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-
grated implants. Several narrative and sys-
tematic reviews are available reporting the
survival of implants in relation to subject-
specific factors such as tobacco smoking, sys-
temic diseases, or periodontitis (Mombelli &
Cionca 2006; Schou et al. 2006; Karoussis
et al. 2007; Klokkevold & Han 2007; Quirynen
et al. 2007; Ong et al. 2008; Bornstein et al.
2009; Heitz-Mayfield & Huynh-Ba 2009; Safii
et al. 2010). The total literature available
today suggests that over a period of 10 years
roughly 1 of 20 implants is lost. A meta-
analysis of five suitable studies (Hardt et al.
2002; Karoussis et al. 2003; Mengel &
Flores-de-Jacoby 2005; Mengel et al. 2007;
Gatti et al. 2008) revealed that the odds for
implant survival were significantly higher in
subjects without than with a history of peri-
odontal disease (Safii et al. 2010). Greater
than the risk for total implant failure are,
however, the odds that a technical complica-
tion (Pjetursson et al. 2007) or an inflamma-
Date:
Accepted 09 June 2012 tory condition of the peri-implant tissues
may arise. The incidence of peri-implant
To cite this article:
Mombelli A, Muller N, Cionca N. The epidemiology of diseases is currently a controversial issue.
peri-implantitis
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
part this may be due to different interpreta-
tions and definitions of disease states and dif-
ferences in study populations.
What is peri-implantitis?
Peri-implantitis (or Periimplantitis) has
been introduced as a term for infectious path-
ological conditions of peri-implant tissues
more than two decades ago (Levignac 1965;
Mombelli et al. 1987). At the 1st European
Workshop on Periodontology in 1993 it was
agreed that this term should be used specifi-
cally for destructive inflammatory processes
around osseointegrated implants in function
that lead to peri-implant pocket formation
and loss of supporting bone (Albrektsson &
Isidor 1994). The definition implied that ini-
tial healing had been uneventful and osseoin-
tegration was achieved as anticipated. Hence,
bone loss following implant installation due
to remodeling had to be distinguished from
bone loss due to a subsequent infection.
The typical signs and symptoms of peri-
implant mucositis and peri-implantitis were
discussed in the context of consensus confer-
ences on several occasions and have been
defined (Mombelli 1994, 1999; Lindhe et al.
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-
ing and/or suppuration upon gentle probing
with a blunt instrument. The marginal tissue
may be swollen or red, these characters are,
however, not always clearly visible. Unless
the access to the lesion is obstructed, a peri-
odontal probe can be advanced 4 mm or more
into the peri-implant sulcus. Pain is usually
not recorded. The typical bone defect is cra-
ter-like, runs all around the implant, and is
strictly demarcated. As perfect osseointegra-
tion is maintained apically to the defect,
bone destruction can progress without any
notable signs of implant mobility. Mobility
therefore indicates complete loss of osseoin-
tegration and is a sign of total failure (Mom-
belli & Lang 1998).
Using the experimental gingivitis model
(originally described by Loe et al. 1965), a
cause and effect relationship between biofilm
formation on implants and peri-implant mu-
cositis can be demonstrated (Pontoriero et al.
1994; Zitzmann et al. 2001). An attractive
extrapolation of these findings is the hypoth-
esis that bacterial biofilm on implant sur-
faces causes peri-implantitis, and that the
removal of these bacteria is the remedy. Ben-
eficial effects of mechanical debridement and
systemic antibiotics in cases diagnosed with
peri-implantitis supported this hypothesis
early (Mombelli & Lang 1992). However,
based on all data available up to 2008, it was
concluded that the predictability of such
treatment was limited and influenced by fac-
tors not yet fully understood (Claffey et al.
2008; Lindhe et al. 2008; Renvert et al. 2008).
As we have pointed out in a recent article on
the role of biofilms in peri-implant diseases
(Mombelli & Decaillet 2011), one needs to
consider the possibility that bacterial peri-
implant infections may also arise occasion-
ally as a consequence of non-microbial
events favoring the emergence of a patho-
genic microbiota. As an example, the fracture
of an implant can give rise to a secondary
bacterial infection, and thus provoke puru-
lent peri-implant disease. Another example is
peri-implant infection due to submucosal
persistence of luting cement, where the pres-
ence of a foreign body gives rise to a bacterial
infection. In one study (Wilson 2009) excess
dental cement was associated with clinical
and/or radiographic signs of peri-implant dis-
ease in 81% of 39 cases. Once the excess
cement was removed, the clinical signs of
disease disappeared in 74%. The differential
diagnosis of peri-implantitis should therefore
include the search for a specific underlying
cause, even if suppuration, or the presence of
a biofilm points to a bacterial infection.
68 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
What is not peri-implantitis?
Although formation of pockets, bleeding on
probing (BOP), suppuration, and loss of bone
belong to the disease-defining clinical signs
of peri-implantitis, increased peri-implant
probing depth (PPD), BOP, or peri-implant
bone loss, as single features are not sufficient
for the diagnosis of peri-implantitis. Bone
resorption can also be caused by the deep
insertion of an implant (Hammerle et al.
1996) or the placement of implants too close
to each other (Tarnow et al. 2000). In the
case of two-piece implants, abutment instal-
lation has been associated with subsequent
bone remodeling that may be unrelated to
infection (Adell et al. 1981). In such cases,
marginal bone loss is commonly limited to
the first few weeks after abutment connec-
tion and is not necessarily the initial stage of
peri-implantitis. Long-term monitoring of
implant performance should therefore not be
based on radiographs taken directly after
implant placement, but should rather relate
to documents obtained once tissue homeosta-
sis has been established (i.e. upon the com-
pletion of the prosthodontic work).
Moreover, not every probing depth of over
3 mm is a definite sign of peri-implantitis.
The type and shape of the implant, the con-
nection parts, and the prosthetic suprastruc-
ture affect the dimensions of the peri-
implant tissues. Soft tissue conditioning in
the esthetic zone to create the illusion of an
interdental papilla can lead to an increase in
the distance from the implant shoulder to
the mucosal margin up to 5 mm (Gallucci
et al. 2011). Combined with a mucositis and
marginal bone remodeling due to deep posi-
tioning of the implant, such a situation could
be misdiagnosed as peri-implantitis.
Whenever key disease-defining signs on
their own are insufficient for a diagnosis, the
prevalence or incidence of the disease cannot
be estimated accurately using the frequencies
of the single signs. This problem has been
addressed in other medical disciplines, and
far-reaching consequences of invalid clinical
conclusions have been shown. As an exam-
ple, the case definition of malaria comprises
a set of clinical and laboratory parameters
combined with the presence of Plasmodium
falciparum parasitemia. While these criteria
are sensitive in diagnosing severe malaria,
they are also present in other serious ill-
nesses. As asymptomatic parasitemia is com-
mon in malaria-endemic areas, patients
fulfilling World Health Organization criteria
for severe malaria often have disease attribut-
able to another cause (Anstey & Price 2007).
For malaria, the specificity of the case
definition can be improved by applying a par-
asite density threshold and by excluding a
number of other medical conditions (Bejon
et al. 2007). We suspect that the same prob-
lem exists with regards to peri-implantitis
and that the prevalence of peri-implantitis
may have been over-estimated by some
authors. Because prevalence and incidence of
any disease depends on the disease-defining
criteria, the primary objective of this article
is to discuss the prevalence and incidence of
peri-implantitis in the context of the diagnos-
tic aspects and their differential diagnosis.
Material and methods
Search strategy
On December 7, 2011 we searched the US
National Institutes of Health free digital
archive of biomedical and life sciences jour-
nal literature (PubMed) to identify all articles
that included the following terms in the
title:
peri-implantitis OR periimplantitis
OR biological complication* OR peri-
implant disease
In addition, we searched previous review
articles on the subject as well as the refer-
ence lists of the articles already identified for
further potentially relevant publications.
This initial search was designed for high
recall rather than high precision. Although
there was no language restriction, the mini-
mum requirement was access to an English
version of the title.
Study selection criteria
To be eligible for inclusion in the review,
reports had to provide data in humans from
dental implants with peri-implantitis. The
study selection criteria were:
Includes at least 20 human subjects with
dental osseointegrated implants.
Implants were in service without compli-
cations for at least one year.
Describes a pathological condition com-
patible with the definition of peri-im-
plantitis.
Quantitative data for signs of peri-implan-
titis, such as PPD, BOP+, suppuration,
bone loss, are presented.
Cases are not selected initially based on
the presence of a peri-implant pathology.
Three independent reviewers (AM, NM,
NC) screened titles and abstracts of the
search results. The full text of all studies of
possible relevance was obtained for assess-
ment against the stated inclusion criteria.
2012 John Wiley & Sons A/S

Any disagreement regarding inclusion was
resolved by discussion.
Data extraction and synthesis of extracted
evidence
A preliminary review of the literature
revealed considerable heterogeneity of criteria
utilized to define peri-implantitis. In view of
the issues deliberated in the introduction we
decided to tabulate the data where appropri-
ate and report the findings in a narrative
manner.
The following information was sought:
Study design, number of cases, implant type,
type of data and disease definition, sub-
groups if any (risk factors), length of follow-
up, number of diseased cases according to the
disease definition.
Results
Included studies
The initial search yielded 321 potentially rel-
evant publications. Two hundred and eighty
nine of them, however, failed to satisfy the
study selection criteria. The main reason for
non-inclusion was that articles did not con-
cern at least 20 human subjects with dental
osseointegrated implants. The second most
frequent reason was that cases with peri-
implant pathology were selected deliberately.
Of the 32 articles that seemed to meet all
study selection criteria five additional ones
were excluded during data extraction: One
(Feloutzis et al. 2003) was not about peri-im-
plantitis; one (Laine et al. 2006) selected
patients with or without peri-implantitis
intentionally; three (Lekholm et al. 1986,
1996; Merickse-Stern et al. 2001) did not pro-
vide peri-implantitis prevalence data. Two
additional studies, one not initially identified
(Astrand et al. 2004), and one becoming avail-
able shortly after the search (Dierens et al.
2012), were added.
For the final evaluation 29 articles, report-
ing data from 23 studies could be included.
They are listed in Table 1 and are presented
narratively below in alphabetic order. The
selected studies all reported data from conve-
nience samples, typically all patients treated
in a clinical center during a certain period
and satisfying certain inclusion criteria.
Case definition
In general, the retained articles described ele-
ments, or combinations of elements of the
disease-defining signs of peri-implantitis and
their frequency, most notably the frequency
of BOP (BOP+), PPD above certain thresholds,
or vertical loss of bone as visible on radio-
2012 John Wiley & Sons A/S
graphs exceeding certain levels (expressed as
millimeters from a landmark, such as the
implant shoulder, or as the exposure of two,
three or more threads of the screw helix). In
several articles, frequencies of individual
parameters were recorded separately, but it
was not reported to what extent the disease-
defining criteria were found simultaneously
at the same sites. Some sites may, however,
be bleeding without bone loss, while others
may show bone loss unrelated to infection.
The frequency of peri-implantitis could not
be determined explicitly due to failure of
using a composite disease definition in Study
2 (Baelum & Ellegaard 2004) and Study 8
(Fransson et al. 2005).
Studies
Study 1 (Astrand et al. 2004): This prospec-
tive split-mouth study included 28 patients
treated in the maxilla with a total of 150
implants of two different types in five cen-
ters. Twenty-five percent were smokers, 29%
had a history of periodontal disease. After
3 years two implants of each type were lost.
Peri-implantitis, defined as infection includ-
ing pus and bone loss, was found at 5%
implants in an undisclosed number of sub-
jects. Six of the seven implants with peri-im-
plantitis were found in patients with a
history of periodontitis, and all implants had
the same implant surface (TPS).
Study 2 (Baelum & Ellegaard 2004): This
case series included all 258 implants inserted
in 128 subjects in a private periodontal prac-
tice during 14 years. Ten-year data were pre-
sented for 19 two-stage, and 41 one-stage
implants. All patients had received extensive
periodontal treatment prior to implant place-
ment and were maintained at a high standard
of oral hygiene. Sixty-five percent were
smokers at the time of implant placement.
Ten-year survival rates were 97% and 78%,
depending on implant type. After 10 years,
21% of the two-stage and 40% of the one-
stage implants showed bone loss  1.5 mm,
but only 5% and 14% at the 3.5 mm thresh-
old. Twenty-three percent of the two-stage
and 25% of the one-stage implants showed
probing depth > 5 mm. Ninety percent of the
two-stage and 69% of the one-stage implants
showed BOP. The description was on the
level of the implant. The frequency of peri-
implantitis could not be determined due to
lack of composite disease definition and
according data.
Study 3 (Bragger et al. 2001): This case ser-
ies includes 48 patients with 103 implants
examined after 45 years of function (105
implants were placed, two were lost early).
69 |
Mombelli et al
Epidemiology of peri-implantitis
Peri-implantitis, defined as presence of
PPD > 4 mm and BOP+, was diagnosed at 10
(10%) implants. If the threshold for definition
of peri-implantitis was set at PPD > 5 mm
and BOP+ the incidence at the implant level
was 5%. The same patients were included in
a later analysis on the incidence of biological
complications at 160 implants in 89 partially
edentulous subjects during 812 years of
maintenance after implant placement (Brag-
ger et al. 2005). The threshold to define a bio-
logical complication was a probing pocket
depth of 5 mm and BOP or pus secretion.
Twenty-four instances of peri-implantitis
were diagnosed in total and intercepted with
therapy. Seven implants were lost because of
biological failures.
Study 4 (Corbella et al. 2011): Sixty-one
patients with 244 immediately loaded
implants, supporting mandibular and maxil-
lary full-arch prostheses, were included in a
structured maintenance program. Peri-im-
plantitis was defined as PPD > 3 mm plus
Bleeding index > 1. Two patients lost a total
of three implants due to peri-implantitis. No
further instances of peri-implantitis were
reported thereafter. The number of cases/
implants with more than 3 years follow-up
was too small for a meaningful long-term
analysis.
Study 5 (Dierens et al. 2012): From a total
of 134 patients with 166 single-tooth
implants, 50 subjects with 59 remaining
implants were examined after 1622 years.
Reasons for the unavailability of subjects
were multiple, mostly administrative or
unwillingness to participate, but also due to
death (3%) or loss of all implants (5%). Three
implants, each in a different subject, showed
bone loss extending over the third implant
thread (>2.7 mm) with BOP + .
Study 6 (Dvorak et al. 2011): One hundred
and seventy seven women with 828 dental
implants in situ since more than one year
were investigated cross-sectionally at age
63 9 years. If there was bleeding on peri-
implant probing and/or suppuration together
with a PPD > 5 mm and radiographic bone
loss the subject was diagnosed as having peri-
implantitis. Twenty-seven of 115 healthy
subjects, four of 16 subjects with a diagnosis
of osteopenia, and 11 of 46 subjects with
osteoporosis were diagnosed with peri-im-
plantitis. The over-all prevalence of peri-im-
plantitis was 24% without significant
differences between groups.
Study 7 (Ferreira et al. 2006): Two hundred
and twelve partially edentulous subjects
rehabilitated with 578 osseointegrated
implants of three different brands were exam-
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.
Peri-implantitis, defined as the presence of
PPD > 4 mm in association with peri-
implant bleeding and/or suppuration, with
radiographic confirmation of bone loss, was
detected in 19 cases (9%). As the time since
implant placement was highly variable, the
prevalence at a given time point could not be
determined. Presence of periodontitis and dia-
betes were statistically associated with
increased risk for peri-implantitis.
Study 8 (Fransson et al. 2005): Radiographs
of 662 subjects with 3413 implants, support-
ing fixed dentures or single crowns, with a
documented function time of at least 5 years,
were analyzed. Four hundred and twenty
three implants (12%), distributed in 184
(28%) subjects, had one or more implants
with progressive bone loss to a level of three
or more threads including detectable bone
loss after the first year in function. The prob-
ability for subjects to exhibit bone loss was
not influenced by age, gender, type of con-
struction, function time, or maxillary/man-
dibular position of the implants. The number
of implants per subject, however, had a sig-
nificant impact. Peri-implantitis was not
explicitly identified on the basis of a compos-
ite disease definition. Some subjects with
progressive bone loss were further character-
ized into two additional publications: In a
subset of 82 subjects, implants with pro-
gressive bone loss were more likely to show
BOP+, suppuration, recession and
PPD > 5 mm. Smokers had larger numbers of
affected implants than non-smokers (Frans-
son et al. 2008). In 182 subjects, 419 of 1070
examined implants exhibited peri-implanti-
tis-associated vertical bone loss > 2 mm.
The proportion of affected implants varied
between 30% and 52% in different jaw posi-
tions and the most common position was the
lower front region (Fransson et al. 2009).
Study 9 (Gatti et al. 2008): Sixty-two par-
tially edentulous patients were consecutively
enrolled in this study. One hundred and
twenty-nine implants were placed in 26
patients with a history of severe periodonti-
tis, 26 implants in seven subjects with a his-
tory of mild periodontitis, and 72 in 29
periodontally healthy subjects. Patients
requiring periodontal treatment were treated
prior to implantation. At 5 years, six
patients, two from each group, had dropped
out. In the severe periodontitis group, two
implants in one patient failed due to peri-im-
plantitis, and two implants in another patient
were successfully treated for peri-implantitis.
The criteria to define peri-implantitis were
loss of > 2 mm of marginal bone from the
last radiographic assessment, in the presence
of pus or another sign of infection and
PPD > 5 mm. Patients affected by severe or
moderate periodontitis had lost 2.6 mm peri-
implant bone over 5 years on average;
healthy subjects lost 1.2 mm.
Study 10 (Gruica et al. 2004): Clinical
charts of 180 consecutively admitted patients
with 292 implants in function for about 8
15 years were analyzed with respect to the
occurrence of biological complications,
defined as clinical conditions with suppura-
tion from the peri-implant sulcus, develop-
ment of a fistula, or peri-implantitis with
radiologic bone loss. Fifty-one implants in 34
patients showed late infectious biologic com-
plications. Fifty-three subjects were smokers.
Heavy smokers had 40%, light smokers had
17%, and never and former smokers had 13%
implants with complications.
Study 11 (Karoussis et al. 2003): Fifty-three
patients with 112 implants were assessed
after 10 years of regular supportive periodon-
tal therapy. Eight subjects with a history of
chronic periodontitis lost 2 of 21 implants,
the remaining 45 periodontally health sub-
jects lost 3 of 91 implants. When peri-im-
plantitis was defined as PPD > 4 mm plus
BOP+ or suppuration 29% of the implants in
periodontally compromised patients, and 6%
in periodontally health subjects were diag-
nosed with peri-implantitis. The analysis was
per implant.
Study 12 (Koldsland et al. 2010): Three
hundred and seventy-two solid screw
implants of four different brands in 109 sub-
jects were examined 8.4 years (SD: 4.6 years)
after functional loading. Peri-implantitis was
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,
radiographic peri-implant bone loss at or
above 2 or 3 mm, PPD > 3 mm, or
PPD > 5 mm. Depending on the combina-
tions and threshold levels used for bone loss
and PPD, the prevalence of peri-implantitis
varied between 11% (12 subjects presenting
19 (5%) implants with PPD > 5 and > 2 mm
bone loss) and 47% (49 subjects presenting
108 (37%) implants with signs of inflamma-
tion and detectable loss of bone). The peri-
implant tissues of 249 (71%) implants were
judged to be inflamed (mBI score > 0 and/or
BOP or suppuration). This concerned 88 sub-
jects (82%). Supplementing information on
the same patients was provided in an addi-
tional publication (Koldsland et al. 2011):
Multi-level statistical analyses identified
location in the maxilla as risk indicator for
detectable peri-implantitis. Gender (male)
and history of periodontitis were identified as
risk indicators for overt peri-implantitis.
Study 13 (Lee et al. 2012): This retrospec-
tive case study included 30 periodontally
compromised patients with 56 implants and
30 periodontally healthy subjects with 61
implants. The groups were matched for age,
gender, implant characteristics, and smoking
(three smokers in each group). At follow-up
at 8 years (range 514) the prevalence of
implants with PPD > 4 mm and BOP+ was
27% in periodontally compromised and 13%
in periodontally healthy subject (37% vs.
17% patients). Patients with residual pockets
had a prevalence of 54%. The prevalence of
bone loss > 3 mm was 17% and 7% at the
level of the patients, and 9% and 3% at the
level if the implants, respectively.
Study 14 (Maximo et al. 2008): One hun-
dred and thirteen individuals with 347
implants in function for at least 1 year were
enrolled in this study. The time since
implant placement or loading was undis-
closed. Twenty-six implants (7%), distributed
in 14 (12%) subjects were diagnosed with
peri-implantitis, defined as presence of
PPD > 4 mm with BOP+ and/or suppuration
and radiographic bone loss of three or more
threads.
Study 15 (Rinke et al. 2011): Data from 89
patients were analyzed 5.7 2.1 years after
implant placement. The patient-related pre-
valence rate of peri-implantitis, defined as
PPD > 4 mm, BOP+ and/or pus, with radio-
graphic bone loss, was 11%. No disease was
diagnosed in non-smoking patients without a
history of periodontal disease and with a
good compliance after treatment. The preva-
lence was 3% in non-smokers and 53% in
smokers with periodontal history.
72 | Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
Study 16 (Roccuzzo et al. 2012): One hun-
dred and one partially edentulous subjects
were examined 10 years after implant place-
ment and fixed prosthodontic therapy.
Twenty-eight periodontally healthy subjects
received 61 implants. Thirty-seven subjects
with moderate periodontal disease, and 36
subjects with advanced periodontal disease,
received 95 and 90 implants, respectively. At
the end of active periodontal treatment,
patients were asked to follow an individual-
ized supportive periodontal therapy program.
The diagnosis and treatment of peri-implant
biological complications was carried out
according to cumulative interceptive support-
ive therapy (CIST) (Mombelli & Lang 1998).
Eighteen implants were removed due to bio-
logical complications (two, seven, nine
implants in the three groups, respectively).
During the 10 years, antibiotic and/or surgi-
cal therapy was performed in 11%, 27%, and
47% cases, respectively, significantly more in
severely compromised than healthy patients
(P = 0.002). At the final examination, the per-
centage of implants with at least one site
with a PPD > 5 mm was, respectively, 2%,
16%, and 27%, with a statistically significant
difference between healthy and compromised
subjects.
Study 17 (Rodrigo et al. 2011): Five years
after implant loading, clinical and radiograph-
ical variables were recorded in 22 implant
patients of a private clinic. Patients were not
included if presenting with untreated peri-
odontitis, inappropriate periodontal mainte-
nance, or with a systemic or local disease.
Thirty-six percent were smokers, 68% were
periodontally treated. Each subject received
at least one post-extraction immediate
implant (34 implants in total) and one
delayed implant (34 implants). During the
follow-up period, 9 of the 22 participants
(40%) showed signs of biological com-
plications: mucositis (PPD > 3 mm, BOP+,
without significant bone loss) was diag-
nosed at 13 (20%) implants, peri-implantitis
(PPD > 3 mm, BOP+, vertical bone loss years
15 > 3x the standard deviation of repeated
measures) at four (6%) implants. There was
no difference between groups. Once these
conditions were diagnosed they were imme-
diately treated according to the CIST proto-
col, with success in all cases except one,
where one delayed implant showed signs of
persisting peri-implantitis (deep PPD and pro-
gressing loss of bone).
Study 18 (Roos-Jansaker et al. 2006a,b,c):
Two hundred and eighteen subjects with 999
implants (71% partially edentulous, 26% cur-
rent smokers) were examined clinically and
radiographically after 914 years of function
(65% of the patients and 60% of the implants
had a follow-up of 11 years or more). The
subjects were not enrolled in a structured
maintenance care program. In this study the
prevalence of peri-implantitis was estimated
using various levels of clinical and radio-
graphic criteria: 48% of the implants had a
PPD > 3 mm and BOP+, but no concomitant
bone loss, which was interpreted as presence
of peri-implant mucositis. This concerned
77% of the subjects. If peri-implantitis was
defined as exposure of three or more threads
(corresponding to at least 1.8 mm vertical
loss of bone following the first year in func-
tion) together with BOP+ and/or suppuration,
then the prevalence of peri-implantitis was
16% on the level of the patient and 7% on
the level of the implant. Bone levels were
associated with the presence or absence of
keratinized mucosa at implants. On the
patient level, smoking was associated with
mucositis, bone level, and peri-implantitis.
Peri-implantitis was related to a history of
periodontitis.
Study 19 (Rutar et al. 2001): Forty-five par-
tially edentulous patients (mean age:
51 years, range: 2783 years), with a total of
64 implants participated in this retrospective
analysis. The subjects had been enrolled in a
maintenance care program during 510 years
between implant installation and examina-
tion. During this time, nine implants experi-
enced one episode and an additional six
implants two episodes of peri-implantitis. In
a patient with a history of diabetes, one of
these implants was lost due to extensive
bone loss. With this exception, all episodes
of peri-implantitis were successfully treated
employing the principles of the CIST proto-
col. At examination, 42 implants (66%)
showed a PPD > 4 mm. All 15 implants with
a history of peri-implantitis belonged to this
group. The insertion of paper points into the
sulcus for microbiological sampling induced
bleeding in 80% of the implants.
Study 20 (Schmidlin et al. 2010): Thirty-
nine single crowns on implants were reexam-
ined in an undisclosed number of patients
with treated chronic periodontitis after a
highly variable observation time ranging from
3 to 22 years. Five implants were diagnosed
with peri-implantitis (PPD > 5 mm and BOP
+ or suppuration). The cumulative risk of
peri-implantitis after 10 years was calculated
to be 18% (95% CI 6.940.9).
Study 21 (Simonis et al. 2010): Fifty-five
partially edentulous patients, including nine
smokers, with 131 implants were recalled 10
16 years after implant placement for clinical
2012 John Wiley & Sons A/S

and radiographic examination. The survival
rate at 10 years was 89%. Fourteen implants
were lost due to the presence of a peri-
implant infection. Twenty-one implants
(17%) were affected by peri-implantitis. The
occurrence of peri-implantitis in individuals
without a history of periodontitis was 11%,
compared with 38% in patients with a history
of periodontitis, with a significant difference
between groups. No other studied variables
were significantly associated with biological
complications. The criteria to define peri-im-
plantitis were PPD > 4 mm plus BOP+ and/or
suppuration and radiographic bone loss
 2.5 mm or bone loss extending  3 threads
for a follow-up of at least 10 years.
Study 22 (Wahlstrom et al. 2010): Forty-six
partially edentulous patients with 116
implants, including five smokers, who had
received fixed partial dentures on implants
between 3 and 6 years earlier, were clinically
and radiographically examined. Peri-implanti-
tis was diagnosed on the basis of the color
and shape of the peri-implant mucosa, bleed-
ing or pus on probing, PPD > 3 mm, and
marginal bone loss > 2 mm compared with
radiographs taken 1 year after prosthetic
loading. Peri-implantitis was diagnosed in
two subjects, one smoker and one former
smoker, both also affected from periodontitis.
Study 23 (Zetterqvist et al. 2010): A pro-
spective, multicenter, randomized-controlled
5-year study of hybrid and fully etched
implants included 112 patients who received
139 control and 165 test implants (total: 304
implants). Peri-implantitis was defined as
BOP+ and/or suppuration, PPD > 5 mm and
progressive crestal bone loss > 5 mm. One
case of peri-implantitis was identified based
on these criteria. It concerned one control
implant in a subject previously treated for
advanced periodontitis.
Discussion
Prospective studies with clinical and radio-
logical baseline data reflecting the status
after initial healing and remodeling, with an
appropriate sampling frame, adequate sample
size and sampling method would be needed
to determine the incidence of peri-implantitis
correctly. Such studies are currently unavail-
able. All included publications provided data
from convenience samples, typically from
patients who were treated in a clinical center
during a certain period, and most data were
cross-sectional or collected retrospectively.
Convenience samples may not be representa-
tive of the general target population for oral
2012 John Wiley & Sons A/S
implant therapy. Where an accurate docu-
mentation of the initial status is missing it is
difficult to differentiate peri-implantitis from
other peri-implant problems that may have
developed early, for example due to improper
implant placement. Threshold values for ver-
tical bone deficiency must consider bone loss
attributable to early remodeling that may be
unrelated to infection, and may be system
specific. Cross-sectional studies are adequate
to measure prevalence, they are however of
limited use to evaluate conditions of tran-
sient nature or that evolve gradually like
peri-implantitis, and they are unsuitable to
infer about causality.
A high frequency of BOP+ in the order of
80% has been noted in several studies (Rutar
et al. 2001; Baelum & Ellegaard 2004; Roos-
Jansaker et al. 2006b; Koldsland et al. 2010;
Dierens et al. 2012). To what extent BOP+
alone indicates presence of pathology has
been debated extensively with regards to peri-
odontal disease of natural teeth. Bleeding can
be induced easily at teeth with untreated
periodontitis with a blunt probe. The BOP+
on its own, however, overestimates the pres-
ence of gingival inflammation in periodon-
tally healthy subjects (Lang et al. 1991) as
well as in successfully treated patients with-
out residual disease (Karayiannis et al. 1992).
The BOP+ is furthermore a poor prognostica-
tor of future periodontal attachment loss
(Claffey & Egelberg 1995). Whether or not
bleeding upon peri-implant probing is associ-
ated with an increased risk for peri-implanti-
tis is currently unknown. The disproportion
between the frequency of BOP+ and clinically
manifested peri-implantitis in several cohorts
suggests that the rate of false positive values
is high. As an example, the insertion of paper
points into the peri-implant crevice induced
bleeding in 80% of the implants of 45 par-
tially edentulous patients enrolled in a main-
tenance care program (Rutar et al. 2001).
However, during 510 years between implant
installation and examination only 15 of the
64 monitored implants experienced one or
two episodes of peri-implantitis, and only
one implant was lost due to an uncontrolla-
ble situation. In another study 73% of 212
patients showed BOP, but only 9% were diag-
nosed with peri-implantitis defined as the
presence of PPD > 4 mm in association with
peri-implant bleeding and/or suppuration,
with radiographic confirmation of bone loss
(Ferreira et al. 2006).
This is not to say that monitoring bleeding
upon peri-implant probing may not have any
clinical value. For natural teeth it has been
shown that absence of bleeding indicates a
73 |
Mombelli et al
Epidemiology of peri-implantitis
healthy situation with high confidence (Lang
et al. 1990). From a prophylaxis point of view
there may be a benefit to aim at absence of
BOP+, as long as one remains aware that this
approach may lead to overtreatment, which
is a common problem in prophylaxis. From
an epidemiological perspective it is inappro-
priate to draw inferences on the prevalence of
peri-implantitis from the frequency of bleed-
ing after peri-implant probing alone.
Based on the reviewed articles one may
state that the prevalence of peri-implantitis
seems to be in the order of 10% implants and
20% patients during 510 years after implan-
tation but this statement needs to be taken
with caution as the individual reported fig-
ures are rather variable, not easily compara-
ble and not suitable for meta-analysis.
Factors that have been shown to affect preva-
lence figures are the disease definition and
the threshold for peri-implantitis, and differ-
ences in the composition of study popula-
tions.
The influence of differences in disease defi-
nition has been mentioned above. Roos-Jan-
saker et al. (2006b) explored the prevalence of
peri-implantitis using various composite dis-
ease definitions. This study concerned two-
piece implants that are known for a system-
immanent non-infectious early bone resorp-
tion processes taking place shortly after abut-
ment connection (Adell et al. 1981). If 48%
of the implants had a PPD > 3 mm and were
BOP+ irrespective of bone level, peri-implan-
titis, defined as bone loss  1.8 mm com-
pared with 1-year data, combined with BOP
and/or pus, was diagnosed in only 16% of the
patients and concerned 7% of the implants.
In the study of Koldsland et al. (2010), the
prevalence ranged from 11% to 47% depend-
ing on how the peri-implant bone loss was
radiographically interpreted and which
threshold was used as the PPD limit.
As can be seen in Table 1, sample popula-
tions comprised variable proportions of
smokers. A differential prevalence figure
with regards to the smoking status was
reported in three studies (Karoussis et al.
2003; Gruica et al. 2004; Rinke et al. 2011).
In all three, smoking was associated with an
increased prevalence of peri-implantitis. A
history of periodontitis has also been associ-
ated with a higher prevalence of peri-implan-
titis. In four studies this issue was
specifically addressed (Karoussis et al. 2003;
Simonis et al. 2010; Lee et al. 2012; Roc-
cuzzo et al. 2012). Peri-implantitis was
detected more than twice as frequently in
periodontally compromised than in periodon-
tally healthy subjects in these studies.
Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776
Mombelli et al
Epidemiology of peri-implantitis
Other plausible factors that could affect
the incidence of peri-implantitis relate to dif-
ferences in treatment philosophy and meth-
ods among clinics (medical and dental
selection criteria of subjects, indications for
therapy, implant system and type, operating
procedures, quality control, etc.). In one
study, each of 28 patients was treated with
implants of two different types (Astrand et al.
2004). Peri-implantitis concerned only
implants having a very rough implant surface
(TPS), and, with one exception, was found
only among the 29% subjects with a history
of periodontal disease.
The evolution from peri-implant mucositis
to peri-implantitis is gradual and the progres-
sion of peri-implantitis may be slow. It is
therefore impossible to exactly determine the
onset of peri-implantitis and challenging to
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