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Review
The Frequency of Peri-Implant Diseases: A SystematicReview and Meta-Analysis
Momen A. Atieh,* Nabeel H.M. Alsabeeha,† Clovis Mariano Faggion Jr.,* and Warwick J. Duncan*
Background: The peri-implant diseases, namely peri-im-plant mucositis and peri-implantitis, have been extensivelystudied. However, little is known about the true magnitudeof the problem, owing mainly to the lack of consistent anddefinite diagnostic criteria used to describe the condition.The objective of the present review is to systematically esti-mate the overall frequency of peri-implant diseases in gen-eral and high-risk patients.
Methods: The systematic review is prepared according tothe Meta-analysis of Observational Studies in Epidemiologystatement. Studies were searched in four electronic data-bases, complemented by manual searching. The quality ofthe studies was assessed according to Strengthening theReporting of Observational Studies in Epidemiology, andthe data were analyzed using statistical software.
Results: Of 504 studies identified, nine studies with 1,497participants and 6,283 implants were included. The sum-mary estimates for the frequency of peri-implant mucositiswere 63.4% of participants and 30.7% of implants, and thoseof peri-implantitis were 18.8% of participants and 9.6% of im-plants. A higher frequency of occurrence of peri-implant dis-eases was recorded for smokers, with a summary estimateof 36.3%. Supportive periodontal therapy seemed to reducethe rate of occurrence of peri-implant diseases.
Conclusions: Peri-implant diseases are not uncommonfollowing implant therapy. Long-term maintenance care forhigh-risk groups is essential to reduce the risk of peri-implantitis. Informed consent for patients receiving implanttreatment must include the need for such maintenance ther-apy. J Periodontol 2013;84:1586-1598.
KEY WORDS
Dental implants; diagnosis; epidemiology; meta-analysis;peri-implantitis; review.
The use of oral implants to sup-port fixed and removable pros-theses is a widely accepted
treatment modality of high success andpredictability.1-3 Despite the highsuccess and survival rates of oral im-plants, failures do occur, and implant-supported prostheses may requiresubstantial periodontal and prostho-dontic maintenance over time.4-6 Im-plant failures have been traditionallydescribed as early or late. Early fail-ures occur before implant loading andcould be caused by surgery-, implant-,or host-related factors. Late failures, onthe other hand, occur after prostho-dontic rehabilitation as a result of peri-implant disease or biomechanicaloverload.7,8 Peri-implant disease isthought to result in bone loss aroundthe implants and subsequent loss ofosseointegration.7,9 An accurate esti-mate of the true prevalence of peri-implant disease, however, remainscontroversial. The inconsistencies indefining and reporting its two commonforms, peri-implant mucositis and peri-implantitis, are very apparent.10
The term peri-implantitis first ap-peared in the literature in 1987 ina study by Mombelli et al.11 It wasdescribed as an infectious disease withmany features common to peri-odontitis. Since then, a growing interestin defining peri-implant disease asa clinical entity and proposing a treat-ment approach for it has been
* Department of Oral Sciences, Faculty of Dentistry, Oral Implantology Research Group,Sir John Walsh Research Institute, University of Otago, Dunedin, New Zealand.
† Prosthetic Section, RAK Dental Center, Ministry of Health, Ras Al-khaimah, United ArabEmirates.
doi: 10.1902/jop.2012.120592
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observed. The multifaceted etiology and variedcharacteristics of the disease, however, resulted inlack of consensus in defining peri-implant diseasefrom a clinical perspective. For example, twoconsensus reports12,13 define peri-implant mucosi-tis as an inflammatory response limited to the softtissues surrounding a functioning oral implant,whereas peri-implantitis elicits an inflammatoryresponse that involves loss of marginal bone arounda functioning oral implant. These reports, however,failed to set rigid clinical parameters that could beused to diagnose the two conditions. Furthermore,the 3rd International Team for Implantology Con-sensus Conference14 presented similar definitions,and additional diagnostic parameters were alsosuggested. Accordingly, the presence of plaque andsuppuration, bleeding on probing (BOP), andprobing depth (PD) >5 mm were required to defineperi-implantitis. Analysis of peri-implant sulcularfluid was also included as a diagnostic aid for peri-implantitis, albeit without indicating a specificmarker for it.
Other variations of the above diagnostic criteriafor peri-implant diseases also exist in the literature.For example, peri-implant mucositis was diagnosedbased on the presence of BOP/suppuration and PD>4 mm, whereas peri-implantitis required PD >5mm and radiographic bone loss of >0.2 mm an-nually or progressive bone loss of >3 threadscombined with signs of peri-implant mucositis.15-17
The prevalence of peri-implant diseases has beenreported in the literature.6,13,18 However, consid-erable variations among these studies are noted. Ina systematic review by Berglundh et al.,18 the bi-ologic and technical complications in oral implanttherapy were summarized by reviewing a largenumber of longitudinal prospective studies. Peri-implantitis, as defined by Albrektsson and Isidor,12
was reported in 6.47% of the implants included intheir review. In contrast, Zitzmann and Berglundh13
showed that the frequency of peri-implantitis variedbetween 28% and ‡56% of the participants and 12%and 43% of individual implants. The causes for thediscrepancy in the results reported in these sys-tematic reviews could be the lack of standardizedcriteria for diagnosing peri-implant mucositis andperi-implantitis, the different implant systems used,or the differences in the observation periods.
The impact of peri-implant diseases on treatmentoutcomes with oral implants has gained much in-terest in recent years. It is deemed essential todetermine the true prevalence of peri-implant dis-ease to allow well-informed consent and developrigid supportive maintenance programs for high-riskgroups. The aim of this article, therefore, is tosystematically review the current literature and
perform a meta-analysis to estimate the prevalenceof peri-implant disease and determine the riskfactors associated with its development in patientsreceiving oral implant treatment.
MATERIALS AND METHODS
The current systematic review and meta-analysisconforms to the guidelines outlined by the Meta-analysis of Observational Studies in Epidemiology(MOOSE) statement.19 The focused question for-mulated to summarize the objectives of the studywas: What is the prevalence of peri-implant dis-eases in general and high-risk participants over 5years? The presence of one or more of three riskfactors (history of periodontal disease, smoking,and diabetes) is required to define a participant athigh risk. An observation period of >5 years wasselected because peri-implant mucositis and peri-implantitis are slowly progressing diseases thatseem to require long-term follow-up to be identi-fied.20
Inclusion CriteriaStudies were selected if they met the following in-clusion criteria: 1) report written in English; 2)human study population; 3) prospective, retro-spective, cross-sectional, and observational cohortstudy reporting the number of cases of peri-implantmucositis and/or peri-implantitis using specificclinical parameters; 4) follow-up duration of at least5 years of functional loading time, an observationperiod needed to critically assess the prevalence ofperi-implant diseases. In the case of multiplepublications of the same study, the one with themost detailed information was included.
Exclusion CriteriaStudies were excluded if they: 1) were case seriesor case reports; 2) did not clearly define clinicalparameters to define peri-implant diseases; 3) failedto report the number of implants with peri-implantdiseases; or 4) had an observation period of <5years after functional loading.
Search StrategyThe relevant articles were retrieved from the fol-lowing electronic databases: 1) MEDLINE; 2) Em-base; 3) Cochrane Central Register of ControlledTrials (Central); and 4) the MetaRegister for on-going and unpublished trials. The search was per-formed up to January 30, 2012, and included thekey words listed in Table 1. Two authors (MA andNA) performed the search independently, in du-plicate, and any disagreement was solved byconsensus. The bibliographies of potentially se-lected papers were scrutinized for additional
J Periodontol • November 2013 Atieh, Alsabeeha, Faggion, Duncan
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material. A manual search was also conductedwithin the last 10 years of the following journals:Clinical Implant Dentistry and Related Research,Clinical Oral Implants Research, Implant Dentistry,International Journal of Oral & Maxillofacial Im-plants, International Journal of Periodontics andRestorative Dentistry, Journal of Clinical Periodon-tology, Journal of Dental Research, Journal of OralImplantology, and Journal of Periodontology.
Data CollectionOnce a study was included in the analysis, twoauthors (MA and NA) independently used a pre-determined data collection form to extract thefollowing information: 1) title of the study; 2) yearof publication; 3) country of origin; 4) numberof participants/implants; 5) implant design andsystem; 5) number of participants/implants asso-ciated with peri-implant mucositis and/or peri-implantitis; and 6) associated risk factors (historyof periodontal disease, smoking, and diabetes).Data related to the smokers or patients withperiodontitis were separately reported from thestudies that clearly defined the number of cases ofperi-implant diseases in smokers or those whohad periodontitis and/or diabetes. Any disagree-ments in the data collection reports were resolvedby consensus. Attempts were made to contact thecorresponding authors when additional informationwas needed.
Definition of Peri-Implant DiseasesThe clinical criteria set to define peri-implantdisease in this review are determined based onestablished consensus reports, workshop sum-maries, and reviews.12-14,21 Peri-implant mucosi-tis is defined as an inflamed mucosa with
a bleeding index of ‡2 and/or suppuration butwithout bone loss. Peri-implant bleeding tendencyis assessed using the modified sulcus bleedingindex.11 Peri-implantitis is defined as the pres-ence of inflamed mucosa with a positive BOP,PD ‡5 mm, and cumulative bone loss of ‡2 mmand/or ‡3 threads of implant (Fig. 1). Studiesnot conforming to the specific clinical criteriadefining peri-implant disease in this review areexcluded from the analysis.
Table 1.
Search Strategy
Database Key words
Published studiesMEDLINE via Ovid (January 30, 2012) (exp peri-implantitis/OR peri-implantitis.mp OR peri-implant mucositis.mp.
OR peri-implant mucositis OR perimucositis) AND (exp Dental Implants/ORexp Dental Implantation OR ((dental or oral) adj5 implant$).mp.)
Embase via Ovid (January 30, 2012) (exp peri-implantitis/ OR peri-implantitis.mp. OR peri-implant mucositis.mp.OR peri-implant mucositis OR perimucositis) AND (dental implantation.mp.OR ((dental or oral) adj5 implant$).mp.)
Cochrane Central Register of Controlled Trials(Central) via Ovid (January 30, 2012)
(peri-implantitis.mp. OR peri-implantitis.mp. OR peri-implant mucositis.mp.OR peri-implant mucositis.mp.) AND (exp Dental Implant/OR exp DentalImplantation/OR ((dental or oral) adj5 implant$).mp.)
Unpublished studiesMetaRegister (January 31, 2012) (peri-implantitis or periimplantitis), (peri-implant mucositis or perimucositis)
Figure 1.Diagnostic criteria of peri-implant diseases.
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Quality Assessment and Data SynthesisA quality assessment tool derived from theStrengthening the Reporting of ObservationalStudies in Epidemiology (STROBE) statement22
was developed to assess the quality of reportingof the studies. A single point was given for eachitem in the study meeting the predefined criteria,for a total of 12 items. Therefore, a summaryscore between 0 and 12 was given for each study,with a higher score indicating better study quality.A statistical software program‡ was used to con-duct the meta-analysis. The summary estimate ofthe frequency of peri-implant diseases was de-termined using a random-effect model23 at bothparticipant and implant levels depending on theselected unit of statistical analysis. Heterogene-ity across the studies was assessed using the I2
statistic.24 An I2 value >50 indicates significantheterogeneity.
Sensitivity and SubgroupAnalysesSensitivity analysis was per-formed to evaluate the in-fluence of deleting studiesthat may have influence onthe meta-analytic summaryestimate. Subgroup analysiswas undertaken to providea prevalence estimate of peri-implant diseases based onthe presence of risk factors(smoking, diabetes, and his-tory of periodontal disease),as well as the effect of a pre-ventive maintenance program,where those data were sepa-rately reported in the selectedstudies.
RESULTS
A total of 504 studies wereidentified from the databases(Fig. 2). Only 22 studies wereeligible for full-text evaluation.Of these, 1415,25-37 were ex-cluded and one was selectedfrom a reference list, resultingin nine papers included in themeta-analysis.16,38-45 The man-ual search did not provide anyfurther studies.
Description of StudiesThe characteristics of the ninestudies are summarized inTable 2. A total of 6,283 im-
plants and 1,497 participants were available at theend of the follow-up period. All the studies wereconducted in a university setting except two,38,44
where implant placement and maintenance werecarried out in private dental practices. The obser-vation period ranged from 5 years39 to >10years.16,42,45 All of the studies presented data onthe frequency of peri-implantitis, whereas only fivestudies provided information on the frequency ofperi-implant mucositis.16,39,41,43,44 Two studiesused the participant as the statistical unit of anal-ysis,39,44 whereas in another two,41,42 data analysiswas based on the implant. The remaining fivestudies16,38,40,43,45 presented their results at bothparticipant and implant levels. Six studies16,38,39,42-44
made provisions for a supportive maintenanceprogram during the observation period. In two of
Figure 2.Flowchart of the search process.
‡ STATA, v.10.1, Stata, College Station, TX.
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Table
2.
CharacteristicsoftheIncludedStudies
Cho
-Yan
Lee
etal.38
Ferreira
etal.39
Fransson
etal.40
Kaemmerer
etal.41
Karoussis
etal.42
Koldslandet
al.43
Rinke
etal.44
Roos-Jansaker
etal.16
Simonis
etal.45
Studydesign
Retrospective
Cross-sectio
nal
Cross-
sectional
Retrospective
Prospective
Cross-sectio
nal
Cross-sectio
nal
Cross-sectio
nal
Retrospective
Locatio
nAustralia
Brazil
Sweden
Germany
Switzerland
Norw
ayGermany
Sweden
France
Participants/im
plants(n)*
60/117
212/578
662/3,413
41/237
53/112
109/351
89/357
216/987
55/124
Supportiveperiodontal
maintenance
program
Provided
Provided
NR
NR
Provided
Provided
Provided
Provided
NR
Implant
system
A†
B,‡
C,§Di
B‡
E¶A†
B,‡
C,§
E¶F#
B‡
A†
Implant
surfacetopography
Titanium
plasm
a-
sprayed
andsand-
blasted
acid-
etched
solid
screws,
hollow
screws,
andho
llow
cylinders
Oxidized
surface,
dualacid-
etched,
and
bioceramic
microblasted
surface
Oxidized
surface
Moderately
rough
surface,
grit-blasted
with
particlesof
titanium
oxide
Plasm
a-
sprayed
Oxidizedsurface,
acid-etched
anddual
acid-etched
Microtextured
surface
Oxidized
surface
Titanium
plasm
a-
sprayed
cylindric
Peri-implant
mucositis
(n)
Participants
NR
137
NR
NR
NR
41
40
167
NR
Implants
NR
NR
NR
21
NR
82
NR
478
NR
Peri-implantitis(n)
Participants
16
19
184
NR
NR
49
10
62
9
Implants
23
NR
423
513
108
NR
69
21
Meanfollow-upperiod
(years)
85
9.1
9.1
10
8.4
5.7
11.5
13
Modified
STROBErating
10
98
75
97
79
NR=notreported
.*
Included
intheanalysisattheen
doffollo
w-upperiod.
†Straumann,Base
l,Switzerland.
‡Nobel
Bioca
re,Goteborg,Swed
en.
§3iIm
plantInnova
tions,
Palm
Bea
chGarden
s,FL.
iIntra-lock
International,Boca
Raton,FL.
¶Astra
Tec
h,Molndal,Swed
en.
#DENTSPLYFriaden
t,Mannheim,Germany.
Frequency of Peri-Implant Diseases Volume 84 • Number 11
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these studies,16,43 the maintenance program wascarried out by the referring dentist.
In a cohort study of 53 partially edentulous pa-tients treated with implant-supported fixed pros-theses, the authors assessed the technical andbiologic complications over 10 years.42 The termsperi-implantitis and biologic complication were usedinterchangeably by the authors and indicated thepresence of PD ‡5 mm, bleeding/suppuration onprobing, and radiographic bone loss. It was shownthat participants with a previous history of peri-odontitis treated before implant placement were ata higher risk of developing peri-implantitis. In ad-dition, smokers were also found to be at a higherrisk compared with non-smokers, but the differencewas not statistically significant.
Fransson et al.40 examined the intraoral radio-graphs of 662 participants with 3,413 implants thatwere in function for 5 to 20 years. Peri-implantitiswas defined as progressive bone loss of >3threads. Results showed that 12.4% of implants and27.8% of participants presented with signs of peri-implantitis. The use of participants rather thanimplants as the unit of analysis was emphasized, asthe larger number of implants tends to dilute theprevalence rate.
Roos-Jansaker et al.16 reported the prevalence ofperi-implant disease in 218 patients with 999 im-plants after 9 to 14 years of function. The preva-lence rate of peri-implant mucositis ranged from18.3% to 76.6%, and that of peri-implantitis rangedfrom 3.7% to 28.7% depending on the PD mea-surements. A supportive maintenance program,although not standardized to all patients, wasprovided by the referring clinicians. It was con-cluded that without supportive maintenance ther-apy, peri-implant disease could be a commoncomplication in the long term.
In a cross-sectional study, Ferreira et al.39 in-vestigated the prevalence of peri-implant mucositisand peri-implantitis in a population of 212 partici-pants. All relevant clinical parameters were as-sessed by two investigators masked to the identityand medical background of the participants. A lo-gistic regression analysis identified high plaquescores and poor glycemic control to be risk factorsfor the development of peri-implant disease. On theother hand, and contrary to other studies, thenumber of maintenance visits did not seem toprevent or reduce the incidence of peri-implantdisease.
Koldsland et al.43 reported the prevalence ofperi-implant mucositis and peri-implantitis ina population of 109 participants followed for up to10 years. The authors presented their findings at theparticipant and implant levels. The prevalence of
peri-implantitis varied from 11.3% to 47.1% forparticipants depending on the severity of the dis-ease, which was assessed according to the extent ofPD (‡4 or ‡6 mm) and radiographic marginal boneloss (‡2 or ‡3 mm).
Simonis et al.45 examined different variablesrelated to implant success in 55 participants with131 roughened-surface implants over a 7-yearperiod. The prevalence of peri-implantitis was re-ported at both implant and participant levels. Re-sults showed that 16.94% of the implants and16.36% of the participants were affected by peri-implantitis. Years of functional loading and historyof periodontitis were considered significant riskfactors for developing peri-implantitis.
Cho-Yan Lee et al.38 investigated the effect ofperiodontal condition of the host on prevalence ofperi-implantitis. A total of 60 participants wereselected from a pool of patients who received im-plant treatment in private practice. Participants witha history of periodontitis were divided into twogroups: those with at least one periodontal PD‡6 mm and those with no residual periodontalpockets at the follow-up visit. All participants wereenrolled in a strict maintenance program through-out the observation period. The findings suggestedthat a history of periodontitis, per se, is not a riskfactor for the development of peri-implantitis unlessthe periodontitis is recurrent with residual peri-odontal pockets of ‡6 mm at the follow-up exam-ination. The authors recommended that for patientswith a history of periodontitis, elimination of anyresidual periodontal pockets is essential.
Kaemmerer et al.41 reported on the prevalence ofperi-implant mucositis and peri-implantitis in 41participants with 237 moderately roughened im-plants followed for 9 years. A correlation betweenthe onset of peri-implant disease and implantloading time was not established. However, factorssuch as nicotine intake, alcohol abuse, and pre-vious radiation therapy were found to significantlyincrease the risk of developing peri-implant disease.
In a recent retrospective cross-sectional study,Rinke et al.44 described the prevalence of peri-implant diseases in 89 participants recruited fromprivate dental practices. Based on participant-related analysis, the overall prevalence rates ofperi-implant mucositis and peri-implantitis were44.9% and 11.2%, respectively. In agreement withthe findings of Karoussis et al.,42 smokers hada 31-fold higher chance for the development ofperi-implantitis than non-smokers. There was noattempt in this study to categorize smokers on thebasis of packs/day; instead, the authors defined‘‘smoker’’ as anyone who was smoking at the timeof follow-up visit or had quit smoking for <5 years.
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Regular attendance to a maintenance program wasshown to reduce the prevalence of peri-implantdisease. In addition, a history of periodontal diseaseshowed a synergistic effect in increasing the prev-alence of peri-implantitis in smokers.
Quality of StudiesThe STROBE score ranged between 5 and 10quality points (Table 3). All the included studiesmet the criteria related to describing the studysetting, periods of recruitment, diagnostic clinicalparameters, statistical methods, and the way theresults were interpreted. Only one study38 de-termined the sample size and conducted a poweranalysis calculation. Strategies to minimize poten-tial sources of bias were not clearly described in anyof the included studies, although in one article39 theuse of masked outcome assessors was reported.
Meta-AnalysisAt the participant level, the computed overallsummary estimates for the frequency of peri-im-plant mucositis and peri-implantitis were 63.4%(95% confidence interval [CI] 59.8% to 67.1%;P <0.001) (Fig. 3) and 18.8% (95% CI 16.8% to20.8%; P <0.001) (Fig. 4), respectively. At theimplant level, the summary estimates for the fre-quency of peri-implant mucositis and peri-im-plantitis were 30.7% (95% CI 28.6% to 32.8%; P<0.001) (Fig. 5) and 9.6% (95% CI 8.8% to 10.4%;P <0.001) (Fig. 6). A high heterogeneity was
demonstrated among the studyestimates (I2 = 94.9% to 99.2%; P<0.001). Sensitivity analysis re-vealed that eliminating the Roos-Jansaker et al.16 study from themeta-analysis resulted in significantchanges in the summary estimatesfor the frequency of peri-implantmucositis, with 54.1% and 15.1% atthe participant and implant levels,respectively. On the other hand, theelimination of each study in turn didnot influence the summary esti-mates for the frequency of peri-implantitis. A funnel plot was notused to assess the publication biasbecause of the small number ofincluded studies.46
Subgroup AnalysesThe calculated summary estimatefor the frequency of occurrence ofperi-implantitis in participants witha history of periodontitis was 21.1%(95% CI 14.5% to 27.8%; P = 0.06)(Fig. 7). A moderate-to-low het-
erogeneity was demonstrated across the studies. Inonly two studies,44,45 the frequency of peri-implantitiswas separately reported in smokers, and its summaryestimate was 36.3% (95% CI 18.4% to 54.2%; P =0.18) (Fig. 8). For the participants who were enrolledin supportive maintenance programs, the overall es-timated summary of the frequency of peri-implantitiswas reduced to 14.3% (95% CI 11.8% to 16.9%;P <0.001) (Fig. 9).
DISCUSSION
This systematic review and meta-analysis aims todetermine the prevalence of peri-implant diseaseand its associated risk factors in patients treatedwith oral implants. The guidelines of MOOSE19 werefollowed. The participant-based analysis showed ahigh frequency of peri-implant diseases, with 63.4%for peri-implant mucositis and 18.8% for peri-implantitis. By pooling the extracted data with theimplant as a unit of analysis, lower rates of 30.7%and 9.6% were estimated for peri-implant mucositisand peri-implantitis, respectively. A subgroup anal-ysis assessing the frequency of peri-implantitis inhigh-risk group participants revealed a small in-creased frequency of peri-implantitis among theparticipants with a history of periodontal disease.However, the use of regular supportive periodontalcare programs seemed to reduce the number ofparticipants presenting with peri-implantitis. In ad-dition, the frequency of the participants with
Table 3.
Summary of Modified STROBE Score
Item
Studies Reporting
the Item (n) References
Study designStudy setting 9 16,38-45
Participant inclusion and exclusioncriteria
6 38-41,43,44
Sample size and power calculation 1 38
Diagnostic criteria for definingperi-implant diseases
9 16,38-45
Masked assessment of outcomes 1 39
Statistical methods 9 16,38-45
ResultsCharacteristics of participants 5 38-40,43,45
Reasons for non-participation 3 16,40,45
Outcome data reported at both patientand implant level
5 16,38,40,43,45
Data reported in participants with riskfactors
7 38,39,41-45
DiscussionLimitations 7 16,38,39,41,43-45
Interpretation 9 16,38-45
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implants exhibiting peri-implantitis was significantlyhigher among smokers (36.3%), despite the limitednumber of studies reporting separate data forsmokers.
The findings of the subgroup analysis wereevaluated based on the guidelines suggested byOxman and Guyatt.47 The subgroup analysis wasplanned before conducting the search on the basisof the previously reported risk factors of peri-implant
diseases and the influence of regular maintenancecare. The difference in prevalence among the dif-ferent subgroups was not significant, but in-consistency among the studies was noted. Therefore,the present conclusions from subgroup analysis,which included a subdivision of a small number of theincluded studies, should be interpreted cautiously.
The use of participants versus implants as thestatistical unit of analysis remains an issue of
Figure 3.Meta-analysis plot of the participant-based frequency estimate of peri-implant mucositis.
Figure 4.Meta-analysis plot of the participant-based frequency estimate of peri-implantitis.
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considerable impact limiting data comparisonsamong systematic reviews. It is the view of the au-thors that the choice of the unit of analysis shoulddepend on the outcome evaluated. For example,when comparing treatment protocols or morpho-logic features of implant designs and surfaces, theimplant could be used as the unit of analysis, whereasthe participant would be a more appropriate unitof analysis in studies evaluating demographics,compliance issues, and systemic complications of
implant therapy. It is apparent that in studying thefrequency of peri-implant diseases, data based onimplants rather than participants as the unit of analysiscould underestimate the true prevalence of the con-dition.40 This is because each implant is notan independent unit, and intraparticipant correlationamong implants needs to be accounted for.48 Inaddition, the use of an implant as a statistical unitmay result in a statistically invalid estimation, par-ticularly in high-risk groups where the difference
Figure 5.Meta-analysis plot of the implant-based frequency estimate of peri-implant mucositis.
Figure 6.Meta-analysis plot of the implant-based frequency estimate of peri-implantitis.
Frequency of Peri-Implant Diseases Volume 84 • Number 11
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between an implant and a participant unit is moreapparent.
Several systematic reviews have previously re-ported on the prevalence of peri-implant dis-eases.6,13,18 In the review by Berglundh et al.,18
only half of the included studies provided data onthe presence of peri-implant diseases. The resultsshowed a frequency value of 6.47% for peri-implantitis in partially edentulous patients with theimplant as the unit of analysis. Pjetursson et al.6
evaluated implant survival and technical and bi-ologic complications of implant-supported fixedpartial dentures over 5 and 10 years of function. Atotal of 21 studies were included in the analysis,which reported a frequency of occurrence of 8.6%for peri-implantitis. It was concluded that despitethe high survival rates of implants over 5 years ofservice, considerable chair time was required for
maintenance of the prostheses. In another review,Zitzmann and Berglundh13 applied predefined clin-ical parameters to diagnose peri-implant diseasesand excluded studies that had small sample size(<50) or <5 years’ follow-up. Nine studies wereidentified,16,38-45 but the prevalence of peri-implantmucositis was reported in just one study,16 whereasthat of peri-implantitis was reported in three pop-ulation samples;16,26,40 no meta-analysis was per-formed. The results were presented at both theparticipant and implant levels, with 80% of theparticipants and 50% of the implants exhibitingperi-implant mucositis. The rates of occurrence ofperi-implantitis ranged between 28% and ‡56% ofparticipants and 12% and 43% of implant sites.
The present systematic review attempts a morerigorous approach to substantiate its findings com-pared with the aforementioned reviews. Initially, an
Figure 7.Meta-analysis plot of the frequency estimate of peri-implantitis in participants with a history of periodontitis.
Figure 8.Meta-analysis plot of the frequency estimate of peri-implantitis in smokers.
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extensive search strategy that included unpublishedtrials and manual searching of relevant journals wasused. Further, known methodologic guidelines (i.e.,MOOSE) meeting strict inclusion criteria and as-sessing the quality of the included studies were fol-lowed. In addition, standardized diagnostic criteriadefining peri-implant disease were applied to allselected studies. This helped in minimizing hetero-geneity among the studies and allowed the use ofmeta-analysis to calculate a summary estimate ofthe frequency of peri-implant diseases. On the otherhand, the meta-analytic findings may need to becautiously interpreted owing to the limited number ofpotentially relevant studies included in the analysis.Variation in study design, implant systems used, andduration of follow-up periods remains an inherentlimitation that needs to be acknowledged, as doesthe lack of standardization in reporting outcomes atboth participant and implant levels. Another limi-tation came from restricting the search to English, asrelevant studies may have been published in otherlanguages. The modified tool that assessed thequality of reporting of the studies, albeit not fullyvalidated, was based on a validated assessment tool.The modified version was proposed due to the lackof a standardized assessment tool for evaluatingthe quality of non-randomized studies.
Sensitivity analysis is often performed to evaluatethe robustness of the overall effect estimate by ex-cluding a study that is considered an outlier andevaluating its influence on the overall outcome ofthe review.49 In the present review, sensitivity anal-yses show that one study16 may have overestimatedthe calculated frequency of peri-implant mucositisat both the participant and implant levels. The lackof standardized supportive maintenance care may
have resulted in the reported high percentage ofparticipants and implants with peri-implant diseases.The maintenance care was carried out by the referringdentists, and records have shown that participantsattend visits only when prosthodontic maintenanceis required.
Contrary to previous reports and reviews,16,42,50
the present systematic review shows that historyof periodontitis did not significantly increase theoccurrence of peri-implantitis. However, the sum-mary estimate of frequency of peri-implantitis amongthe participants that had regular maintenance pro-cedures was considerably reduced. In one study,44
the frequency of peri-implantitis among participantswith a history of periodontal disease was comparableto that of those without a history of periodontal dis-ease. The authors attributed the favorable resultsto the effect of regular maintenance and showed thatthe lack of such a supportive care program increasedthe risk of peri-implant disease by 11-fold. The im-portance of supportive periodontal maintenancecare was further demonstrated in another review51
that concluded that supportive periodontal therapycan maintain moderately rough implants in peri-odontally compromised patients.
Considering that >2 million oral implants are placedannually,20 peri-implant disease can affect more thanhalf a million implants each year. Therefore, cliniciansand patients must be prepared to accept long-term,regular maintenance care to identify early signs ofthe disease and develop treatment strategies, partic-ularly for those at high risk. Although the relationshipbetween peri-implant mucositis and peri-implantitisis still not fully understood, regular follow-up caremay also allow early intervention that may halt thepotential progression of peri-implant mucositis into
Figure 9.Meta-analysis plot of the frequency estimate of peri-implantitis in participants who received supportive periodontal care.
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peri-implantitis. The usefulness of meta-analysis issignificantly enhanced as the number of studiessuitable for inclusion increases; to this end, re-searchers and clinicians should be strongly en-couraged to adhere to standardized guidelines forreporting observational and clinical data and useprecise and clear diagnostic criteria that may allowa better understanding of the overall effect of peri-implant diseases.
CONCLUSIONS
Within the limitations of this systematic review andmeta-analysis, there is a relatively high occurrenceof peri-implant diseases that can manifest andpersist for years. Long-term maintenance care forhigh-risk groups is essential to reduce the risk ofperi-implantitis. Informed consent for patients re-ceiving implant treatment must include the need forsuch maintenance therapy.
ACKNOWLEDGMENT
The authors report no conflicts of interest related tothis review.
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Correspondence: Dr. Momen A. Atieh, Oral ImplantologyResearch Group, Sir John Walsh Research Institute,Department of Oral Sciences, Faculty of Dentistry,University of Otago, 310 Great King Street, Dunedin9016, New Zealand. E-mail: [email protected].
Submitted October 3, 2012; accepted for publicationNovember 14, 2012.
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