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Published in: Clinical Oral Investigations 2/2017

Open Access 01-03-2017 | Original Article

Bacterial colonization of the peri-implant sulcus in dentate patients: a prospective observational study

Authors: M. A. Stokman, A. J. van Winkelhoff, A. Vissink, F. K. L. Spijkervet, G. M. Raghoebar

Published in: Clinical Oral Investigations | Issue 2/2017

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Abstract

Objectives

The aim of the present study was to compare the composition of the periodontal microflora at baseline (T0) with the submucosal microflora at least 1 year after implant placement (T1) in periodontally healthy patients.

Material and methods

For all 169 consecutive patients that visited our clinic during 1 year, we determined their periodontal parameters, implant mucosal index, and presence of implant calculus. At T0, self-reported smoking status was recorded and subgingival and submucosal biofilm samples were obtained and analyzed for the presence and numbers of selected periodontal pathogens. All measurements were repeated at T1.

Results

One hundred twenty patients completed the study. Periodontal parameters were stable or had improved at T1. The total bacterial load was lower at implant sites (P < 0.05). The prevalence of Porphyromonas gingivalis was low at baseline, but at T1, detection rate and numbers were higher at implant sites compared to dentate sites. At T1, the frequency of detection of P. gingivalis (P = 0.01), Parvimonas micra (P = 0.018), and Fusobacterium nucleatum (P = 0.035) was higher in smoking patients (n = 23) than in non-smokers (n = 97).

Conclusions

Colonization of the submucosal peri-implant area is similar to the composition of subgingival microbiota. Smoking has a measurable effect on the colonization of implant-associated biofilms and may select for P. gingivalis, P. micra, and F. nucleatum.

Clinical relevance

The colonization of implants by well-known periodontal pathogens is very similar to that in normal dentition, also in a healthy cohort. Smoking status was related with the prevalence of periodontal pathogens where smokers harbored more often periodontal pathogens such as P. gingivalis, P. micra, and F. nucleatum.
Literature
1.
go back to reference Jung RE, Zembic A, Pjetursson BE, Zwahlen M, Thoma DS (2012) Systematic review of the survival rate and the incidence of biological, technical, and aesthetic complications of single crowns on implants reported in longitudinal studies with a mean follow-up of 5 years. Clin Oral Implants Res 23(Suppl 6):2–21CrossRefPubMed Jung RE, Zembic A, Pjetursson BE, Zwahlen M, Thoma DS (2012) Systematic review of the survival rate and the incidence of biological, technical, and aesthetic complications of single crowns on implants reported in longitudinal studies with a mean follow-up of 5 years. Clin Oral Implants Res 23(Suppl 6):2–21CrossRefPubMed
2.
go back to reference Berglundh T, Persson L, Klinge B (2002) A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. J Clin Periodontol 29(Suppl 3):197–212CrossRefPubMed Berglundh T, Persson L, Klinge B (2002) A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. J Clin Periodontol 29(Suppl 3):197–212CrossRefPubMed
3.
go back to reference Atieh MA, Alsabeeha NH, Faggion CM Jr, Duncan WJ (2013) The frequency of peri-implant diseases: a systematic review and meta-analysis. J Periodontol 84:1586–1598PubMed Atieh MA, Alsabeeha NH, Faggion CM Jr, Duncan WJ (2013) The frequency of peri-implant diseases: a systematic review and meta-analysis. J Periodontol 84:1586–1598PubMed
4.
go back to reference Mombelli A, Decaillet F (2011) The characteristics of biofilms in peri-implant disease. J Clin Periodontol 38(Suppl 11):203–213CrossRefPubMed Mombelli A, Decaillet F (2011) The characteristics of biofilms in peri-implant disease. J Clin Periodontol 38(Suppl 11):203–213CrossRefPubMed
5.
go back to reference Fürst MM, Salvi GE, Lang NP, Persson GR (2007) Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 18:501–508CrossRefPubMed Fürst MM, Salvi GE, Lang NP, Persson GR (2007) Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 18:501–508CrossRefPubMed
6.
go back to reference Mombelli A, Buser D, Lang NP (1988) Colonization of osseointegrated titanium implants in edentulous patients. Early results. Oral Microbiol Immunol 3:113–120CrossRefPubMed Mombelli A, Buser D, Lang NP (1988) Colonization of osseointegrated titanium implants in edentulous patients. Early results. Oral Microbiol Immunol 3:113–120CrossRefPubMed
7.
go back to reference Mombelli A, Mericske-Stern R (1990) Microbiological features of stable osseointegrated implants used as abutments for overdentures. Clin Oral Implants Res 1:1–7CrossRefPubMed Mombelli A, Mericske-Stern R (1990) Microbiological features of stable osseointegrated implants used as abutments for overdentures. Clin Oral Implants Res 1:1–7CrossRefPubMed
8.
go back to reference Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A (2006) Dynamics of initial subgingival colonization of ‘pristine’ peri-implant pockets. Clin Oral Implants Res 17:25–37CrossRefPubMed Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A (2006) Dynamics of initial subgingival colonization of ‘pristine’ peri-implant pockets. Clin Oral Implants Res 17:25–37CrossRefPubMed
9.
go back to reference van Winkelhoff AJ, Goene RJ, Benschop C, Folmer T (2000) Early colonization of dental implants by putative periodontal pathogens in partially edentulous patients. Clin Oral Implants Res 11:511–520CrossRefPubMed van Winkelhoff AJ, Goene RJ, Benschop C, Folmer T (2000) Early colonization of dental implants by putative periodontal pathogens in partially edentulous patients. Clin Oral Implants Res 11:511–520CrossRefPubMed
10.
go back to reference Takanashi K, Kishi M, Okuda K, Ishihara K (2004) Colonization by Porphyromonas gingivalis and Prevotella intermedia from teeth to osseointegrated implant regions. Bull Tokyo Dent Coll 45:77–85CrossRefPubMed Takanashi K, Kishi M, Okuda K, Ishihara K (2004) Colonization by Porphyromonas gingivalis and Prevotella intermedia from teeth to osseointegrated implant regions. Bull Tokyo Dent Coll 45:77–85CrossRefPubMed
11.
go back to reference De Boever AL, De Boever JA (2006) Early colonization of non-submerged dental implants in patients with a history of advanced aggressive periodontitis. Clin Oral Implants Res 17:8–17CrossRefPubMed De Boever AL, De Boever JA (2006) Early colonization of non-submerged dental implants in patients with a history of advanced aggressive periodontitis. Clin Oral Implants Res 17:8–17CrossRefPubMed
12.
go back to reference van Brakel R, Cune MS, van Winkelhoff AJ, de Putter C, Verhoeven JW, van der Reijden W (2011) Early bacterial colonization and soft tissue health around zirconia and titanium abutments: an in vivo study in man. Clin Oral Implants Res 22:571–577CrossRefPubMed van Brakel R, Cune MS, van Winkelhoff AJ, de Putter C, Verhoeven JW, van der Reijden W (2011) Early bacterial colonization and soft tissue health around zirconia and titanium abutments: an in vivo study in man. Clin Oral Implants Res 22:571–577CrossRefPubMed
13.
go back to reference Mombelli A, van Oosten MA, Schurch E Jr, Land NP (1987) The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2:145–151CrossRefPubMed Mombelli A, van Oosten MA, Schurch E Jr, Land NP (1987) The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2:145–151CrossRefPubMed
14.
go back to reference Löe H, Silness J (1963) Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533–551CrossRefPubMed Löe H, Silness J (1963) Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533–551CrossRefPubMed
15.
go back to reference Syed SA, Loesche WJ (1972) Survival of human dental plaque flora in various transport media. Appl Microbiol 24:638–644PubMedPubMedCentral Syed SA, Loesche WJ (1972) Survival of human dental plaque flora in various transport media. Appl Microbiol 24:638–644PubMedPubMedCentral
17.
go back to reference van Steenbergen TJ, Petit MD, Tijhof CJ, van Winkelhoff AJ, van der Velden U, de Graaff J (1993) Survival in transport media of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia in human subgingival samples. Oral Microbiol Immunol 8:370–374CrossRefPubMed van Steenbergen TJ, Petit MD, Tijhof CJ, van Winkelhoff AJ, van der Velden U, de Graaff J (1993) Survival in transport media of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia in human subgingival samples. Oral Microbiol Immunol 8:370–374CrossRefPubMed
18.
go back to reference van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, van der Reijden WA (2001) Smoking affects the subgingival microflora in periodontitis. J Periodontol 72:666–671CrossRefPubMed van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, van der Reijden WA (2001) Smoking affects the subgingival microflora in periodontitis. J Periodontol 72:666–671CrossRefPubMed
19.
go back to reference 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 19:975–982CrossRefPubMed 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 19:975–982CrossRefPubMed
20.
go back to reference Eick S, Ramseier CA, Rothenberger K, Bragger U, Buser D, Salvi GE (2015) Microbiota at teeth and implants in partially edentulous patients. A 10-year retrospective study. Clin Oral Implants Res 27:218–225CrossRefPubMed Eick S, Ramseier CA, Rothenberger K, Bragger U, Buser D, Salvi GE (2015) Microbiota at teeth and implants in partially edentulous patients. A 10-year retrospective study. Clin Oral Implants Res 27:218–225CrossRefPubMed
21.
go back to reference Lindhe J, Berglundh T (1998). In: Lindhe J, Karring T, Lang NP (eds) Clinical periodontology and implant dentistry, 3rd edition. Munksgaard, Copenhagen, pp 862–867 Lindhe J, Berglundh T (1998). In: Lindhe J, Karring T, Lang NP (eds) Clinical periodontology and implant dentistry, 3rd edition. Munksgaard, Copenhagen, pp 862–867
22.
go back to reference van Winkelhoff AJ, Loos BG, van der Reijden WA, van der Velden U (2002) Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol 29:1023–1028CrossRefPubMed van Winkelhoff AJ, Loos BG, van der Reijden WA, van der Velden U (2002) Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol 29:1023–1028CrossRefPubMed
23.
go back to reference Leonhardt A, Renvert S, Dahlen G (1999) Microbial findings at failing implants. Clin Oral Implants Res 10:339–345CrossRefPubMed Leonhardt A, Renvert S, Dahlen G (1999) Microbial findings at failing implants. Clin Oral Implants Res 10:339–345CrossRefPubMed
24.
go back to reference Kumar PS, Matthews CR, Joshi V, de Jager M, Aspiras M (2011) Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect Immun 79:4730–4738CrossRefPubMedPubMedCentral Kumar PS, Matthews CR, Joshi V, de Jager M, Aspiras M (2011) Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect Immun 79:4730–4738CrossRefPubMedPubMedCentral
25.
go back to reference Cortelli SC, Cortelli JR, Romeiro RL, Costa FO, Aquino DR, Orzechowski PR, Araujo VC, Duarte PM (2013) Frequency of periodontal pathogens in equivalent peri-implant and periodontal clinical statuses. Arch Oral Biol 58:67–74CrossRefPubMed Cortelli SC, Cortelli JR, Romeiro RL, Costa FO, Aquino DR, Orzechowski PR, Araujo VC, Duarte PM (2013) Frequency of periodontal pathogens in equivalent peri-implant and periodontal clinical statuses. Arch Oral Biol 58:67–74CrossRefPubMed
26.
go back to reference Tamura N, Ochi M, Miyakawa H, Nakazawa F (2013) Analysis of bacterial flora associated with peri-implantitis using obligate anaerobic culture technique and 16S rDNA gene sequence. Int J Oral Maxillofac Implants 28:1521–1529CrossRefPubMed Tamura N, Ochi M, Miyakawa H, Nakazawa F (2013) Analysis of bacterial flora associated with peri-implantitis using obligate anaerobic culture technique and 16S rDNA gene sequence. Int J Oral Maxillofac Implants 28:1521–1529CrossRefPubMed
27.
go back to reference Persson GR, Renvert S (2014) Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res 16:783–793CrossRefPubMed Persson GR, Renvert S (2014) Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res 16:783–793CrossRefPubMed
Metadata
Title
Bacterial colonization of the peri-implant sulcus in dentate patients: a prospective observational study
Authors
M. A. Stokman
A. J. van Winkelhoff
A. Vissink
F. K. L. Spijkervet
G. M. Raghoebar
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 2/2017
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-1941-x

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