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Experimental mucositis/gingivitis in persons aged 70 or over: microbiological findings and prediction of clinical outcome

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Abstract

Objectives

To assess in persons aged 70 years or older the microbiological alterations occurring around implants and natural teeth during and after 3 weeks of undisturbed plaque accumulation. Furthermore, to test the predictive value of several markers at baseline for the extent of inflammation around implants and teeth after this period.

Materials and methods

Twenty partially edentulous participants with titanium implants refrained from oral hygiene practices while being clinically monitored in weekly intervals for 21 days. Teeth and implants were then cleaned, oral hygiene resumed, and the participants were further monitored. Levels of six subgingival plaque microorganisms, the plaque index (PI), and the gingival index (GI) were assessed before (baseline), during (days 0, 7, 14, 21), and after plaque accumulation (days 28, 42). Six microorganisms; demographic and clinical variables at day 0 were further evaluated as potential predictors for presence of GI > 1 at days 21 and 28.

Results

The detection frequency of the selected bacteria did not differ between implants and teeth at any time point. Bacteria counts decreased in the preparatory phase and increased in the plaque accumulation phase. Patterns observed at implants and teeth were similar. Only Parvimonas micra at day 21 reached significantly higher counts at implants than teeth. For the prediction of clinical outcome at day 21, in the multivariable model, only implant vs. tooth was significant indicator for the primary outcome (p = 0.01).

Conclusions

Overall, the analysis of subgingival/submucosal samples revealed only minor differences between implants and teeth during the development and resolution of inflammation.

Clinical relevance

Within the limitations of our study, with plaque accumulation, elders develop more inflammation around implants than around teeth, in spite of similar bacterial profiles.

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References

  1. Löe H, Theilade E, Jensen SB (1965) Experimental gingivitis in man. J Periodontol 36:177–187

    Article  Google Scholar 

  2. Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP (1994) Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res 5:254–259

    Article  Google Scholar 

  3. Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B (1992) Soft tissue reaction to de novo plaque formation on implants and teeth. Clin Oral Implants Res 3:1–8

    Article  Google Scholar 

  4. Zitzmann NU, Berglundh T, Marinello CP, Lindhe J (2001) Experimental peri-implant mucositis in man. J Clin Periodontol 28(6):517–523

    Article  Google Scholar 

  5. Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP, Ramseier CA (2012) Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res 23(2):182–190. https://doi.org/10.1111/j.1600-0501.2011.02220.x

    Article  PubMed  Google Scholar 

  6. Ramseier CA, Eick S, Bronnimann C, Buser D, Bragger U, Salvi GE (2015) Host-derived biomarkers at teeth and implants in partially edentulous patients. A 10-year retrospective study. Clin Oral Implants Res. https://doi.org/10.1111/clr.12566

  7. Nogueira-Filho G, Pesun I, Isaak-Ploegman C, Wijegunasinghe M, Wierzbicki T, McCulloch CA (2014) Longitudinal comparison of cytokines in peri-implant fluid and gingival crevicular fluid in healthy mouths. J Periodontol 85(11):1582–1588. https://doi.org/10.1902/jop.2014.130642

    Article  PubMed  Google Scholar 

  8. Ramseier CA, Eick S, Bronnimann C, Buser D, Bragger U, Salvi GE (2016) Host-derived biomarkers at teeth and implants in partially edentulous patients. A 10-year retrospective study. Clin Oral Implants Res 27(2):211–217. https://doi.org/10.1111/clr.12566

    Article  PubMed  Google Scholar 

  9. Theilade E (1996) The experimental gingivitis studies: the microbiological perspective. J Dent Res 75(7):1434–1438

    Article  Google Scholar 

  10. Loesche WJ, Syed SA (1978) Bacteriology of human experimental gingivitis; effect of plaque and gingivitis score. Infect Immun 21:830–839

    PubMed  PubMed Central  Google Scholar 

  11. Holm-Pedersen P, Agerbaek N, Theilade E (1975) Experimental gingivitis in young and elderly individuals. J Clin Periodontol 2:14–24

    Article  Google Scholar 

  12. Fransson C, Berglundh T, Lindhe J (1996) The effect of age on the development of gingivitis. J Clin Periodontol 23:379–385

    Article  Google Scholar 

  13. Zavala WD, Cavicchia JC (2006) Deterioration of the Langerhans cell network of the human gingival epithelium with aging. Arch Oral Biol 51(12):1150–1155

    Article  Google Scholar 

  14. Hajishengallis G (2014) Aging and its impact on innate immunity and inflammation: implications for periodontitis. J Oral Biosci 56(1):30–37. https://doi.org/10.1016/j.job.2013.09.001

    Article  PubMed  PubMed Central  Google Scholar 

  15. Preshaw PM, Henne K, Taylor JJ, Valentine RA, Conrads G (2017) Age-related changes in immune function (immune senescence) in caries and periodontal diseases: a systematic review. J Clin Periodontol 44(Suppl 18):S153–S177. https://doi.org/10.1111/jcpe.12675

    Article  PubMed  Google Scholar 

  16. Srinivasan M, Meyer S, Mombelli A, Muller F (2017) Dental implants in the elderly population: a systematic review and meta-analysis. Clin Oral Implants Res 28(8):920–930. https://doi.org/10.1111/clr.12898

    Article  PubMed  Google Scholar 

  17. Kay EJ, Locker D (1996) Is dental health education effective? A systematic review of current evidence. Community Dent Oral Epidemiol 24(4):231–235

    Article  Google Scholar 

  18. MacEntee MI (2005) Caring for elderly long-term care patients: oral health-related concerns and issues. Dent Clin N Am 49(2):429–443

    Article  Google Scholar 

  19. Meyer S, Giannopoulou C, Courvoisier D, Schimmel M, Muller F, Mombelli A (2017) Experimental mucositis and experimental gingivitis in persons aged 70 or over. Clinical and biological responses. Clin Oral Implants Res 28(8):1005–1012. https://doi.org/10.1111/clr.12912

    Article  PubMed  Google Scholar 

  20. Loe H, Silness J (1963) Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533–551

    Article  Google Scholar 

  21. Silness J, Loe H (1964) Periodontal disease in pregnancy. II. Correlation between Oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135

    Article  Google Scholar 

  22. Kozarov E, Sweier D, Shelburne C, Progulske-Fox A, Lopatin D (2006) Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect 8(3):687–693. https://doi.org/10.1016/j.micinf.2005.09.004

    Article  PubMed  Google Scholar 

  23. Shelburne CE, Prabhu A, Gleason RM, Mullally BH, Coulter WA (2000) Quantitation of Bacteroides forsythus in subgingival plaque comparison of immunoassay and quantitative polymerase chain reaction. J Microbiol Methods 39(2):97–107

    Article  Google Scholar 

  24. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144

    Article  Google Scholar 

  25. Haubek D, Ennibi OK, Poulsen K, Vaeth M, Poulsen S, Kilian M (2008) Risk of aggressive periodontitis in adolescent carriers of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans in Morocco: a prospective longitudinal cohort study. Lancet 371(9608):237–242

    Article  Google Scholar 

  26. Quirynen M, Vogels R, Pauwels M, Haffajee AD, Socransky SS, Uzel NG, van Steenberghe D (2005) Initial subgingival colonization of ‘pristine’ pockets. J Dent Res 84(4):340–344. https://doi.org/10.1177/154405910508400409

    Article  PubMed  Google Scholar 

  27. Botero JE, Gonzalez AM, Mercado RA, Olave G, Contreras A (2005) Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol 76(9):1490–1495. https://doi.org/10.1902/jop.2005.76.9.1490

    Article  PubMed  Google Scholar 

  28. Salvi GE, Furst MM, Lang NP, Persson GR (2008) One-year bacterial colonization patterns of Staphylococcus aureus and other bacteria at implants and adjacent teeth. Clin Oral Implants Res 19(3):242–248. https://doi.org/10.1111/j.1600-0501.2007.01470.x

    Article  PubMed  Google Scholar 

  29. Mombelli A, Van Oosten MAC, Schürch E, Lang NP (1987) The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2:145–151

    Article  Google Scholar 

  30. Mombelli A, Décaillet F (2011) The characteristics of biofilms in peri-implant disease. J Clin Periodontol 38(Suppl 11):203–213. https://doi.org/10.1111/j.1600-051X.2010.01666.x

    Article  PubMed  Google Scholar 

  31. Dierens M, Vandeweghe S, Kisch J, Persson GR, Cosyn J, De Bruyn H (2013) Long-term follow-up of turned single implants placed in periodontally healthy patients after 16 to 22 years: microbiologic outcome. J Periodontol 84(7):880–894. https://doi.org/10.1902/jop.2012.120187

    Article  PubMed  Google Scholar 

  32. Salvi GE, Cosgarea R, Sculean A (2016) Prevalence and mechanisms of peri-implant diseases. J Dent Res 96:31–37. https://doi.org/10.1177/0022034516667484

    Article  PubMed  Google Scholar 

  33. Koldsland OC, Scheie AA, Aass AM (2010) Prevalence of peri-implantitis related to severity of the disease with different degrees of bone loss. J Periodontol 81(2):231–238. https://doi.org/10.1902/jop.2009.090269

    Article  PubMed  Google Scholar 

  34. Derks J, Tomasi C (2015) Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol 42(Suppl 16):S158–S171. https://doi.org/10.1111/jcpe.12334

    Article  PubMed  Google Scholar 

  35. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M (2008) Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res 19(10):975–982. https://doi.org/10.1111/j.1600-0501.2008.01566.x

    Article  PubMed  Google Scholar 

  36. Maximo MB, de Mendonca AC, Renata Santos V, Figueiredo LC, Feres M, Duarte PM (2009) Short-term clinical and microbiological evaluations of peri-implant diseases before and after mechanical anti-infective therapies. Clin Oral Implants Res 20(1):99–108. https://doi.org/10.1111/j.1600-0501.2008.01618.x

    Article  PubMed  Google Scholar 

  37. Wade WG (2013) Detection and culture of novel oral bacteria. In: Jakubovics NS, Palmer RJ Jr (eds) Oral microbiology ecology - current research and new perspectives. Caister Academic press, Norfolk

    Google Scholar 

  38. Arweiler NB, Netuschil L (2016) The oral microbiota. Adv Exp Med Biol 902:45–60. https://doi.org/10.1007/978-3-319-31248-4_4

    Article  PubMed  Google Scholar 

  39. Marsh PD (2015) Dental biofilms. In: Lang NP, Lindhe J (eds) Clinical periodontology and implant dentistry. Wiley, Chichester

    Google Scholar 

  40. Charalampakis G, Belibasakis GN (2015) Microbiome of peri-implant infections: lessons from conventional, molecular and metagenomic analyses. Virulence 6(3):183–187. https://doi.org/10.4161/21505594.2014.980661

    Article  PubMed  PubMed Central  Google Scholar 

  41. Dabdoub SM, Tsigarida AA, Kumar PS (2013) Patient-specific analysis of periodontal and peri-implant microbiomes. J Dent Res 92(12 Suppl):168S–175S. https://doi.org/10.1177/0022034513504950

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kumar PS, Mason MR, Brooker MR, O’Brien K (2012) Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol 39(5):425–433. https://doi.org/10.1111/j.1600-051X.2012.01856.x

    Article  PubMed  PubMed Central  Google Scholar 

  43. Heuer W, Kettenring A, Stumpp SN, Eberhard J, Gellermann E, Winkel A, Stiesch M (2012) Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig 16(3):843–850

    Article  Google Scholar 

  44. Esposito M, Hirsch J-M, Lekholm U, Thomsen P (1998) Biological factors contributing to failures of osseointegrated oral implants (I). Success criteria and epidemiology. Eur J Oral Sci 106:527–551

    Article  Google Scholar 

  45. Esposito M, Hirsch J-M, Lekholm U, Thomsen P (1998) Biological factors contributing to failures of osseointegrated oral implants (II). Etiopathogenesis. Eur J Oral Sci 106:721–764

    Article  Google Scholar 

  46. Syftestad GT, Urist MR (1982) Bone aging. Clin Orthop Relat Res (162):288–297

  47. Tsigarida AA, Dabdoub SM, Nagaraja HN, Kumar PS (2015) The influence of smoking on the peri-implant microbiome. J Dent Res 94(9):1202–1217. https://doi.org/10.1177/0022034515590581

    Article  PubMed  PubMed Central  Google Scholar 

  48. Andjelkovic M, Sojic LT, Lemic AM, Nikolic N, Kannosh IY, Milasin J (2017) Does the prevalence of periodontal pathogens change in elderly edentulous patients after complete denture treatment? J Prosthodont 26(5):364–369. https://doi.org/10.1111/jopr.12402

    Article  PubMed  Google Scholar 

  49. Schimmel M (2018) Effect of advanced age, and/oir systemic medical condition on dental implant survival: a systematic review and meta-analysis. Clin Oral Implants Res. Accepted March 2018

  50. Stahringer SS, Clemente JC, Corley RP, Hewitt J, Knights D, Walters WA, Knight R, Krauter KS (2012) Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res 22(11):2146–2152. https://doi.org/10.1101/gr.140608.112

    Article  PubMed  PubMed Central  Google Scholar 

  51. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, Knights D, Gajer P, Ravel J, Fierer N, Gordon JI, Knight R (2011) Moving pictures of the human microbiome. Genome Biol 12(5):R50. https://doi.org/10.1186/gb-2011-12-5-r50

    Article  PubMed  PubMed Central  Google Scholar 

  52. David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, Erdman SE, Alm EJ (2014) Host lifestyle affects human microbiota on daily timescales. Genome Biol 15(7):R89. https://doi.org/10.1186/gb-2014-15-7-r89

    Article  PubMed  PubMed Central  Google Scholar 

  53. Holm-Pedersen P, Folke LEA, Gawronski TH (1980) Composition and metabolic activity of dental plaque from healthy young and elderly individuals. J Dent Res 59:771–776

    Article  Google Scholar 

  54. Fransson C, Mooney J, Kinane DF, Berglundh T (1999) Differences in the inflammatory response in young and old human subjects during the course of experimental gingivitis. J Clin Periodontol 26(7):453–460

    Article  Google Scholar 

  55. Feres M, Teles F, Teles R, Figueiredo LC, Faveri M (2016) The subgingival periodontal microbiota of the aging mouth. Periodontol 72(1):30–53. https://doi.org/10.1111/prd.12136

    Article  Google Scholar 

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Funding

This work was financed by research funds of the Division of Periodontology, School of Dental Medicine, University of Geneva, and supported in part by an unrestricted research grant from the Swiss Society of Periodontology.

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Authors and Affiliations

  1. Division of Periodontology, University Clinics of Dental Medicine, University of Geneva, 1 rue Michel-Servet, 1211, Geneva 4, Switzerland

    Simon Meyer, Catherine Giannopoulou, Jose Cancela & Andrea Mombelli

  2. Division of Rheumatology, University Hospitals of Geneva, Geneva, Switzerland

    Delphine Courvoisier

  3. Division of Gerodontology and Removable Prosthesis, University Clinics of Dental Medicine, Geneva, Switzerland

    Frauke Müller

Authors
  1. Simon Meyer
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  2. Catherine Giannopoulou
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  3. Jose Cancela
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  6. Andrea Mombelli
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Correspondence to Catherine Giannopoulou.

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This study was performed in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of the University Hospital of Geneva, Switzerland (CER: 13-241).

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Meyer, S., Giannopoulou, C., Cancela, J. et al. Experimental mucositis/gingivitis in persons aged 70 or over: microbiological findings and prediction of clinical outcome. Clin Oral Invest 23, 3855–3863 (2019). https://doi.org/10.1007/s00784-019-02815-1

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  • DOI: https://doi.org/10.1007/s00784-019-02815-1

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