Hahnel S, Schwarz F, Gerlach T, Reichert TE, Burgers R. Effect of six different peri-implantitis disinfection methods on in vivo human oral biofilm. Clin Oral Implants Res. 2010;21:866–72.

    PubMed  Google Scholar 

  6. Al-Hashedi AA, Laurenti M, Benhamou V, Tamimi F. Decontamination of titanium implants using physical methods. Clin Oral Implants Res. 2017;28:1013–21.

    Article  PubMed  Google Scholar 

  7. Patianna G, Valente NA, D'Addona A, Andreana S. In vitro evaluation of controlled-release 14% doxycycline gel for decontamination of machined and sandblasted acid-etched implants. J Periodontol. 2018;89:325–30.

    Article  PubMed  Google Scholar 

  8. Bernardi S, Bianchi S, Tomei AR, Continenza MA, Macchiarelli G. Microbiological and SEM-EDS evaluation of titanium surfaces exposed to periodontal gel: in vitro study. Materials. 2019;12:1448.

    Article  PubMed Central  Google Scholar 

  9. Roos-Jansåker AM, Persson GR, Lindahl C, Renvert S. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: a 5-year follow-up. J Clin Periodontol. 2014;41:1108–14.

    Article  PubMed  Google Scholar 

  10. Mahato N, Wu X, Wang L. Management of peri-implantitis: a systematic review, 2010–2015. Springerplus. 2016;5:105.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Renvert S, Roos-Jansåker AM, Persson GR. Surgical treatment of peri-implantitis lesions with or without the use of a bone substitute–a randomized clinical trial. J Clin Periodontol. 2018;45:1266–74.

    Article  PubMed  Google Scholar 

  12. Carcuac O, Derks J, Abrahamsson I, Wennström JL, Petzold M, Berglundh T. Surgical treatment of peri-implantitis: 3-year results from a randomized controlled clinical trial. J Clin Periodontol. 2017;44:1294–303.

    Article  PubMed  Google Scholar 

  13. Carcuac O, Derks J, Charalampakis G, Abrahamsson I, Wennström J, Berglundh T. Adjunctive systemic and local antimicrobial therapy in the surgical treatment of peri-implantitis: a randomized controlled clinical trial. J Dental Res. 2016;95:50–7.

    Article  Google Scholar 

  14. Wang HL, Garaicoa-Pazmino C, Collins A, Ong HS, Chudri R, Giannobile WV. Protein biomarkers and microbial profiles in peri-implantitis. Clin Oral Implants Res. 2016;27:1129–36.

    Article  PubMed  Google Scholar 

  15. Hauser-Gerspach I, Vadaszan J, Deronjic I, et al. Influence of gaseous ozone in peri-implantitis: bactericidal efficacy and cellular response. An in vitro study using titanium and zirconia. Clin Oral Investig. 2012;16:1049–59.

    Article  PubMed  Google Scholar 

  16. Alpan AL, Toker H, Ozer H. Ozone therapy enhances osseous healing in rats with diabetes with calvarial defects: a morphometric and immunohistochemical study. J Periodontol. 2016;87:982–9.

    Article  PubMed  Google Scholar 

  17. Li Z, Tighe RM, Feng F, Ledford JG, Hollingsworth JW. Genes of innate immunity and the biological response to inhaled ozone. J Biochem Mol Toxicol. 2013;27:3–16.

    Article  PubMed  Google Scholar 

  18. Toita R, Tsuru K, Ishikawa K. A superhydrophilic titanium implant functionalized by ozone gas modulates bone marrow cell and macrophage responses. J Mater Sci Mater Med. 2016;27:127.

    Article  PubMed  Google Scholar 

  19. Sanz M, Chapple IL. Clinical research on peri-implant diseases: consensus report of Working Group 4. J Clin Periodontol. 2012;39:202–6.

    Article  PubMed  Google Scholar 

  20. Petkovic-Curcin A, Zeljic K, Cikota-Aleksic B, Dakovic D, Tatic Z, Magic Z. Association of cytokine gene polymorphism with peri-implantitis risk. Int J Oral Maxillofac Implants. 2017;32:241–8.

    Article  Google Scholar 

  21. Zani SR, Moss K, Shibli JA, et al. Peri-implant crevicular fluid biomarkers as discriminants of peri-implant health and disease. J Clin Periodontol. 2016;43:825–32.

    Article  PubMed  Google Scholar 

  22. Melo RF, Lopes BM, Shibli JA, Marcantonio Junior E, Marcantonio RAC, Galli GMT. Interleukin-1β and interleukin-6 expression and gene polymorphisms in subjects with peri-implant disease. Clin Implant Dent Relat Res. 2012;14:905–14.

    Article  PubMed  Google Scholar 

  23. Casado PL, Canullo L, de Almeida FA, Granjeiro JM, Barboza EP, Duarte MEL. Interleukins 1β and 10 expressions in the periimplant crevicular fluid from patients with untreated periimplant disease. Implant Dent. 2013;22:143–50.

    Article  PubMed  Google Scholar 

  24. Ata-Ali J, Flichy-Fernández AJ, Alegre-Domingo T, Ata-Ali F, Palacio J, Peñarrocha-Diago M. Clinical, microbiological, and immunological aspects of healthy versus peri-implantitis tissue in full arch reconstruction patients: a prospective cross-sectional study. BMC Oral Health. 2015;15:43.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Severino VO, Beghini M, de Araújo MF, et al. Expression of IL-6, IL-10, IL-17 and IL-33 in the peri-implant crevicular fluid of patients with peri-implant mucositis and peri-implantitis. Arch Oral Biol. 2016;72:194–9.

    Article  PubMed  Google Scholar 

  26. Fonseca FJPO, Junior MM, Lourenço EJV, de Moraes TD, Figueredo CM. Cytokines expression in saliva and peri-implant crevicular fluid of patients with peri-implant disease. Clin Oral Implants Res. 2014;25:68–72.

    Article  Google Scholar 

  27. Renvert S, Widén C, Persson GR. Cytokine expression in peri-implant crevicular fluid in relation to bacterial presence. J Clin Periodontol. 2015;42:697–702.

    Article  PubMed  Google Scholar 

  28. Rakic M, Struillou X, Petkovic-Curcin A, et al. Estimation of bone loss biomarkers as a diagnostic tool for peri-implantitis. J Periodontol. 2014;85:1566–74.

    Article  PubMed  Google Scholar 

  29. Wohlfahrt JC, Aass AM, Granfeldt F, Lyngstadaas SP, Reseland JE. Sulcus fluid bone marker levels and the outcome of surgical treatment of peri-implantitis. J Clin Periodontol. 2014;41:424–31.

    Article  PubMed  Google Scholar 

  30. Renvert S, Widén C, Persson RG. Cytokine and microbial profiles in relation to the clinical outcome following treatment of peri-implantitis. Clin Oral Implants Res. 2017;28:1127–32.

    Article  PubMed  Google Scholar 

  31. Berglundh T, Armitage G, Araujo MG, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89:313–8.

    Article  Google Scholar 

  32. Schwarz F, Sahm N, Schwarz K, Becker J. Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. J Clin Periodontol. 2010;37:449–55.

    Article  PubMed  Google Scholar 

  33. Silness J, Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–35.

    Article  PubMed  Google Scholar 

  34. Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand. 1963;21:533–51.

    Article  PubMed  Google Scholar 

  35. Isler SC, Unsal B, Soysal F, Ozcan G, Peker E, Karaca IR. The effects of ozone therapy as an adjunct to the surgical treatment of peri-implantitis. J Periodontal Implant Sci. 2018;48:136–51.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101–8.

    Article  PubMed  Google Scholar 

  37. Renvert S, Polyzois I. Treatment of pathologic peri-implant pockets. Periodontol. 2000;2018(76):180–90.

    Google Scholar 

  38. Ramanauskaite A, Daugela P, Juodzbalys G. Treatment of peri-implantitis: meta-analysis of findings in a systematic literature review and novel protocol proposal. Quintessence Int. 2016;47:379–93.

    PubMed  Google Scholar 

  39. Fernandes MH, de Sousa GP. Bone cells dynamics during peri-implantitis: a theoretical analysis. Oral Maxillofac Res. 2016;7:e6.

    Google Scholar 

  40. Duarte PM, de Mendonça AC, Máximo MBB, Santos VR, Bastos MF, Nociti FH Jr. Effect of anti-infective mechanical therapy on clinical parameters and cytokine levels in human peri-implant diseases. J Periodontol. 2009;80:234–43.

    Article  PubMed  Google Scholar 

  41. Mardegan GP, Shibli JA, Roth LA, Faveri M, Giro G, Bastos MF. Transforming growth factor-β, interleukin-17, and IL-23 gene expression profiles associated with human peri-implantitis. Clin Oral Implants Res. 2017;28:10–5.

    Article  Google Scholar 

  42. Al Ghazal L, O’Sullivan J, Claffey N, Polyzois I. Comparison of two different techniques used for the maintenance of peri-implant soft tissue health: a pilot randomized clinical trial. Acta Odontol Scand. 2017;75:542–9.

    Article  PubMed  Google Scholar 

  43. Duarte PM, De Mendonça AC, Máximo MBB, Santos VR, Bastos MF, Nociti Júnior FH. Differential cytokine expressions affect the severity of peri-implant disease. Clin Oral Implants Res. 2009;20:514–20.

    Article  PubMed  Google Scholar 

  44. Qu G, von Schroeder HP. Role of osterix in endothelin-1-induced downregulation of vascular endothelial growth factor in osteoblastic cells. Bone. 2006;38:21–9.

    Article  PubMed  Google Scholar 

  45. Mierzwinska-Nastalska E, Lomzynski L, Jaworska-Zaremba M, Kostrzewa-Janicka J. Vascular endothelial growth factor in gingival crevicular fluid around dental implants. Eur J Med Res. 2010;15:88–91.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Hall J, Pehrson NG, Ekestubbe A, Jemt T, Friberg B. A controlled, cross-sectional exploratory study on markers for the plasminogen system and inflammation in crevicular fluid samples from healthy, mucositis and peri-implantitis sites. Eur J Oral Implantol. 2015;8:153–66.

    PubMed  Google Scholar 

  47. Severino VO, Napimoga MH, de Lima Pereira SA. Expression of IL-6, IL-10, IL-17 and IL-8 in the peri-implant crevicular fluid of patients with peri-implantitis. Arch Oral Biol. 2011;56:823–8.

    Article  PubMed  Google Scholar 

  48. Balli U, Aydogdu A, Dede FO, Turer CC, Guven B. Gingival crevicular fluid levels of sclerostin, osteoprotegerin, and receptor activator of nuclear factor-κB ligand in periodontitis. J Periodontol. 2015;86:1396–404.

    Article  PubMed  Google Scholar 

  49. Sebastian A, Loots GG. Transcriptional control of Sost in bone. Bone. 2017;96:76–84.

    Article  PubMed  Google Scholar 

  50. Kim JH, Kim AR, Choi YH, et al. Tumor necrosis factor-α antagonist diminishes osteocytic RANKL and sclerostin expression in diabetes rats with periodontitis. PLoS ONE. 2017;12:e0189702.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Liu M, Kurimoto P, Zhang J, et al. Sclerostin and DKK1 inhibition preserves and augments alveolar bone volume and architecture in rats with alveolar bone loss. J Dent Res. 2018;97:1031–8.

    Article  PubMed  Google Scholar 

  52. Ozdemir H, Toker H, Balcı H, Ozer H. Effect of ozone therapy on autogenous bone graft healing in calvarial defects: a histologic and histometric study in rats. J Periodontal Res. 2013;48:722–6.

    Article  PubMed  Google Scholar 

  53. Kazancioglu H, Kurklu E, Ezirganli S. Effects of ozone therapy on pain, swelling, and trismus following third molar surgery. Int J Oral Maxillofac Surg. 2014;43:644–8.

    Article  PubMed  Google Scholar 

  54. Stavroullakis A, Brito C, Chen HY, Bajenova E, Prakki A, Nogueira-Filho G. Dental implant surface treatments may modulate cytokine secretion in Porphyromonas gingivalis-stimulated human gingival fibroblasts: a comparative study. J Biomed Mater Res A. 2015;103:1131–40.

    Article  PubMed  Google Scholar 

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Funding

This study was financially supported by Gazi University Research Board, with project number 03/2017-03.

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Correspondence to Sila Cagri Isler.

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The authors declare that they have no conflicts of interest.

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The research protocol was approved by the Ethics Committee of the Faculty of Medicine, Gazi University, Ankara, Turkey, Ankara, Turkey in accordance with the ethical principles, including Declaration of Helsinki of 1975, as revised in 2013. (Protocol ID: 25901600-2858). The trial is registered at ClinicalTrials.gov NCT03018795.

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Isler, S.C., Soysal, F., Akca, G. et al. The effects of decontamination methods of dental implant surface on cytokine expression analysis in the reconstructive surgical treatment of peri-implantitis. Odontology 109, 103–113 (2021). https://doi.org/10.1007/s10266-020-00520-0

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  • DOI: https://doi.org/10.1007/s10266-020-00520-0

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