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Andrea Mombelli The epidemiology of peri-implantitis

Nada Muller
Norbert Cionca

Authors affiliations: Key words: epidemiology, peri-implantitis, prevalence, review, risk factors
Andrea Mombelli, Nada Muller, Norbert Cionca,
School of Dental Medicine, Division of
Periodontology and Oral Pathophysiology, Abstract
University of Geneva, Rue Barthelemy-Menn 19, Aim: To review the literature on the prevalence and incidence of peri-implantitis.
CH-1205, Geneva, Switzerland
Methods: Out of 322 potentially relevant publications we identified 29 articles concerning 23
Corresponding author: studies, with information on the presence of signs of peri-implantitis in populations of at least 20
Andrea Mombelli cases.
School of Dental Medicine
Division of Periodontology and Oral Results and conclusions: All studies provided data from convenience samples, typically from
Pathophysiology patients who were treated in a clinical center during a certain period, and most data were cross-
University of Geneva sectional or collected retrospectively. Based on the reviewed papers one may state that the
Rue Barthelemy-Menn 19
CH-1205 Geneva, Switzerland prevalence of peri-implantitis seems to be in the order of 10% implants and 20% patients during 5
Tel.: +41 22 379 40 30 10 years after implant placement but the individual reported figures are rather variable, not easily
Fax: +41 22 379 40 32 comparable and not suitable for meta-analysis. Factors that should be considered to affect
e-mail: andrea.mombelli@unige.ch
prevalence figures are the disease definition, the differential diagnosis, the chosen thresholds for
Conflict of Interest and Source of Funding Statement: probing depths and bone loss, differences in treatment methods and aftercare of patients, and
The authors declare that they have no conflict of
interests. The study was self-funded by the authors and dissimilarities in the composition of study populations. Smoking and a history of periodontitis have
their institution. been associated with a higher prevalence of peri-implantitis.

Missing teeth can be replaced successfully consequences of this problem. At least in


with reconstructions anchored on osseointe- part this may be due to different interpreta-
grated implants. Several narrative and sys- tions and definitions of disease states and dif-
tematic reviews are available reporting the ferences in study populations.
survival of implants in relation to subject-
specific factors such as tobacco smoking, sys- What is peri-implantitis?
temic diseases, or periodontitis (Mombelli & Peri-implantitis (or Periimplantitis) has
Cionca 2006; Schou et al. 2006; Karoussis been introduced as a term for infectious path-
et al. 2007; Klokkevold & Han 2007; Quirynen ological conditions of peri-implant tissues
et al. 2007; Ong et al. 2008; Bornstein et al. more than two decades ago (Levignac 1965;
2009; Heitz-Mayfield & Huynh-Ba 2009; Safii Mombelli et al. 1987). At the 1st European
et al. 2010). The total literature available Workshop on Periodontology in 1993 it was
today suggests that over a period of 10 years agreed that this term should be used specifi-
roughly 1 of 20 implants is lost. A meta- cally for destructive inflammatory processes
analysis of five suitable studies (Hardt et al. around osseointegrated implants in function
2002; Karoussis et al. 2003; Mengel & that lead to peri-implant pocket formation
Flores-de-Jacoby 2005; Mengel et al. 2007; and loss of supporting bone (Albrektsson &
Gatti et al. 2008) revealed that the odds for Isidor 1994). The definition implied that ini-
implant survival were significantly higher in tial healing had been uneventful and osseoin-
subjects without than with a history of peri- tegration was achieved as anticipated. Hence,
odontal disease (Safii et al. 2010). Greater bone loss following implant installation due
than the risk for total implant failure are, to remodeling had to be distinguished from
however, the odds that a technical complica- bone loss due to a subsequent infection.
tion (Pjetursson et al. 2007) or an inflamma- The typical signs and symptoms of peri-
Date:
Accepted 09 June 2012 tory condition of the peri-implant tissues implant mucositis and peri-implantitis were
may arise. The incidence of peri-implant discussed in the context of consensus confer-
To cite this article:
Mombelli A, Muller N, Cionca N. The epidemiology of diseases is currently a controversial issue. ences on several occasions and have been
peri-implantitis defined (Mombelli 1994, 1999; Lindhe et al.
Conflicting statements have been made with
Clin. Oral Implants Res. 23(Suppl. 6), 2012, 6776
doi: 10.1111/j.1600-0501.2012.02541.x regards to the magnitude and the long-term 2008; Zitzmann & Berglundh 2008; Lang

2012 John Wiley & Sons A/S 67


Mombelli et al  Epidemiology of peri-implantitis

et al. 2011). The inflammation causes bleed- What is not peri-implantitis? definition can be improved by applying a par-
ing and/or suppuration upon gentle probing Although formation of pockets, bleeding on asite density threshold and by excluding a
with a blunt instrument. The marginal tissue probing (BOP), suppuration, and loss of bone number of other medical conditions (Bejon
may be swollen or red, these characters are, belong to the disease-defining clinical signs et al. 2007). We suspect that the same prob-
however, not always clearly visible. Unless of peri-implantitis, increased peri-implant lem exists with regards to peri-implantitis
the access to the lesion is obstructed, a peri- probing depth (PPD), BOP, or peri-implant and that the prevalence of peri-implantitis
odontal probe can be advanced 4 mm or more bone loss, as single features are not sufficient may have been over-estimated by some
into the peri-implant sulcus. Pain is usually for the diagnosis of peri-implantitis. Bone authors. Because prevalence and incidence of
not recorded. The typical bone defect is cra- resorption can also be caused by the deep any disease depends on the disease-defining
ter-like, runs all around the implant, and is insertion of an implant (Hammerle et al. criteria, the primary objective of this article
strictly demarcated. As perfect osseointegra- 1996) or the placement of implants too close is to discuss the prevalence and incidence of
tion is maintained apically to the defect, to each other (Tarnow et al. 2000). In the peri-implantitis in the context of the diagnos-
bone destruction can progress without any case of two-piece implants, abutment instal- tic aspects and their differential diagnosis.
notable signs of implant mobility. Mobility lation has been associated with subsequent
therefore indicates complete loss of osseoin- bone remodeling that may be unrelated to
tegration and is a sign of total failure (Mom- infection (Adell et al. 1981). In such cases, Material and methods
belli & Lang 1998). marginal bone loss is commonly limited to
Using the experimental gingivitis model the first few weeks after abutment connec- Search strategy
(originally described by Loe et al. 1965), a tion and is not necessarily the initial stage of On December 7, 2011 we searched the US
cause and effect relationship between biofilm peri-implantitis. Long-term monitoring of National Institutes of Health free digital
formation on implants and peri-implant mu- implant performance should therefore not be archive of biomedical and life sciences jour-
cositis can be demonstrated (Pontoriero et al. based on radiographs taken directly after nal literature (PubMed) to identify all articles
1994; Zitzmann et al. 2001). An attractive implant placement, but should rather relate that included the following terms in the
extrapolation of these findings is the hypoth- to documents obtained once tissue homeosta- title:
esis that bacterial biofilm on implant sur- sis has been established (i.e. upon the com- peri-implantitis OR periimplantitis
faces causes peri-implantitis, and that the pletion of the prosthodontic work). OR biological complication* OR peri-
removal of these bacteria is the remedy. Ben- Moreover, not every probing depth of over implant disease
eficial effects of mechanical debridement and 3 mm is a definite sign of peri-implantitis. In addition, we searched previous review
systemic antibiotics in cases diagnosed with The type and shape of the implant, the con- articles on the subject as well as the refer-
peri-implantitis supported this hypothesis nection parts, and the prosthetic suprastruc- ence lists of the articles already identified for
early (Mombelli & Lang 1992). However, ture affect the dimensions of the peri- further potentially relevant publications.
based on all data available up to 2008, it was implant tissues. Soft tissue conditioning in This initial search was designed for high
concluded that the predictability of such the esthetic zone to create the illusion of an recall rather than high precision. Although
treatment was limited and influenced by fac- interdental papilla can lead to an increase in there was no language restriction, the mini-
tors not yet fully understood (Claffey et al. the distance from the implant shoulder to mum requirement was access to an English
2008; Lindhe et al. 2008; Renvert et al. 2008). the mucosal margin up to 5 mm (Gallucci version of the title.
As we have pointed out in a recent article on et al. 2011). Combined with a mucositis and
the role of biofilms in peri-implant diseases marginal bone remodeling due to deep posi- Study selection criteria
(Mombelli & Decaillet 2011), one needs to tioning of the implant, such a situation could To be eligible for inclusion in the review,
consider the possibility that bacterial peri- be misdiagnosed as peri-implantitis. reports had to provide data in humans from
implant infections may also arise occasion- Whenever key disease-defining signs on dental implants with peri-implantitis. The
ally as a consequence of non-microbial their own are insufficient for a diagnosis, the study selection criteria were:
events favoring the emergence of a patho-
genic microbiota. As an example, the fracture
prevalence or incidence of the disease cannot
be estimated accurately using the frequencies
Includes at least 20 human subjects with
dental osseointegrated implants.
of an implant can give rise to a secondary
bacterial infection, and thus provoke puru-
of the single signs. This problem has been
addressed in other medical disciplines, and
Implants were in service without compli-
cations for at least one year.
lent peri-implant disease. Another example is
peri-implant infection due to submucosal
far-reaching consequences of invalid clinical
conclusions have been shown. As an exam-
Describes a pathological condition com-
patible with the definition of peri-im-
persistence of luting cement, where the pres- ple, the case definition of malaria comprises
plantitis.
ence of a foreign body gives rise to a bacterial
infection. In one study (Wilson 2009) excess
a set of clinical and laboratory parameters
combined with the presence of Plasmodium
Quantitative data for signs of peri-implan-
titis, such as PPD, BOP+, suppuration,
dental cement was associated with clinical falciparum parasitemia. While these criteria
bone loss, are presented.
and/or radiographic signs of peri-implant dis-
ease in 81% of 39 cases. Once the excess
are sensitive in diagnosing severe malaria,
they are also present in other serious ill-
Cases are not selected initially based on
the presence of a peri-implant pathology.
cement was removed, the clinical signs of nesses. As asymptomatic parasitemia is com-
disease disappeared in 74%. The differential mon in malaria-endemic areas, patients Three independent reviewers (AM, NM,
diagnosis of peri-implantitis should therefore fulfilling World Health Organization criteria NC) screened titles and abstracts of the
include the search for a specific underlying for severe malaria often have disease attribut- search results. The full text of all studies of
cause, even if suppuration, or the presence of able to another cause (Anstey & Price 2007). possible relevance was obtained for assess-
a biofilm points to a bacterial infection. For malaria, the specificity of the case ment against the stated inclusion criteria.

68 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776 2012 John Wiley & Sons A/S
Mombelli et al  Epidemiology of peri-implantitis

Any disagreement regarding inclusion was graphs exceeding certain levels (expressed as Peri-implantitis, defined as presence of
resolved by discussion. millimeters from a landmark, such as the PPD > 4 mm and BOP+, was diagnosed at 10
implant shoulder, or as the exposure of two, (10%) implants. If the threshold for definition
Data extraction and synthesis of extracted three or more threads of the screw helix). In of peri-implantitis was set at PPD > 5 mm
evidence several articles, frequencies of individual and BOP+ the incidence at the implant level
A preliminary review of the literature
parameters were recorded separately, but it was 5%. The same patients were included in
revealed considerable heterogeneity of criteria
was not reported to what extent the disease- a later analysis on the incidence of biological
utilized to define peri-implantitis. In view of
defining criteria were found simultaneously complications at 160 implants in 89 partially
the issues deliberated in the introduction we
at the same sites. Some sites may, however, edentulous subjects during 812 years of
decided to tabulate the data where appropri-
be bleeding without bone loss, while others maintenance after implant placement (Brag-
ate and report the findings in a narrative
may show bone loss unrelated to infection. ger et al. 2005). The threshold to define a bio-
manner.
The frequency of peri-implantitis could not logical complication was a probing pocket
The following information was sought:
be determined explicitly due to failure of depth of 5 mm and BOP or pus secretion.
Study design, number of cases, implant type,
using a composite disease definition in Study Twenty-four instances of peri-implantitis
type of data and disease definition, sub-
2 (Baelum & Ellegaard 2004) and Study 8 were diagnosed in total and intercepted with
groups if any (risk factors), length of follow-
(Fransson et al. 2005). therapy. Seven implants were lost because of
up, number of diseased cases according to the
biological failures.
disease definition.
Studies Study 4 (Corbella et al. 2011): Sixty-one
Study 1 (Astrand et al. 2004): This prospec- patients with 244 immediately loaded
Results tive split-mouth study included 28 patients implants, supporting mandibular and maxil-
treated in the maxilla with a total of 150 lary full-arch prostheses, were included in a
Included studies implants of two different types in five cen- structured maintenance program. Peri-im-
The initial search yielded 321 potentially rel- ters. Twenty-five percent were smokers, 29% plantitis was defined as PPD > 3 mm plus
evant publications. Two hundred and eighty had a history of periodontal disease. After Bleeding index > 1. Two patients lost a total
nine of them, however, failed to satisfy the 3 years two implants of each type were lost. of three implants due to peri-implantitis. No
study selection criteria. The main reason for Peri-implantitis, defined as infection includ- further instances of peri-implantitis were
non-inclusion was that articles did not con- ing pus and bone loss, was found at 5% reported thereafter. The number of cases/
cern at least 20 human subjects with dental implants in an undisclosed number of sub- implants with more than 3 years follow-up
osseointegrated implants. The second most jects. Six of the seven implants with peri-im- was too small for a meaningful long-term
frequent reason was that cases with peri- plantitis were found in patients with a analysis.
implant pathology were selected deliberately. history of periodontitis, and all implants had Study 5 (Dierens et al. 2012): From a total
Of the 32 articles that seemed to meet all the same implant surface (TPS). of 134 patients with 166 single-tooth
study selection criteria five additional ones Study 2 (Baelum & Ellegaard 2004): This implants, 50 subjects with 59 remaining
were excluded during data extraction: One case series included all 258 implants inserted implants were examined after 1622 years.
(Feloutzis et al. 2003) was not about peri-im- in 128 subjects in a private periodontal prac- Reasons for the unavailability of subjects
plantitis; one (Laine et al. 2006) selected tice during 14 years. Ten-year data were pre- were multiple, mostly administrative or
patients with or without peri-implantitis sented for 19 two-stage, and 41 one-stage unwillingness to participate, but also due to
intentionally; three (Lekholm et al. 1986, implants. All patients had received extensive death (3%) or loss of all implants (5%). Three
1996; Merickse-Stern et al. 2001) did not pro- periodontal treatment prior to implant place- implants, each in a different subject, showed
vide peri-implantitis prevalence data. Two ment and were maintained at a high standard bone loss extending over the third implant
additional studies, one not initially identified of oral hygiene. Sixty-five percent were thread (>2.7 mm) with BOP + .
(Astrand et al. 2004), and one becoming avail- smokers at the time of implant placement. Study 6 (Dvorak et al. 2011): One hundred
able shortly after the search (Dierens et al. Ten-year survival rates were 97% and 78%, and seventy seven women with 828 dental
2012), were added. depending on implant type. After 10 years, implants in situ since more than one year
For the final evaluation 29 articles, report- 21% of the two-stage and 40% of the one- were investigated cross-sectionally at age
ing data from 23 studies could be included. stage implants showed bone loss  1.5 mm, 63 9 years. If there was bleeding on peri-
They are listed in Table 1 and are presented but only 5% and 14% at the 3.5 mm thresh- implant probing and/or suppuration together
narratively below in alphabetic order. The old. Twenty-three percent of the two-stage with a PPD > 5 mm and radiographic bone
selected studies all reported data from conve- and 25% of the one-stage implants showed loss the subject was diagnosed as having peri-
nience samples, typically all patients treated probing depth > 5 mm. Ninety percent of the implantitis. Twenty-seven of 115 healthy
in a clinical center during a certain period two-stage and 69% of the one-stage implants subjects, four of 16 subjects with a diagnosis
and satisfying certain inclusion criteria. showed BOP. The description was on the of osteopenia, and 11 of 46 subjects with
level of the implant. The frequency of peri- osteoporosis were diagnosed with peri-im-
Case definition implantitis could not be determined due to plantitis. The over-all prevalence of peri-im-
In general, the retained articles described ele- lack of composite disease definition and plantitis was 24% without significant
ments, or combinations of elements of the according data. differences between groups.
disease-defining signs of peri-implantitis and Study 3 (Bragger et al. 2001): This case ser- Study 7 (Ferreira et al. 2006): Two hundred
their frequency, most notably the frequency ies includes 48 patients with 103 implants and twelve partially edentulous subjects
of BOP (BOP+), PPD above certain thresholds, examined after 45 years of function (105 rehabilitated with 578 osseointegrated
or vertical loss of bone as visible on radio- implants were placed, two were lost early). implants of three different brands were exam-

2012 John Wiley & Sons A/S 69 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
Mombelli et al  Epidemiology of peri-implantitis

Table 1. Publications addressing the incidence or prevalence of peri-implantitis from 23 studies


Peri-implantitis
Incidence/
References Study design n I type Disease definition Risk factors Follow-up prevalence Comments
Astrand Prospective C: Branemark, ITI SUP plus BL n 25% smok 3 yrs C: nd All I with peri-implantitis had
et al. split-mouth 28 TPS 29% PCP I: 5% TPS surface
(2004) I:
150
Baelum & Prospective C: Astra, ITI PPD, BOP, BL 65% smok 014 yrs nd Analysis on implant level
Ellegaard case series 128 No composite
(2004) I: disease definition
258
Bragger Retrospective C: ITI PPD > 4 plus BOP+ 5 yrs C: 10% If the threshold was PPD > 5
et al. case series 48 I: 10% and BOP+ the incidence was
(2001) I: 5% (I)
103
Bragger Prospective C: ITI PPD > 5 plus BOP+/ 812 yrs 24 instances of Periimplantitis as part of
et al. case series 89 SUP peri-implantitis biological complication.
(2005) I: Includes C from Bragger et al.
160 (2001)
Lee et al. Retrospective C: Straumann PPD > 4 plus BOP+ 50% PCP 8 yrs C: 37% PCP, 54% for C with residual
(2012) case series 60 TPS, SLA 17% PHP pockets
I: I: 27% PCP,
117 13% PHP
Corbella Prospective C: Undisclosed PPD > 3 plus 49% smok 6 m5 yrs C: 3% Short mean observation time
et al. case series 61 Bleeding index > 1 I: 1.4% (mean 18.3 m). Only full-arch
(2011) I: rehabilitations
244
Dierens Cross- C: Branemark BL > 3 threads plus 1622 yrs C: 6% Available subset of 134 C with
et al. sectional 50 BOP+ I: 5% 166 single-tooth I
(2012) I: 59
Dvorak Cross- C: Nobel PPD > 5 plus BOP+ 26% 6 yrs C: 24% Includes only postmenopausal
et al. sectional 177 plus BL osteoporosis, I: 13% women
(2011) I: 9%
828 osteopenia
Ferreira Cross- C: Nobel, 3i, PPD > 4 plus BOP+/ 14% PCP Mean C: 9% Periodontitis and diabetes
et al. sectional 212 Intra-lock SUP plus BL loading I: 7% associated with increased risk
(2006) I: time of peri-implantitis
578 42.5 m
Fransson Retrospective C: Branemark Progressive BL. No 5 yrs C: 28% Threshold level: position
et al. case series 662 composite disease I: 12% located about 3 mm apical to
(2005) I: definition the abutment-fixture
3413 junction
Gatti et al. Prospective C: Nobel, PPD > 5 mm plus 53% PCP 5 yrs C: 3%
(2008) case series 62 Zimmer, pus or other sign of I: 1%
I: Mathys, infection plus
227 Straumann, BL > 2 mm
Friadent
Gruica Prospective C: ITI SUP plus BL 29% smok 815 yrs C: 19% Heavy smok I: 40%, light smok
et al. case series 180 I: 17% I: 17%, never and former
(2004) I: smok I: 13% I with
292 complications
Karoussis Prospective C: ITI PPD > 4 plus BOP+/ 15% PCP 10 yrs C: nd Prevalence associated with
et al. case series 53 SUP plus BL I: 29% PCP, 6% smok
(2003) I: PHP
112
Koldsland Cross- C: Astra Tech, PPD > 4 or > 5 plus 8.4 yrs C: 1147% Different levels of severity
et al. sectional 109 Branemark, BOP+/SUP plus BL I: 537% assessed on C and I level
(2010) I: Straumann, 3i
372
Maximo Prospective C: Branemark PPD > 4 plus BOP+/ 19% smok Undisclosed C: 12%
et al. case series 113 SUP plus BL  3 I: 7%
(2008) I: threads
374
Rinke et al. Retrospective C: Ankylos PPD > 4 plus BOP+/ 19% smok, 211 yrs C: 11% Smok and PCP C: 53%, non-
(2011) case series 89 SUP plus BL 72% PCP I: nd smok and PHP C: 3%
I: nd
Roccuzzo Prospective C: Straumann Antibiotic/surgical 37% PCP 10 yrs C: 11% PHP,
et al. case series 101 TPS therapy according to 27% moderate
(2012) I: the CIST protocol PCP, 47% severe
228 PCP
Rodrigo Prospective C: Straumann PPD > 3 plus BOP+ 36% smok, 5 yrs C: nd
et al. case series 22 SLA plus BL > 3xSD of 68% PCP I: 6%
(2011) I: 68 repeated measures

70 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776 2012 John Wiley & Sons A/S
Mombelli et al  Epidemiology of peri-implantitis

Table 1. (continued)
Peri-implantitis
Incidence/
References Study design n I type Disease definition Risk factors Follow-up prevalence Comments
Roos- Retrospective C: Branemark BL  3 threads 26% smok, 914 yrs C: 16% Different levels of severity
Jansaker case series 218 following 1st year no I: 7% assessed on C and I level
et al. I: plus BOP+/SUP maintenance
(2006b) 999 care
Rutar et al. Retrospective C: ITI PPD > 4 plus BOP+/ 38% smok 510 yrs C: nd
(2001) case series 45 SUP plus BL I: 23%
I: 64
Schmidlin Retrospective C: PPD > 5 plus BOP+/ 322 yrs C: nd
et al. case series nd SUP plus BL I: 13%
(2010) I: 39
Simonis Retrospective C: Straumann PPD > 4 plus BOP+ 16% smok, 10 yrs C: nd
et al. case series 55 TPS plus BL  2.5 mm/ 26% PCP I: 38% PCP,
(2010) I:  3 threads 11% PHP
131
Wahlstrom Retrospective C: Astra Tech Color and shape of 11% smok, 5 yrs C: 4% 80% teeth lost due to
et al. case series 46 Nobel mucosa; PPD > 3 all PCP I: nd periodontal disease, 29% C
(2010) I: plus BOP+ plus mean bone loss 1/32/3 of
116 BL > 2 mm root length
Zetterqvist Prospective C: 3i PPD > 5 plus BOP+/ 5 yrs C: 1%
et al. RCT 112 SUP plus plus BL > 5 I: <1%
(2010) I:
304

Abbreviations:
BL: Bone loss, BOP: Bleeding on probing, C: Case, I: Implant, smok: Smoking, nd: Not determined, PCP: Periodontally compromised patient, PHP: Periodon-
tally healthy patient, PPD: Pocket probing depth, SUP: Suppuration, yrs: Years, m: Months

ined between 6 and 5 years after placement. BOP+, suppuration, recession and Study 10 (Gruica et al. 2004): Clinical
Peri-implantitis, defined as the presence of PPD > 5 mm. Smokers had larger numbers of charts of 180 consecutively admitted patients
PPD > 4 mm in association with peri- affected implants than non-smokers (Frans- with 292 implants in function for about 8
implant bleeding and/or suppuration, with son et al. 2008). In 182 subjects, 419 of 1070 15 years were analyzed with respect to the
radiographic confirmation of bone loss, was examined implants exhibited peri-implanti- occurrence of biological complications,
detected in 19 cases (9%). As the time since tis-associated vertical bone loss > 2 mm. defined as clinical conditions with suppura-
implant placement was highly variable, the The proportion of affected implants varied tion from the peri-implant sulcus, develop-
prevalence at a given time point could not be between 30% and 52% in different jaw posi- ment of a fistula, or peri-implantitis with
determined. Presence of periodontitis and dia- tions and the most common position was the radiologic bone loss. Fifty-one implants in 34
betes were statistically associated with lower front region (Fransson et al. 2009). patients showed late infectious biologic com-
increased risk for peri-implantitis. Study 9 (Gatti et al. 2008): Sixty-two par- plications. Fifty-three subjects were smokers.
Study 8 (Fransson et al. 2005): Radiographs tially edentulous patients were consecutively Heavy smokers had 40%, light smokers had
of 662 subjects with 3413 implants, support- enrolled in this study. One hundred and 17%, and never and former smokers had 13%
ing fixed dentures or single crowns, with a twenty-nine implants were placed in 26 implants with complications.
documented function time of at least 5 years, patients with a history of severe periodonti- Study 11 (Karoussis et al. 2003): Fifty-three
were analyzed. Four hundred and twenty tis, 26 implants in seven subjects with a his- patients with 112 implants were assessed
three implants (12%), distributed in 184 tory of mild periodontitis, and 72 in 29 after 10 years of regular supportive periodon-
(28%) subjects, had one or more implants periodontally healthy subjects. Patients tal therapy. Eight subjects with a history of
with progressive bone loss to a level of three requiring periodontal treatment were treated chronic periodontitis lost 2 of 21 implants,
or more threads including detectable bone prior to implantation. At 5 years, six the remaining 45 periodontally health sub-
loss after the first year in function. The prob- patients, two from each group, had dropped jects lost 3 of 91 implants. When peri-im-
ability for subjects to exhibit bone loss was out. In the severe periodontitis group, two plantitis was defined as PPD > 4 mm plus
not influenced by age, gender, type of con- implants in one patient failed due to peri-im- BOP+ or suppuration 29% of the implants in
struction, function time, or maxillary/man- plantitis, and two implants in another patient periodontally compromised patients, and 6%
dibular position of the implants. The number were successfully treated for peri-implantitis. in periodontally health subjects were diag-
of implants per subject, however, had a sig- The criteria to define peri-implantitis were nosed with peri-implantitis. The analysis was
nificant impact. Peri-implantitis was not loss of > 2 mm of marginal bone from the per implant.
explicitly identified on the basis of a compos- last radiographic assessment, in the presence Study 12 (Koldsland et al. 2010): Three
ite disease definition. Some subjects with of pus or another sign of infection and hundred and seventy-two solid screw
progressive bone loss were further character- PPD > 5 mm. Patients affected by severe or implants of four different brands in 109 sub-
ized into two additional publications: In a moderate periodontitis had lost 2.6 mm peri- jects were examined 8.4 years (SD: 4.6 years)
subset of 82 subjects, implants with pro- implant bone over 5 years on average; after functional loading. Peri-implantitis was
gressive bone loss were more likely to show healthy subjects lost 1.2 mm. assessed using the following criteria: clinical

2012 John Wiley & Sons A/S 71 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
Mombelli et al  Epidemiology of peri-implantitis

signs of inflammation, presence of BOP, Study 16 (Roccuzzo et al. 2012): One hun- radiographically after 914 years of function
radiographic peri-implant bone loss at or dred and one partially edentulous subjects (65% of the patients and 60% of the implants
above 2 or 3 mm, PPD > 3 mm, or were examined 10 years after implant place- had a follow-up of 11 years or more). The
PPD > 5 mm. Depending on the combina- ment and fixed prosthodontic therapy. subjects were not enrolled in a structured
tions and threshold levels used for bone loss Twenty-eight periodontally healthy subjects maintenance care program. In this study the
and PPD, the prevalence of peri-implantitis received 61 implants. Thirty-seven subjects prevalence of peri-implantitis was estimated
varied between 11% (12 subjects presenting with moderate periodontal disease, and 36 using various levels of clinical and radio-
19 (5%) implants with PPD > 5 and > 2 mm subjects with advanced periodontal disease, graphic criteria: 48% of the implants had a
bone loss) and 47% (49 subjects presenting received 95 and 90 implants, respectively. At PPD > 3 mm and BOP+, but no concomitant
108 (37%) implants with signs of inflamma- the end of active periodontal treatment, bone loss, which was interpreted as presence
tion and detectable loss of bone). The peri- patients were asked to follow an individual- of peri-implant mucositis. This concerned
implant tissues of 249 (71%) implants were ized supportive periodontal therapy program. 77% of the subjects. If peri-implantitis was
judged to be inflamed (mBI score > 0 and/or The diagnosis and treatment of peri-implant defined as exposure of three or more threads
BOP or suppuration). This concerned 88 sub- biological complications was carried out (corresponding to at least 1.8 mm vertical
jects (82%). Supplementing information on according to cumulative interceptive support- loss of bone following the first year in func-
the same patients was provided in an addi- ive therapy (CIST) (Mombelli & Lang 1998). tion) together with BOP+ and/or suppuration,
tional publication (Koldsland et al. 2011): Eighteen implants were removed due to bio- then the prevalence of peri-implantitis was
Multi-level statistical analyses identified logical complications (two, seven, nine 16% on the level of the patient and 7% on
location in the maxilla as risk indicator for implants in the three groups, respectively). the level of the implant. Bone levels were
detectable peri-implantitis. Gender (male) During the 10 years, antibiotic and/or surgi- associated with the presence or absence of
and history of periodontitis were identified as cal therapy was performed in 11%, 27%, and keratinized mucosa at implants. On the
risk indicators for overt peri-implantitis. 47% cases, respectively, significantly more in patient level, smoking was associated with
Study 13 (Lee et al. 2012): This retrospec- severely compromised than healthy patients mucositis, bone level, and peri-implantitis.
tive case study included 30 periodontally (P = 0.002). At the final examination, the per- Peri-implantitis was related to a history of
compromised patients with 56 implants and centage of implants with at least one site periodontitis.
30 periodontally healthy subjects with 61 with a PPD > 5 mm was, respectively, 2%, Study 19 (Rutar et al. 2001): Forty-five par-
implants. The groups were matched for age, 16%, and 27%, with a statistically significant tially edentulous patients (mean age:
gender, implant characteristics, and smoking difference between healthy and compromised 51 years, range: 2783 years), with a total of
(three smokers in each group). At follow-up subjects. 64 implants participated in this retrospective
at 8 years (range 514) the prevalence of Study 17 (Rodrigo et al. 2011): Five years analysis. The subjects had been enrolled in a
implants with PPD > 4 mm and BOP+ was after implant loading, clinical and radiograph- maintenance care program during 510 years
27% in periodontally compromised and 13% ical variables were recorded in 22 implant between implant installation and examina-
in periodontally healthy subject (37% vs. patients of a private clinic. Patients were not tion. During this time, nine implants experi-
17% patients). Patients with residual pockets included if presenting with untreated peri- enced one episode and an additional six
had a prevalence of 54%. The prevalence of odontitis, inappropriate periodontal mainte- implants two episodes of peri-implantitis. In
bone loss > 3 mm was 17% and 7% at the nance, or with a systemic or local disease. a patient with a history of diabetes, one of
level of the patients, and 9% and 3% at the Thirty-six percent were smokers, 68% were these implants was lost due to extensive
level if the implants, respectively. periodontally treated. Each subject received bone loss. With this exception, all episodes
Study 14 (Maximo et al. 2008): One hun- at least one post-extraction immediate of peri-implantitis were successfully treated
dred and thirteen individuals with 347 implant (34 implants in total) and one employing the principles of the CIST proto-
implants in function for at least 1 year were delayed implant (34 implants). During the col. At examination, 42 implants (66%)
enrolled in this study. The time since follow-up period, 9 of the 22 participants showed a PPD > 4 mm. All 15 implants with
implant placement or loading was undis- (40%) showed signs of biological com- a history of peri-implantitis belonged to this
closed. Twenty-six implants (7%), distributed plications: mucositis (PPD > 3 mm, BOP+, group. The insertion of paper points into the
in 14 (12%) subjects were diagnosed with without significant bone loss) was diag- sulcus for microbiological sampling induced
peri-implantitis, defined as presence of nosed at 13 (20%) implants, peri-implantitis bleeding in 80% of the implants.
PPD > 4 mm with BOP+ and/or suppuration (PPD > 3 mm, BOP+, vertical bone loss years Study 20 (Schmidlin et al. 2010): Thirty-
and radiographic bone loss of three or more 15 > 3x the standard deviation of repeated nine single crowns on implants were reexam-
threads. measures) at four (6%) implants. There was ined in an undisclosed number of patients
Study 15 (Rinke et al. 2011): Data from 89 no difference between groups. Once these with treated chronic periodontitis after a
patients were analyzed 5.7 2.1 years after conditions were diagnosed they were imme- highly variable observation time ranging from
implant placement. The patient-related pre- diately treated according to the CIST proto- 3 to 22 years. Five implants were diagnosed
valence rate of peri-implantitis, defined as col, with success in all cases except one, with peri-implantitis (PPD > 5 mm and BOP
PPD > 4 mm, BOP+ and/or pus, with radio- where one delayed implant showed signs of + or suppuration). The cumulative risk of
graphic bone loss, was 11%. No disease was persisting peri-implantitis (deep PPD and pro- peri-implantitis after 10 years was calculated
diagnosed in non-smoking patients without a gressing loss of bone). to be 18% (95% CI 6.940.9).
history of periodontal disease and with a Study 18 (Roos-Jansaker et al. 2006a,b,c): Study 21 (Simonis et al. 2010): Fifty-five
good compliance after treatment. The preva- Two hundred and eighteen subjects with 999 partially edentulous patients, including nine
lence was 3% in non-smokers and 53% in implants (71% partially edentulous, 26% cur- smokers, with 131 implants were recalled 10
smokers with periodontal history. rent smokers) were examined clinically and 16 years after implant placement for clinical

72 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776 2012 John Wiley & Sons A/S
Mombelli et al  Epidemiology of peri-implantitis

and radiographic examination. The survival implant therapy. Where an accurate docu- healthy situation with high confidence (Lang
rate at 10 years was 89%. Fourteen implants mentation of the initial status is missing it is et al. 1990). From a prophylaxis point of view
were lost due to the presence of a peri- difficult to differentiate peri-implantitis from there may be a benefit to aim at absence of
implant infection. Twenty-one implants other peri-implant problems that may have BOP+, as long as one remains aware that this
(17%) were affected by peri-implantitis. The developed early, for example due to improper approach may lead to overtreatment, which
occurrence of peri-implantitis in individuals implant placement. Threshold values for ver- is a common problem in prophylaxis. From
without a history of periodontitis was 11%, tical bone deficiency must consider bone loss an epidemiological perspective it is inappro-
compared with 38% in patients with a history attributable to early remodeling that may be priate to draw inferences on the prevalence of
of periodontitis, with a significant difference unrelated to infection, and may be system peri-implantitis from the frequency of bleed-
between groups. No other studied variables specific. Cross-sectional studies are adequate ing after peri-implant probing alone.
were significantly associated with biological to measure prevalence, they are however of Based on the reviewed articles one may
complications. The criteria to define peri-im- limited use to evaluate conditions of tran- state that the prevalence of peri-implantitis
plantitis were PPD > 4 mm plus BOP+ and/or sient nature or that evolve gradually like seems to be in the order of 10% implants and
suppuration and radiographic bone loss peri-implantitis, and they are unsuitable to 20% patients during 510 years after implan-
 2.5 mm or bone loss extending  3 threads infer about causality. tation but this statement needs to be taken
for a follow-up of at least 10 years. A high frequency of BOP+ in the order of with caution as the individual reported fig-
Study 22 (Wahlstrom et al. 2010): Forty-six 80% has been noted in several studies (Rutar ures are rather variable, not easily compara-
partially edentulous patients with 116 et al. 2001; Baelum & Ellegaard 2004; Roos- ble and not suitable for meta-analysis.
implants, including five smokers, who had Jansaker et al. 2006b; Koldsland et al. 2010; Factors that have been shown to affect preva-
received fixed partial dentures on implants Dierens et al. 2012). To what extent BOP+ lence figures are the disease definition and
between 3 and 6 years earlier, were clinically alone indicates presence of pathology has the threshold for peri-implantitis, and differ-
and radiographically examined. Peri-implanti- been debated extensively with regards to peri- ences in the composition of study popula-
tis was diagnosed on the basis of the color odontal disease of natural teeth. Bleeding can tions.
and shape of the peri-implant mucosa, bleed- be induced easily at teeth with untreated The influence of differences in disease defi-
ing or pus on probing, PPD > 3 mm, and periodontitis with a blunt probe. The BOP+ nition has been mentioned above. Roos-Jan-
marginal bone loss > 2 mm compared with on its own, however, overestimates the pres- saker et al. (2006b) explored the prevalence of
radiographs taken 1 year after prosthetic ence of gingival inflammation in periodon- peri-implantitis using various composite dis-
loading. Peri-implantitis was diagnosed in tally healthy subjects (Lang et al. 1991) as ease definitions. This study concerned two-
two subjects, one smoker and one former well as in successfully treated patients with- piece implants that are known for a system-
smoker, both also affected from periodontitis. out residual disease (Karayiannis et al. 1992). immanent non-infectious early bone resorp-
Study 23 (Zetterqvist et al. 2010): A pro- The BOP+ is furthermore a poor prognostica- tion processes taking place shortly after abut-
spective, multicenter, randomized-controlled tor of future periodontal attachment loss ment connection (Adell et al. 1981). If 48%
5-year study of hybrid and fully etched (Claffey & Egelberg 1995). Whether or not of the implants had a PPD > 3 mm and were
implants included 112 patients who received bleeding upon peri-implant probing is associ- BOP+ irrespective of bone level, peri-implan-
139 control and 165 test implants (total: 304 ated with an increased risk for peri-implanti- titis, defined as bone loss  1.8 mm com-
implants). Peri-implantitis was defined as tis is currently unknown. The disproportion pared with 1-year data, combined with BOP
BOP+ and/or suppuration, PPD > 5 mm and between the frequency of BOP+ and clinically and/or pus, was diagnosed in only 16% of the
progressive crestal bone loss > 5 mm. One manifested peri-implantitis in several cohorts patients and concerned 7% of the implants.
case of peri-implantitis was identified based suggests that the rate of false positive values In the study of Koldsland et al. (2010), the
on these criteria. It concerned one control is high. As an example, the insertion of paper prevalence ranged from 11% to 47% depend-
implant in a subject previously treated for points into the peri-implant crevice induced ing on how the peri-implant bone loss was
advanced periodontitis. bleeding in 80% of the implants of 45 par- radiographically interpreted and which
tially edentulous patients enrolled in a main- threshold was used as the PPD limit.
tenance care program (Rutar et al. 2001). As can be seen in Table 1, sample popula-
Discussion However, during 510 years between implant tions comprised variable proportions of
installation and examination only 15 of the smokers. A differential prevalence figure
Prospective studies with clinical and radio- 64 monitored implants experienced one or with regards to the smoking status was
logical baseline data reflecting the status two episodes of peri-implantitis, and only reported in three studies (Karoussis et al.
after initial healing and remodeling, with an one implant was lost due to an uncontrolla- 2003; Gruica et al. 2004; Rinke et al. 2011).
appropriate sampling frame, adequate sample ble situation. In another study 73% of 212 In all three, smoking was associated with an
size and sampling method would be needed patients showed BOP, but only 9% were diag- increased prevalence of peri-implantitis. A
to determine the incidence of peri-implantitis nosed with peri-implantitis defined as the history of periodontitis has also been associ-
correctly. Such studies are currently unavail- presence of PPD > 4 mm in association with ated with a higher prevalence of peri-implan-
able. All included publications provided data peri-implant bleeding and/or suppuration, titis. In four studies this issue was
from convenience samples, typically from with radiographic confirmation of bone loss specifically addressed (Karoussis et al. 2003;
patients who were treated in a clinical center (Ferreira et al. 2006). Simonis et al. 2010; Lee et al. 2012; Roc-
during a certain period, and most data were This is not to say that monitoring bleeding cuzzo et al. 2012). Peri-implantitis was
cross-sectional or collected retrospectively. upon peri-implant probing may not have any detected more than twice as frequently in
Convenience samples may not be representa- clinical value. For natural teeth it has been periodontally compromised than in periodon-
tive of the general target population for oral shown that absence of bleeding indicates a tally healthy subjects in these studies.

2012 John Wiley & Sons A/S 73 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
Mombelli et al  Epidemiology of peri-implantitis

Other plausible factors that could affect identify initial cases with high specificity. necessary from time to time but catastrophic
the incidence of peri-implantitis relate to dif- On the other hand, if the disease evolves cases of advanced peri-implant pathology
ferences in treatment philosophy and meth- slowly and gradually, it is of utmost impor- were rare. In an additional study where the
ods among clinics (medical and dental tance that the infection can be intercepted patient-related prevalence rate of peri-implan-
selection criteria of subjects, indications for early to prevent massive damage of peri- titis was 11%, no peri-implant disease was
therapy, implant system and type, operating implant tissues. In modern dental care sys- diagnosed in non-smoking patients with a
procedures, quality control, etc.). In one tems that include individualized regular good compliance after treatment and without
study, each of 28 patients was treated with maintenance, cases of advanced peri-implan- a history of periodontitis (Rinke et al. 2011).
implants of two different types (Astrand et al. titis should be seen rarely, as they are inter- To gain the full picture of the epidemiology
2004). Peri-implantitis concerned only cepted at an earlier stage. Patients of the of peri-implantitis with all its clinical and
implants having a very rough implant surface reviewed studies have or have not been economical implications, it will be necessary
(TPS), and, with one exception, was found included in a maintenance care program. The in future studies to assess how much subse-
only among the 29% subjects with a history diagnosis and treatment of peri-implant bio- quent treatment is generated by placing
of periodontal disease. logical complications was carried out accord- implants, including prophylaxis, treatment of
The evolution from peri-implant mucositis ing to CIST in four studies (Rutar et al. 2001; mucositis and peri-implantitis, and therapy
to peri-implantitis is gradual and the progres- Bragger et al. 2005; Roccuzzo et al. 2012; after implant failure. Thus, there is a need
sion of peri-implantitis may be slow. It is Rodrigo et al. 2011). In all these studies, for monitoring implant patients longitudi-
therefore impossible to exactly determine the interceptive therapy for symptoms of peri- nally in view of a potential occurrence of
onset of peri-implantitis and challenging to implant mucositis or peri-implantitis was peri-implantitis.

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