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Andrea Mombelli

Nada Muller
Norbert Cionca

The epidemiology of peri-implantitis

Authors affiliations:
Andrea Mombelli, Nada Muller, Norbert Cionca,
School of Dental Medicine, Division of
Periodontology and Oral Pathophysiology,
University of Geneva, Rue Barthelemy-Menn 19,
CH-1205, Geneva, Switzerland

Key words: epidemiology, peri-implantitis, prevalence, review, risk factors

Corresponding author:
Andrea Mombelli
School of Dental Medicine
Division of Periodontology and Oral
Pathophysiology
University of Geneva
Rue Barthelemy-Menn 19
CH-1205 Geneva, Switzerland
Tel.: +41 22 379 40 30
Fax: +41 22 379 40 32
e-mail: andrea.mombelli@unige.ch

studies, with information on the presence of signs of peri-implantitis in populations of at least 20

Conflict of Interest and Source of Funding Statement:


The authors declare that they have no conflict of
interests. The study was self-funded by the authors and
their institution.

probing depths and bone loss, differences in treatment methods and aftercare of patients, and

Date:
Accepted 09 June 2012
To cite this article:
Mombelli A, Muller N, Cionca N. The epidemiology of
peri-implantitis
Clin. Oral Implants Res. 23(Suppl. 6), 2012, 6776
doi: 10.1111/j.1600-0501.2012.02541.x

2012 John Wiley & Sons A/S

Abstract
Aim: To review the literature on the prevalence and incidence of peri-implantitis.
Methods: Out of 322 potentially relevant publications we identified 29 articles concerning 23
cases.
Results and conclusions: All studies provided data from convenience samples, typically from
patients who were treated in a clinical center during a certain period, and most data were crosssectional or collected retrospectively. Based on the reviewed papers one may state that the
prevalence of peri-implantitis seems to be in the order of 10% implants and 20% patients during 5
10 years after implant placement but the individual reported figures are rather variable, not easily
comparable and not suitable for meta-analysis. Factors that should be considered to affect
prevalence figures are the disease definition, the differential diagnosis, the chosen thresholds for
dissimilarities in the composition of study populations. Smoking and a history of periodontitis have
been associated with a higher prevalence of peri-implantitis.

Missing teeth can be replaced successfully


with reconstructions anchored on osseointegrated implants. Several narrative and systematic reviews are available reporting the
survival of implants in relation to subjectspecific factors such as tobacco smoking, systemic 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 metaanalysis 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 periodontal disease (Safii et al. 2010). Greater
than the risk for total implant failure are,
however, the odds that a technical complication (Pjetursson et al. 2007) or an inflammatory condition of the peri-implant tissues
may arise. The incidence of peri-implant
diseases is currently a controversial issue.
Conflicting statements have been made with
regards to the magnitude and the long-term

consequences of this problem. At least in


part this may be due to different interpretations and definitions of disease states and differences in study populations.
What is peri-implantitis?

Peri-implantitis (or Periimplantitis) has


been introduced as a term for infectious pathological 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 specifically 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 initial healing had been uneventful and osseointegration 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 periimplant mucositis and peri-implantitis were
discussed in the context of consensus conferences on several occasions and have been
defined (Mombelli 1994, 1999; Lindhe et al.
2008; Zitzmann & Berglundh 2008; Lang

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Mombelli et al  Epidemiology of peri-implantitis

et al. 2011). The inflammation causes bleeding 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 periodontal probe can be advanced 4 mm or more
into the peri-implant sulcus. Pain is usually
not recorded. The typical bone defect is crater-like, runs all around the implant, and is
strictly demarcated. As perfect osseointegration is maintained apically to the defect,
bone destruction can progress without any
notable signs of implant mobility. Mobility
therefore indicates complete loss of osseointegration and is a sign of total failure (Mombelli & 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 mucositis can be demonstrated (Pontoriero et al.
1994; Zitzmann et al. 2001). An attractive
extrapolation of these findings is the hypothesis that bacterial biofilm on implant surfaces causes peri-implantitis, and that the
removal of these bacteria is the remedy. Beneficial 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 factors 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 periimplant infections may also arise occasionally as a consequence of non-microbial
events favoring the emergence of a pathogenic microbiota. As an example, the fracture
of an implant can give rise to a secondary
bacterial infection, and thus provoke purulent peri-implant disease. Another example is
peri-implant infection due to submucosal
persistence of luting cement, where the presence 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 disease 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.

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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 installation 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 connection 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 homeostasis has been established (i.e. upon the completion 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 connection parts, and the prosthetic suprastructure affect the dimensions of the periimplant 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 positioning 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 example, 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 illnesses. As asymptomatic parasitemia is common in malaria-endemic areas, patients
fulfilling World Health Organization criteria
for severe malaria often have disease attributable to another cause (Anstey & Price 2007).
For malaria, the specificity of the case

Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776

definition can be improved by applying a parasite density threshold and by excluding a


number of other medical conditions (Bejon
et al. 2007). We suspect that the same problem 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 diagnostic 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 journal literature (PubMed) to identify all articles
that included the following terms in the
title:
peri-implantitis OR periimplantitis
OR biological complication* OR periimplant disease
In addition, we searched previous review
articles on the subject as well as the reference 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 minimum 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 complications for at least one year.
Describes a pathological condition compatible with the definition of peri-implantitis.
Quantitative data for signs of peri-implantitis, 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 assessment against the stated inclusion criteria.
2012 John Wiley & Sons A/S

Mombelli et al  Epidemiology of peri-implantitis

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 appropriate 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, subgroups if any (risk factors), length of followup, number of diseased cases according to the
disease definition.

Results
Included studies

The initial search yielded 321 potentially relevant 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 concern at least 20 human subjects with dental
osseointegrated implants. The second most
frequent reason was that cases with periimplant 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-implantitis; 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 provide peri-implantitis prevalence data. Two
additional studies, one not initially identified
(Astrand et al. 2004), and one becoming available shortly after the search (Dierens et al.
2012), were added.
For the final evaluation 29 articles, reporting 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 convenience 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 elements, 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 diseasedefining 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 prospective split-mouth study included 28 patients
treated in the maxilla with a total of 150
implants of two different types in five centers. 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 including pus and bone loss, was found at 5%
implants in an undisclosed number of subjects. Six of the seven implants with peri-implantitis 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 practice during 14 years. Ten-year data were presented for 19 two-stage, and 41 one-stage
implants. All patients had received extensive
periodontal treatment prior to implant placement 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 onestage implants showed bone loss  1.5 mm,
but only 5% and 14% at the 3.5 mm threshold. 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 periimplantitis could not be determined due to
lack of composite disease definition and
according data.
Study 3 (Bragger et al. 2001): This case series includes 48 patients with 103 implants
examined after 45 years of function (105
implants were placed, two were lost early).

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 (Bragger et al. 2005). The threshold to define a biological 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 maxillary full-arch prostheses, were included in a
structured maintenance program. Peri-implantitis 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 periimplant probing and/or suppuration together
with a PPD > 5 mm and radiographic bone
loss the subject was diagnosed as having periimplantitis. 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-implantitis. The over-all prevalence of peri-implantitis 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-

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Mombelli et al  Epidemiology of peri-implantitis

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


Peri-implantitis
Incidence/
prevalence

Comments

References

Study design

I type

Disease definition

Risk factors

Follow-up

Astrand
et al.
(2004)

Prospective
split-mouth

Branemark, ITI
TPS

SUP plus BL n

25% smok
29% PCP

3 yrs

C: nd
I: 5%

All I with peri-implantitis had


TPS surface

Baelum &
Ellegaard
(2004)

Prospective
case series

Astra, ITI

PPD, BOP, BL
No composite
disease definition

65% smok

014 yrs

nd

Analysis on implant level

Bragger
et al.
(2001)

Retrospective
case series

ITI

PPD > 4 plus BOP+

5 yrs

C: 10%
I: 10%

If the threshold was PPD > 5


and BOP+ the incidence was
5% (I)

Bragger
et al.
(2005)

Prospective
case series

ITI

PPD > 5 plus BOP+/


SUP

812 yrs

24 instances of
peri-implantitis

Lee et al.
(2012)

Retrospective
case series

Straumann
TPS, SLA

PPD > 4 plus BOP+

50% PCP

8 yrs

Prospective
case series

Undisclosed

PPD > 3 plus


Bleeding index > 1

49% smok

6 m5 yrs

C: 37% PCP,
17% PHP
I: 27% PCP,
13% PHP
C: 3%
I: 1.4%

Periimplantitis as part of
biological complication.
Includes C from Bragger et al.
(2001)
54% for C with residual
pockets

Corbella
et al.
(2011)
Dierens
et al.
(2012)
Dvorak
et al.
(2011)

Crosssectional

C:
28
I:
150
C:
128
I:
258
C:
48
I:
103
C:
89
I:
160
C:
60
I:
117
C:
61
I:
244
C:
50
I: 59
C:
177
I:
828
C:
212
I:
578
C:
662
I:
3413
C:
62
I:
227

Branemark

BL > 3 threads plus


BOP+

Nobel

PPD > 5 plus BOP+


plus BL

Nobel, 3i,
Intra-lock

PPD > 4 plus BOP+/


SUP plus BL

Branemark

Progressive BL. No
composite disease
definition

Nobel,
Zimmer,
Mathys,
Straumann,
Friadent
ITI

PPD > 5 mm plus


pus or other sign of
infection plus
BL > 2 mm

53% PCP

5 yrs

C: 3%
I: 1%

SUP plus BL

29% smok

815 yrs

C: 19%
I: 17%

ITI

PPD > 4 plus BOP+/


SUP plus BL

15% PCP

10 yrs

C: nd
I: 29% PCP, 6%
PHP

Astra Tech,
Branemark,
Straumann, 3i

PPD > 4 or > 5 plus


BOP+/SUP plus BL

8.4 yrs

C: 1147%
I: 537%

Branemark

PPD > 4 plus BOP+/


SUP plus BL  3
threads

19% smok

Undisclosed

C: 12%
I: 7%

Ankylos

PPD > 4 plus BOP+/


SUP plus BL

19% smok,
72% PCP

211 yrs

C: 11%
I: nd

Straumann
TPS

Antibiotic/surgical
therapy according to
the CIST protocol

37% PCP

10 yrs

Straumann
SLA

PPD > 3 plus BOP+


plus BL > 3xSD of
repeated measures

36% smok,
68% PCP

5 yrs

C: 11% PHP,
27% moderate
PCP, 47% severe
PCP
C: nd
I: 6%

Crosssectional

Ferreira
et al.
(2006)

Crosssectional

Fransson
et al.
(2005)

Retrospective
case series

Gatti et al.
(2008)

Prospective
case series

Gruica
et al.
(2004)

Prospective
case series

Karoussis
et al.
(2003)

Prospective
case series

Koldsland
et al.
(2010)

Crosssectional

Maximo
et al.
(2008)

Prospective
case series

Rinke et al.
(2011)

Retrospective
case series

Roccuzzo
et al.
(2012)

Prospective
case series

Rodrigo
et al.
(2011)

Prospective
case series

70 |

C:
180
I:
292
C:
53
I:
112
C:
109
I:
372
C:
113
I:
374
C:
89
I: nd
C:
101
I:
228
C:
22
I: 68

Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776

26%
osteoporosis,
9%
osteopenia
14% PCP

Short mean observation time


(mean 18.3 m). Only full-arch
rehabilitations

1622 yrs

C: 6%
I: 5%

Available subset of 134 C with


166 single-tooth I

6 yrs

C: 24%
I: 13%

Includes only postmenopausal


women

Mean
loading
time
42.5 m
5 yrs

C: 9%
I: 7%

Periodontitis and diabetes


associated with increased risk
of peri-implantitis

C: 28%
I: 12%

Threshold level: position


located about 3 mm apical to
the abutment-fixture
junction

Heavy smok I: 40%, light smok


I: 17%, never and former
smok I: 13% I with
complications
Prevalence associated with
smok

Different levels of severity


assessed on C and I level

Smok and PCP C: 53%, nonsmok and PHP C: 3%

2012 John Wiley & Sons A/S

Mombelli et al  Epidemiology of peri-implantitis

Table 1. (continued)
Peri-implantitis
Incidence/
prevalence

Comments
Different levels of severity
assessed on C and I level

References

Study design

I type

Disease definition

Risk factors

Follow-up

RoosJansaker
et al.
(2006b)
Rutar et al.
(2001)

Retrospective
case series

C:
218
I:
999
C:
45
I: 64
C:
nd
I: 39
C:
55
I:
131
C:
46
I:
116
C:
112
I:
304

Branemark

BL  3 threads
following 1st year
plus BOP+/SUP

914 yrs

C: 16%
I: 7%

ITI

PPD > 4 plus BOP+/


SUP plus BL

26% smok,
no
maintenance
care
38% smok

510 yrs

C: nd
I: 23%

322 yrs

C: nd
I: 13%

Retrospective
case series

Schmidlin
et al.
(2010)
Simonis
et al.
(2010)

Retrospective
case series

Wahlstrom
et al.
(2010)

Retrospective
case series

Zetterqvist
et al.
(2010)

Prospective
RCT

Retrospective
case series

PPD > 5 plus BOP+/


SUP plus BL
Straumann
TPS

PPD > 4 plus BOP+


plus BL  2.5 mm/
 3 threads

16% smok,
26% PCP

10 yrs

C: nd
I: 38% PCP,
11% PHP

Astra Tech
Nobel

Color and shape of


mucosa; PPD > 3
plus BOP+ plus
BL > 2 mm
PPD > 5 plus BOP+/
SUP plus plus BL > 5

11% smok,
all PCP

5 yrs

C: 4%
I: nd

5 yrs

C: 1%
I: <1%

3i

80% teeth lost due to


periodontal disease, 29% C
mean bone loss 1/32/3 of
root length

Abbreviations:
BL: Bone loss, BOP: Bleeding on probing, C: Case, I: Implant, smok: Smoking, nd: Not determined, PCP: Periodontally compromised patient, PHP: Periodontally 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 periimplant 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 diabetes were statistically associated with
increased risk for peri-implantitis.
Study 8 (Fransson et al. 2005): Radiographs
of 662 subjects with 3413 implants, supporting 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 probability for subjects to exhibit bone loss was
not influenced by age, gender, type of construction, function time, or maxillary/mandibular position of the implants. The number
of implants per subject, however, had a significant impact. Peri-implantitis was not
explicitly identified on the basis of a composite disease definition. Some subjects with
progressive bone loss were further characterized into two additional publications: In a
subset of 82 subjects, implants with progressive bone loss were more likely to show
2012 John Wiley & Sons A/S

BOP+,
suppuration,
recession
and
PPD > 5 mm. Smokers had larger numbers of
affected implants than non-smokers (Fransson et al. 2008). In 182 subjects, 419 of 1070
examined implants exhibited peri-implantitis-associated vertical bone loss > 2 mm.
The proportion of affected implants varied
between 30% and 52% in different jaw positions and the most common position was the
lower front region (Fransson et al. 2009).
Study 9 (Gatti et al. 2008): Sixty-two partially edentulous patients were consecutively
enrolled in this study. One hundred and
twenty-nine implants were placed in 26
patients with a history of severe periodontitis, 26 implants in seven subjects with a history 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-implantitis, 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 periimplant 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 suppuration from the peri-implant sulcus, development of a fistula, or peri-implantitis with
radiologic bone loss. Fifty-one implants in 34
patients showed late infectious biologic complications. 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 periodontal therapy. Eight subjects with a history of
chronic periodontitis lost 2 of 21 implants,
the remaining 45 periodontally health subjects lost 3 of 91 implants. When peri-implantitis 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 diagnosed 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 subjects were examined 8.4 years (SD: 4.6 years)
after functional loading. Peri-implantitis was
assessed using the following criteria: clinical

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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 combinations 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 inflammation and detectable loss of bone). The periimplant tissues of 249 (71%) implants were
judged to be inflamed (mBI score > 0 and/or
BOP or suppuration). This concerned 88 subjects (82%). Supplementing information on
the same patients was provided in an additional 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 retrospective 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 hundred 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 undisclosed. 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 prevalence rate of peri-implantitis, defined as
PPD > 4 mm, BOP+ and/or pus, with radiographic 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 prevalence was 3% in non-smokers and 53% in
smokers with periodontal history.

72 |

Study 16 (Roccuzzo et al. 2012): One hundred and one partially edentulous subjects
were examined 10 years after implant placement 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 individualized supportive periodontal therapy program.
The diagnosis and treatment of peri-implant
biological complications was carried out
according to cumulative interceptive supportive therapy (CIST) (Mombelli & Lang 1998).
Eighteen implants were removed due to biological complications (two, seven, nine
implants in the three groups, respectively).
During the 10 years, antibiotic and/or surgical 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 percentage 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 radiographical variables were recorded in 22 implant
patients of a private clinic. Patients were not
included if presenting with untreated periodontitis, inappropriate periodontal maintenance, 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 complications: mucositis (PPD > 3 mm, BOP+,
without significant bone loss) was diagnosed 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 immediately treated according to the CIST protocol, with success in all cases except one,
where one delayed implant showed signs of
persisting peri-implantitis (deep PPD and progressing loss of bone).
Study 18 (Roos-Jansaker et al. 2006a,b,c):
Two hundred and eighteen subjects with 999
implants (71% partially edentulous, 26% current smokers) were examined clinically and

Clin. Oral Implants Res. 23(Suppl. 6), 2012/6776

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 radiographic 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 function) 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 partially 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 examination. During this time, nine implants experienced 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 protocol. 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): Thirtynine single crowns on implants were reexamined 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

Mombelli et al  Epidemiology of peri-implantitis

and radiographic examination. The survival


rate at 10 years was 89%. Fourteen implants
were lost due to the presence of a periimplant 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-implantitis 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-implantitis was diagnosed on the basis of the color
and shape of the peri-implant mucosa, bleeding 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 prospective, 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 radiological 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 unavailable. 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 representative of the general target population for oral
2012 John Wiley & Sons A/S

implant therapy. Where an accurate documentation 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 vertical 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 transient 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; RoosJansaker 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 periodontal 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 presence of gingival inflammation in periodontally healthy subjects (Lang et al. 1991) as
well as in successfully treated patients without residual disease (Karayiannis et al. 1992).
The BOP+ is furthermore a poor prognosticator of future periodontal attachment loss
(Claffey & Egelberg 1995). Whether or not
bleeding upon peri-implant probing is associated with an increased risk for peri-implantitis 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 partially edentulous patients enrolled in a maintenance 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 uncontrollable situation. In another study 73% of 212
patients showed BOP, but only 9% were diagnosed 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

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 inappropriate to draw inferences on the prevalence of
peri-implantitis from the frequency of bleeding 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 implantation but this statement needs to be taken
with caution as the individual reported figures are rather variable, not easily comparable and not suitable for meta-analysis.
Factors that have been shown to affect prevalence figures are the disease definition and
the threshold for peri-implantitis, and differences in the composition of study populations.
The influence of differences in disease definition has been mentioned above. Roos-Jansaker et al. (2006b) explored the prevalence of
peri-implantitis using various composite disease definitions. This study concerned twopiece implants that are known for a systemimmanent non-infectious early bone resorption processes taking place shortly after abutment connection (Adell et al. 1981). If 48%
of the implants had a PPD > 3 mm and were
BOP+ irrespective of bone level, peri-implantitis, defined as bone loss  1.8 mm compared 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% depending 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 populations 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 associated with a higher prevalence of peri-implantitis. In four studies this issue was
specifically addressed (Karoussis et al. 2003;
Simonis et al. 2010; Lee et al. 2012; Roccuzzo et al. 2012). Peri-implantitis was
detected more than twice as frequently in
periodontally compromised than in periodontally healthy subjects in these studies.

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Mombelli et al  Epidemiology of peri-implantitis

Other plausible factors that could affect


the incidence of peri-implantitis relate to differences in treatment philosophy and methods 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 progression of peri-implantitis may be slow. It is
therefore impossible to exactly determine the
onset of peri-implantitis and challenging to

identify initial cases with high specificity.


On the other hand, if the disease evolves
slowly and gradually, it is of utmost importance that the infection can be intercepted
early to prevent massive damage of periimplant tissues. In modern dental care systems that include individualized regular
maintenance, cases of advanced peri-implantitis should be seen rarely, as they are intercepted at an earlier stage. Patients of the
reviewed studies have or have not been
included in a maintenance care program. The
diagnosis and treatment of peri-implant biological complications was carried out according to CIST in four studies (Rutar et al. 2001;
Bragger et al. 2005; Roccuzzo et al. 2012;
Rodrigo et al. 2011). In all these studies,
interceptive therapy for symptoms of periimplant mucositis or peri-implantitis was

necessary from time to time but catastrophic


cases of advanced peri-implant pathology
were rare. In an additional study where the
patient-related prevalence rate of peri-implantitis was 11%, no peri-implant disease was
diagnosed in non-smoking patients with a
good compliance after treatment and without
a history of periodontitis (Rinke et al. 2011).
To gain the full picture of the epidemiology
of peri-implantitis with all its clinical and
economical implications, it will be necessary
in future studies to assess how much subsequent treatment is generated by placing
implants, including prophylaxis, treatment of
mucositis and peri-implantitis, and therapy
after implant failure. Thus, there is a need
for monitoring implant patients longitudinally in view of a potential occurrence of
peri-implantitis.

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