Prevalences of peri-implantitis and peri-implant mucositis: systematic review and meta-analysis

Abstract

Objectives

Due to the inconsistent definitions, reporting methods and study characteristics, prevalences of peri-implant diseases significantly varied in studies. This study aimed to systematically analyze implant-based and subject-based prevalences of peri-implant diseases and assess clinical variables potentially affecting the prevalence.

Sources

Electronic search of studies was conducted using MEDLINE (PubMed), EMBASE and Web of Science. Publication screening, data extraction, and quality assessment were performed.

Study selection

Clinical studies having an at least average three-year follow-up period were selected. The numbers of subjects and implants in the studies had to be equal to or more than thirty.

Data

Forty seven studies were selected and prevalences of peri-implant diseases were analyzed. Since heterogeneity existed in each outcome (I 2 = 94.7, 95.7, 95.3, and 99.3 for implant-based and subject-based peri-implantitis and peri-implant mucositis, respectively), the random-effects model based on the DerSimonian and Laird method, which incorporate an estimate of heterogeneity in the weighting, was applied to obtain the pooled prevalence. Weighted mean implant-based and subject-based peri-implantitis prevalences were 9.25% (95% Confidence Interval (CI): [7.57, 10.93]) and 19.83% (CI [15.38, 24.27) respectively. Weighted mean implant-based and subject-based peri-implant mucositis prevalences were 29.48% (CI: [22.65, 36.32]) and 46.83% (CI: [38.30, 55.36]) respectively. Functional time and implant to subject ratio were associated with subject-based peri-implantitis prevalence, but not peri-implant mucositis prevalences.

Conclusions

Peri-implant diseases were prevalent and prevalence of peri-implantitis increased over time. Prevalences of peri-implantitis and peri-implant mucositis might not be highly associated since the prevalences were influenced by distinct variables. The results should be carefully interpreted because of data heterogeneity.

Clinical significance

Peri-implant diseases affect a significant number of dental implants and patients. It is important to understand the difficulties in diagnosis of these diseases and risk factors which may be modified to reduce the potential for disease occurrence or progression.

Introduction

Peri-implant inflammation was observed at the time when clinicians initially started to place implants . Clinically, inflammatory peri-implant diseases are categorized into peri-implant mucositis or peri-implantitis. In the 1st European Workshop on Periodontology (EWOP), peri-implant mucositis was defined as a reversible inflammatory reaction in the soft tissues surrounding a functioning implant, and peri-implantitis was described as inflammatory reactions associated with loss of supporting bone around a functioning implant . Peri-implant diseases are treatable if inflammation is properly controlled . Therefore, reversibility of the disease has not been described in the definition nowadays. Briefly, peri-implant mucositis describes an inflammatory lesion that resides in the mucosa, while peri-implantitis describes a lesion not only involving mucosa but which also affects the supporting bone .

Clinically, peri-implantitis is more concerning than peri-implant mucositis given progressive bone loss will result in the loss of the functional implant. Although peri-implantitis is a term used to describe the symptoms of inflammation and alveolar bone loss around an implant decades ago , high prevalences of peri-implant diseases have not been noticed until the last decade . It was found that peri-implant mucositis occurred in approximately 80% of the subjects and in 50% of the implant sites. Peri-implantitis had a lower prevalence than peri-implant mucositis but it still occurred in approximately 28% to 77% of the subjects as well as in 12% to 43% of the implant sites . The reported prevalences varied due to the different diagnostic definitions . Peri-implant mucositis is usually diagnosed by clinical inflammation symptoms, such as bleeding on probing and/or suppuration and peri-implantitis can be diagnosed by radiographic alveolar bone level combined with or without clinical inflammation symptoms and/or probing depth (at least >4 mm) . The alveolar bone level is a useful parameter to represent the severity of peri-implantitis, however, it is difficult to know whether the observed bone level change is progressively caused by inflammation without the serial observations and radiographic images. Also, it is debatable how much bone loss should be considered to be a diseased state. Recently, it has been recommended to use the vertical distance of 2 mm from the expected marginal bone level following remodeling as the threshold for diagnosing peri-implantitis in the absence of consecutive radiographic images . However, the expected marginal bone level becomes subjective when the clinicians apply this definition.

There have been several reviews discussing the diagnosis and prevalences of peri-implant mucositis and peri-implantitis . The results from the meta-analyses demonstrated inconsistent prevalences due to the different study selection criteria and limited number of selected studies. This review aimed to systematically estimate prevalences of peri-implantitis and peri-implant mucositis with assessing the effects of different variables on prevalences. This review also included a large number of studies in the analyses since prevalences of peri-implant diseases had been productively reported over the last three years.

Materials and methods

This systematic review was performed by following the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guideline and previous recommendations .

Focused question

The focused question was proposed by following PICOS principle: the Population, the Intervention (or exposure), the appropriate Control (or comparator), the Outcomes of interest and the Study design.

“What are the prevalences of peri-implantitis and peri-implant mucositis in the implants and/or subjects of studies with an at least mean three-year follow-up period after implants are exposed?”

Study selection criteria

  • The articles were published in English

  • The retrospective, prospective, and cross sectional studies having an at least average three-year follow-up period after the implants were connected with abutments or restored with crowns. These studies only recruited human subjects.

  • The numbers of subjects and implants in the studies had to be equal to or more than thirty

  • The study reported the prevalence ofperi-implantitis/peri-implant mucositis or the prevalence of biological complications based on specific clinical parameters. The prevalence could be reported at the implant level or the subject level. The study was excluded if there was no information ofperi-implantitis prevalence.

Search strategy

Search of articles was conducted in the electronic databases, including MEDLINE (PubMed), EMBASE, Web of Science and Dental and Oral Sciences Source from January 1900 to March 2016. Specific search terms were used in each database ( Fig. 1 , Appendix 1 in Supplementary material).

Fig. 1
Study search and selection. This flow chart demonstrated the process of selecting articles.

Quality of the selected studies

Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement was used to evaluate the quality of selected studies . Varied numbers of items on the checklist of STROBE were assessed in each study depending on the study design (Appendix 2 in Supplementary material). Each assessed item was documented as present, absent, or not applicable in the articles. The results were demonstrated as adherence rate that was calculated by dividing assessed items present in each study by the total assessed items .

Data extraction

The titles and abstracts of articles found in databases were independently screened by two authors (C.L, Y.H), then the full texts of qualified articles were read and selected. Any disagreement was solved by discussion of authors (C.L, Y.H). Data were extracted independently by two authors (C.L, Y.H) with a specially designed data extraction form. The accuracy of the extracted data was confirmed by another author (L.Z).

Statistical analysis

The primary outcome in the present study was the prevalence of peri-implantitis. Peri-implantitis was defined in each study by the radiographic bone level of the implant with or without other clinical parameters, such as bleeding on probing/suppuration and/or clinical probing depth. Prevalence is described as the proportion of individuals (implants) in a population that have the condition (peri-implant diseases) at a specified point in time . All studies were treated as cross-sectional studies for data analysis. Only the data at one specific time point were retracted. If the study reported results of peri-implantitis prevalence with multiple time points and/or defined peri-implantitis by multiple thresholds, the results with the last follow-up appointment and/or the threshold closest to the peri-implantitis definition in the VIII European Workshop on Periodontology were chosen for the analysis. Data extraction for peri-implant mucositis also followed the same rationale. Both implant-based and subject-based peri-implantitis prevalences were estimated. Implant-based peri-implantitis prevalence (IPI) was calculated by dividing the number of implants affected by peri-implantitis by the number of all implants. Subject-based peri-implantitis prevalence (SPI) was calculated by dividing the number of subjects having peri-implantitis affected implant(s) by the number of all subjects. In addition to the prevalences of peri-implantitis, implant-based peri-implant mucositis prevalence (IM) and subject-based peri-implant mucositis prevalence (SM) were also calculated. Peri-implant mucositis was defined by the presence of bleeding on probing of the implant with or without other clinical parameters. Each implant was diagnosed with peri-implantitis, peri-implant mucositis or no peri-implant disease.

For each outcome, heterogeneity was examined with I 2 (Appendix 3 in Supplementary material) and heterogeneity chi-square test, and p value <0.05 was considered statistically significant for heterogeneity . Since heterogeneity existed in each outcome, the random-effects model based on the DerSimonian and Laird method was applied to obtain the pooled prevalence: weighted mean subject-based peri-implantitis prevalence (WSPI), weighted mean implant-based peri-implantitis prevalence (WIPI), weighted mean subject-based peri-implant mucositis prevalence (WSM), and weighted mean implant-based peri-implant mucositis prevalence (WIM). We generated forest plots to depict the prevalence along with its 95% confidence interval (95% CI) for each individual study as well as the pooled prevalence by combining all studies. Considering these are proportion studies with low proportion outcomes, a logit transformation was used to calculate the overall proportion, and Clopper-Pearson method was used to calculate 95% confidence interval . Potential publication bias was evaluated using funnel plots, and Egger test was performed to evaluate the symmetry of the funnel plots . Because conventional funnel plots are inaccurate for meta-analyses of proportion studies with low proportion outcomes , the funnel plots and Egger test were based on the results after logit transformation as well.

In addition, since significant heterogeneity was found in each outcome, a meta-regression analysis was performed to assess whether heterogeneity among results of multiple studies was related to specific characteristics of the studies including the follow-up period, implant/subject ratio, implant surface characteristics, prosthesis type, definition of peri-implant diseases (radiographic bone level; inflammatory signs), smoking history, periodontitis history, and immediate implant placement.

We further assessed bone level change threshold (>2 mm or ≤2 mm) and subject number (n ≥ 100 or <100) in subgroup analysis. It is generally accepted that the bone level change threshold, whether >2 mm or ≤2 mm, defines the occurrence of peri-implantitis . Utilizing the selected articles, prevalence of peri-implantitis was determined in a subgroup analysis of the data with >2 mm or ≤2 mm threshold of bone level change. A previous meta-analysis limited the selection of studies with ≥100 participants . In order to determine if mean prevalence differed based on the number of participants, a subgroup analysis of data from selected studies including ≥ or <100 participants was performed.

A leave-one-out sensitivity analysis, which is iteratively removing one study at a time to confirm whether our findings were driven by any single study, and other sub-analyses were performed. Statistical analyses were mainly conducted using STATA (Stata Statistical Software, Version 14, 2015, Stata Corp, College Station, TX, USA).

Materials and methods

This systematic review was performed by following the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guideline and previous recommendations .

Focused question

The focused question was proposed by following PICOS principle: the Population, the Intervention (or exposure), the appropriate Control (or comparator), the Outcomes of interest and the Study design.

“What are the prevalences of peri-implantitis and peri-implant mucositis in the implants and/or subjects of studies with an at least mean three-year follow-up period after implants are exposed?”

Study selection criteria

  • The articles were published in English

  • The retrospective, prospective, and cross sectional studies having an at least average three-year follow-up period after the implants were connected with abutments or restored with crowns. These studies only recruited human subjects.

  • The numbers of subjects and implants in the studies had to be equal to or more than thirty

  • The study reported the prevalence ofperi-implantitis/peri-implant mucositis or the prevalence of biological complications based on specific clinical parameters. The prevalence could be reported at the implant level or the subject level. The study was excluded if there was no information ofperi-implantitis prevalence.

Search strategy

Search of articles was conducted in the electronic databases, including MEDLINE (PubMed), EMBASE, Web of Science and Dental and Oral Sciences Source from January 1900 to March 2016. Specific search terms were used in each database ( Fig. 1 , Appendix 1 in Supplementary material).

Fig. 1
Study search and selection. This flow chart demonstrated the process of selecting articles.

Quality of the selected studies

Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement was used to evaluate the quality of selected studies . Varied numbers of items on the checklist of STROBE were assessed in each study depending on the study design (Appendix 2 in Supplementary material). Each assessed item was documented as present, absent, or not applicable in the articles. The results were demonstrated as adherence rate that was calculated by dividing assessed items present in each study by the total assessed items .

Data extraction

The titles and abstracts of articles found in databases were independently screened by two authors (C.L, Y.H), then the full texts of qualified articles were read and selected. Any disagreement was solved by discussion of authors (C.L, Y.H). Data were extracted independently by two authors (C.L, Y.H) with a specially designed data extraction form. The accuracy of the extracted data was confirmed by another author (L.Z).

Statistical analysis

The primary outcome in the present study was the prevalence of peri-implantitis. Peri-implantitis was defined in each study by the radiographic bone level of the implant with or without other clinical parameters, such as bleeding on probing/suppuration and/or clinical probing depth. Prevalence is described as the proportion of individuals (implants) in a population that have the condition (peri-implant diseases) at a specified point in time . All studies were treated as cross-sectional studies for data analysis. Only the data at one specific time point were retracted. If the study reported results of peri-implantitis prevalence with multiple time points and/or defined peri-implantitis by multiple thresholds, the results with the last follow-up appointment and/or the threshold closest to the peri-implantitis definition in the VIII European Workshop on Periodontology were chosen for the analysis. Data extraction for peri-implant mucositis also followed the same rationale. Both implant-based and subject-based peri-implantitis prevalences were estimated. Implant-based peri-implantitis prevalence (IPI) was calculated by dividing the number of implants affected by peri-implantitis by the number of all implants. Subject-based peri-implantitis prevalence (SPI) was calculated by dividing the number of subjects having peri-implantitis affected implant(s) by the number of all subjects. In addition to the prevalences of peri-implantitis, implant-based peri-implant mucositis prevalence (IM) and subject-based peri-implant mucositis prevalence (SM) were also calculated. Peri-implant mucositis was defined by the presence of bleeding on probing of the implant with or without other clinical parameters. Each implant was diagnosed with peri-implantitis, peri-implant mucositis or no peri-implant disease.

For each outcome, heterogeneity was examined with I 2 (Appendix 3 in Supplementary material) and heterogeneity chi-square test, and p value <0.05 was considered statistically significant for heterogeneity . Since heterogeneity existed in each outcome, the random-effects model based on the DerSimonian and Laird method was applied to obtain the pooled prevalence: weighted mean subject-based peri-implantitis prevalence (WSPI), weighted mean implant-based peri-implantitis prevalence (WIPI), weighted mean subject-based peri-implant mucositis prevalence (WSM), and weighted mean implant-based peri-implant mucositis prevalence (WIM). We generated forest plots to depict the prevalence along with its 95% confidence interval (95% CI) for each individual study as well as the pooled prevalence by combining all studies. Considering these are proportion studies with low proportion outcomes, a logit transformation was used to calculate the overall proportion, and Clopper-Pearson method was used to calculate 95% confidence interval . Potential publication bias was evaluated using funnel plots, and Egger test was performed to evaluate the symmetry of the funnel plots . Because conventional funnel plots are inaccurate for meta-analyses of proportion studies with low proportion outcomes , the funnel plots and Egger test were based on the results after logit transformation as well.

In addition, since significant heterogeneity was found in each outcome, a meta-regression analysis was performed to assess whether heterogeneity among results of multiple studies was related to specific characteristics of the studies including the follow-up period, implant/subject ratio, implant surface characteristics, prosthesis type, definition of peri-implant diseases (radiographic bone level; inflammatory signs), smoking history, periodontitis history, and immediate implant placement.

We further assessed bone level change threshold (>2 mm or ≤2 mm) and subject number (n ≥ 100 or <100) in subgroup analysis. It is generally accepted that the bone level change threshold, whether >2 mm or ≤2 mm, defines the occurrence of peri-implantitis . Utilizing the selected articles, prevalence of peri-implantitis was determined in a subgroup analysis of the data with >2 mm or ≤2 mm threshold of bone level change. A previous meta-analysis limited the selection of studies with ≥100 participants . In order to determine if mean prevalence differed based on the number of participants, a subgroup analysis of data from selected studies including ≥ or <100 participants was performed.

A leave-one-out sensitivity analysis, which is iteratively removing one study at a time to confirm whether our findings were driven by any single study, and other sub-analyses were performed. Statistical analyses were mainly conducted using STATA (Stata Statistical Software, Version 14, 2015, Stata Corp, College Station, TX, USA).

Results

Study selection

Two thousand eight hundred and thirty articles were found following the search process ( Fig. 1 ). After reviewing the titles and abstracts, 192 articles were identified and 145 articles were excluded from the final analysis (Appendix 4 in Supplementary material). Finally, forty-seven studies with forty-nine data sets were selected for the analyses (Appendix 4 in Supplementary material). Some studies contributed more than one data set because multiple groups had the data of interest. In the selected studies, not every study reported the data of IPI, SPI, IM, and SM. The studies were included in the analyses when they provided required information.

Quality assessment

The adherence rate ranged from 0.39 to 0.79 and the mean adherence rate was 0.60 (Appendix 5 in Supplementary material). Twenty-eight out of forty-seven articles had adherence rate over the mean. The impact of study quality (adherence rare > or ≤ 0.60) was assessed in a sub-analysis.

Subject characteristics

Two studies had more than one subject group depending on the severity of periodontitis . Only twenty-two studies reported the history of periodontitis and nine of them included all subjects with periodontitis . Most of the studies reported subjects’ history of smoking but ten out of forty-seven studies did not. ( Table 1 ).

Table 1
Studies characteristics.
Study Fransson et al. (2005) Roos-Jansaker et al. (2006) Gatti et al. (2008) Maximo et al. (2008) Koldsland et al. (2010) Rocccuzzo et al. (2010)
Study design Cross-sectional Cohort Cohort Cross-sectional Cross-sectional Cohort
Number of subjects/number of implants 662/3413 216/987 56/N/A 113/347 99/305 73/185
Follow-up in years 8.6 10.8 5.0 3.4 7.4 10.0
Patient with periodontitis N/A N/A Patients included N/A N/A All
Smokers (%) N/A 69.5 22.6 18.6 54.1 N/A
Prosthesis Fixed/removable Fixed/removable Fixed/removable Fixed/removable N/A Fixed
Implant surface Smooth Smooth Rough/smooth Smooth Rough/smooth Rough
Case definition Peri-implantitis : Bone level change > 1.8 mm after the first year of function Mucositis : Not defined Peri-implantitis : Bone level change > 1.8 mm after the first yeat of function + BOP Mucositis : BOP + PD > 4 mm + no bone level change after the first year of function Peri-implantitis : Bone level change > 2 mm from the platform + BOP + PD > 5 mm Mucositis : Not defined Peri-implantitis : Bone level change > 1.8 mm from the platform + BOP + PD > 5 mm Mucositis : BOP + bone level change < 1.8 mm from the platform Peri-implantitis : Bone level change > 2 mm from the platform + BOP + PD > 4 mm Mucositis : BOP + no bone level change from the platform Peri-implantitis : Bone level change > 3 mm from the platform Mucositis : Not defined
Prevalence ofperi-implantitis Implant level: 12.4
Subject level: 27.8
Implant level: 6.6 Subject level: 16.2 Implant level: N/A Subject level: 3.6 Implant level: 7.5 Subject level: 12.4 Implant level: 12.5 Subject level: 21.2 Implant level: N/A Subject level: 28.8
Prevalence of mucositis Implant level: N/A
Subject level: N/A
Implant level: 16.0 Subject level: 48.2 Implant level: N/A Subject level: N/A Implant level: 32.0 Subject level: 26.3 Implant level: 26.9 Subject level: 41.4 Implant level: N/A Subject level: N/A
Study Simonis et al. (2010) Wahlström et al. (2010) Zetterqvist et al. (2010) Kammerer et al. (2011) Dierens et al. (2012) Finne et al. (2012)
Study design Cohort Cohort Cohort RCT Cross-sectional Cohort Cohort
Number of subjects/number of implants 55/124 46/116 96/270 41/237 48/59 47/66
Follow-up in years 13.0 5.1 5.0 9.1 18.4 3.0
Patient with periodontitis Patients included All N/A N/A None N/A
Smokers (%) 16.4 57 15 7.3 22.2 N/A
Prosthesis Fixed Fixed Fixed Fixed/removable Fixed Fixed
Implant surface Rough Rough Rough/hybrid Rough Smooth Rough
Case definition Peri-implantitis : Bone level change > 2.5 mm or 3 threads bone level change from the platform + BOP + PD > 5 mm Mucositis : Not defined Peri-implantitis : Bone level change > 2 mm after the first year of function + BOP + PD > 4 mm Mucositis: BOP + PD < 4 mm + no bone level change after the first year of function Peri-implantitis : Bone level change > 5 mm from the platform + BOP + PD > 5 mm Mucositis : Not defined Peri-implantitis : Bone level change > 2 mm during the first year and > 0.2 mm annually after the first year + PD > 5 mm + BOP Mocositis : BOP + PD > 5 mm + bone level change < 2 mm during the first year and < 0.2 mm annually after the first year Peri-implantitis : Bone level change > 2 mm from the platform + BOP + PD > 4 mm Mocusitis : BOP + PD > 4 mm + bone level change < 2 mm from the platform Peri-implantitis : Bone level change > 3 mm from the platform + BOP + PD > 5 mm Mucositis : Not defined
Prevalence ofperi-implantitis Implant level: 16.9 Subject level: N/A Implant level: N/A Subject level: 4.4 Implant level: 0.4 Subject level: N/A Implant level: 2.1 Subject level: N/A Implant level: 10.2 Subject level: N/A Implant level: 1.5 Subject level: 2.1
Prevalence of mucositis Implant level: N/A Subject level: N/A Implant level: N/A Subject level: 21.7 Implant level: N/A Subject level: N/A Implant level: 8.9 Subject level: N/A Implant level: 32.2 Subject level: N/A Implant level: N/A Subject level: N/A
Study Lee et al. (2012) Lopez-Priz et al. (2012) Mir-Mari et al. (2012) Pjetursson et al. (2012) Swierkot et al. (2012) Fardal et al. (2013)
Study design Case control Cross-sectional Cross-sectional Cohort Cohort Cross-sectional
Number of subjects/number of implants 60/117 117/268 245/964 70/152 35/143 43/119
Follow-up in years 8.1 4.5 6.3 7.9 8.6 16.4
Patient with periodontitis Patients included N/A All All All All
Smokers (%) 10 37.6 N/A 27.4 42.3 63
Prosthesis Fixed/removable Fixed/removable N/A Fixed Fixed/removable Fixed
Implant surface Rough N/A Rough/smooth Rough Rough/smooth Rough
Case definition Peri-implantitis : Bone level change > 2 mm from the platform + BOP + PD > 5 mm Mucositis : BOP + PD > 5 mm Peri-implantitis : Bone level change > 2 mm from the platform + BOP Mucositis : BOP + bone level change < 2 mm from the platform Peri-implantitis : Bone level change > 1.2 mm from the platform + BOP Mucositis : BOP + bone level change < 1.2 mm from the platform Peri-implantitis : Bone level change > 2 mm after bone remodeling Mucositis : BOP + PD > 5 mm Peri-implantitis : Bone level change > 0.2 mm annually after the first year of function Mucositis : BOP + PD > 5 mm + no bone level change Peri-implantitis : Bone level change > 3 threads after the first year of function + BOP Mucositis: Not defined
Prevalence ofperi-implantitis Implant level: 10.3 Subject level: 33.3 Implant level: 16.0 Subject level: N/A Implant level: 9.1 Subject level: 16.3 Implant level: 4.6 Subject level: N/A Implant level: 27.2 Subject level: 42.9 Implant level: 31.1 Subject level: 53.5
Prevalence of mucositis Implant level: 9.4 Subject level: 53.3 Implant level: 36.9 Subject level: N/A Implant level: 21.6 Subject level: 39.2 Implant level: 25.0 Subject level: 38.6 Implant level: 58.7 Subject level: 74.3 Implant level: N/A Subject level: N/A
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Jun 17, 2018 | Posted by in General Dentistry | Comments Off on Prevalences of peri-implantitis and peri-implant mucositis: systematic review and meta-analysis
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